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  • 1
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    An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome (2019)
    American Association for the Advancement of Science
    In:  EPIC3Science Advances, American Association for the Advancement of Science, 5(4), ISSN: 2375-2548
    Details
    Publication Date: 2020-02-12
    Description: Dinoflagellates are microbial eukaryotes that have exceptionally large nuclear genomes; however, their organelle genomes are small and fragmented and contain fewer genes than those of other eukaryotes. The genus Amoebophrya (Syndiniales) comprises endoparasites with high genetic diversity that can infect other dinoflagellates, such as those forming harmful algal blooms (e.g., Alexandrium). We sequenced the genome (~100 Mb) of Amoebophrya ceratii to investigate the early evolution of genomic characters in dinoflagellates. The A. ceratii genome encodes almost all essential biosynthetic pathways for self-sustaining cellular metabolism, suggesting a limited dependency on its host. Although dinoflagellates are thought to have descended from a photosynthetic ancestor, A. ceratii appears to have completely lost its plastid and nearly all genes of plastid origin. Functional mitochondria persist in all life stages of A. ceratii, but we found no evidence for the presence of a mitochondrial genome. Instead, all mitochondrial proteins appear to be lost or encoded in the A. ceratii nucleus.
    Repository Name: EPIC Alfred Wegener Institut
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  • 2
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    Different iron storage strategies among bloom-forming diatoms (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2018. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 115(52), (2018): E12275-E12284. doi: 10.1073/pnas.1805243115.
    Description: Diatoms are prominent eukaryotic phytoplankton despite being limited by the micronutrient iron in vast expanses of the ocean. As iron inputs are often sporadic, diatoms have evolved mechanisms such as the ability to store iron that enable them to bloom when iron is resupplied and then persist when low iron levels are reinstated. Two iron storage mechanisms have been previously described: the protein ferritin and vacuolar storage. To investigate the ecological role of these mechanisms among diatoms, iron addition and removal incubations were conducted using natural phytoplankton communities from varying iron environments. We show that among the predominant diatoms, Pseudo-nitzschia were favored by iron removal and displayed unique ferritin expression consistent with a long-term storage function. Meanwhile, Chaetoceros and Thalassiosira gene expression aligned with vacuolar storage mechanisms. Pseudo-nitzschia also showed exceptionally high iron storage under steady-state high and low iron conditions, as well as following iron resupply to iron-limited cells. We propose that bloom-forming diatoms use different iron storage mechanisms and that ferritin utilization may provide an advantage in areas of prolonged iron limitation with pulsed iron inputs. As iron distributions and availability change, this speculated ferritin-linked advantage may result in shifts in diatom community composition that can alter marine ecosystems and biogeochemical cycles.
    Description: We thank the captain and crew of the R/V Melville and the CCGS J. P. Tully as well as the participants of the IRNBRU (MV1405) cruise for the California-based data, particularly K. Ellis [University of North Carolina (UNC)], T. Coale (University of California, San Diego), F. Kuzminov (Rutgers), H. McNair [University of California, Santa Barbara (UCSB)], and J. Jones (UCSB). W. Burns (UNC), S. Haines (UNC), and S. Bargu (Louisiana State University) assisted with sample processing and analysis. This work was funded by the National Science Foundation Grants OCE-1334935 (to A.M.), OCE-1334632 (to B.S.T.), OCE-1333929 (to K.T.), OCE-1334387 (to M.A.B.), OCE-1259776 (to K.W.B), and DGE-1650116 (Graduate Research Fellowship to R.H.L).
    Description: 2019-06-11
    Keywords: phytoplankton ; iron limitation ; Pseudo-nitzschia ; ferritin ; metatranscriptomics
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  • 3
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    Agreement between reconstructed and modeled boreal precipitation of the Last Interglacial (2019)
    American Association for the Advancement of Science
    In:  EPIC3Science Advances, American Association for the Advancement of Science, 5(11), pp. eaax7047, ISSN: 2375-2548
    Details
    Publication Date: 2019-11-25
    Description: The last extended time period when climate may have been warmer than today was during the Last Interglacial (LIG; ca. 129 to 120 thousand years ago). However, a global view of LIG precipitation is lacking. Here, seven new LIG climate models are compared to the first global database of proxies for LIG precipitation. In this way, models are assessed in their ability to capture important hydroclimatic processes during a different climate. The models can reproduce the proxy-based positive precipitation anomalies from the preindustrial period over much of the boreal continents. Over the Southern Hemisphere, proxy-model agreement is partial. In models, LIG boreal monsoons have 42% wider area than in the preindustrial and produce 55% more precipitation and 50% more extreme precipitation. Austral monsoons are weaker. The mechanisms behind these changes are consistent with stronger summer radiative forcing over boreal high latitudes and with the associated higher temperatures during the LIG.
    Repository Name: EPIC Alfred Wegener Institut
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  • 4
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    Geodetic measurements reveal similarities between Last Glacial Maximum and present-day mass loss from the Greenland ice sheet (2016)
    American Association for the Advancement of Science
    In:  EPIC3Science Advances, American Association for the Advancement of Science, 2(9), pp. e1600931
    Details
    Publication Date: 2022-06-20
    Description: Accurate quantification of the millennial-scale mass balance of the Greenland ice sheet (GrIS) and its contribution to global sea-level rise remain challenging because of sparse in situ observations in key regions. Glacial isostatic adjustment (GIA) is the ongoing response of the solid Earth to ice and ocean load changes occurring since the Last Glacial Maximum (LGM; ~21 thousand years ago) and may be used to constrain the GrIS deglaciation history. We use data from the Greenland Global Positioning System network to directly measure GIA and estimate basin-wide mass changes since the LGM. Unpredicted, large GIA uplift rates of +12 mm/year are found in southeast Greenland. These rates are due to low upper mantle viscosity in the region, from when Greenland passed over the Iceland hot spot about 40 million years ago. This region of concentrated soft rheology has a profound influence on reconstructing the deglaciation history of Greenland. We reevaluate the evolution of the GrIS since LGM and obtain a loss of 1.5-m sea-level equivalent from the northwest and southeast. These same sectors are dominating modern mass loss. We suggest that the present destabilization of these marine-based sectors may increase sea level for centuries to come. Our new deglaciation history and GIA uplift estimates suggest that studies that use the Gravity Recovery and Climate Experiment satellite mission to infer present-day changes in the GrIS may have erroneously corrected for GIA and underestimated the mass loss by about 20 gigatons/year.
    Repository Name: EPIC Alfred Wegener Institut
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  • 5
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    A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 116(36), (2019): 17934-17942, doi:10.1073/pnas.1910121116.
    Description: Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because dinoflagellate plastids have repeatedly been reduced, lost, and replaced by new plastids, leading to a spectrum of ages and integration levels. Here we describe deep-transcriptomic analyses of the Antarctic Ross Sea dinoflagellate (RSD), which harbors long-term but temporary kleptoplasts stolen from haptophyte prey, and is closely related to dinoflagellates with fully integrated plastids derived from different haptophytes. In some members of this lineage, called the Kareniaceae, their tertiary haptophyte plastids have crossed a tipping point to stable integration, but RSD has not, and may therefore reveal the order of events leading up to endosymbiotic integration. We show that RSD has retained its ancestral secondary plastid and has partitioned functions between this plastid and the kleptoplast. It has also obtained genes for kleptoplast-targeted proteins via horizontal gene transfer (HGT) that are not derived from the kleptoplast lineage. Importantly, many of these HGTs are also found in the related species with fully integrated plastids, which provides direct evidence that genetic integration preceded organelle fixation. Finally, we find that expression of kleptoplast-targeted genes is unaffected by environmental parameters, unlike prey-encoded homologs, suggesting that kleptoplast-targeted HGTs have adapted to posttranscriptional regulation mechanisms of the host.
    Description: We are grateful to Martin Kolisko and Fabien Burki for helpful discussion about and comments on the phylogenetic analysis; and Filip Husnik and Vittorio Boscaro for valuable comments on the manuscript. This work was supported by a grant from the National Science Foundation to R.J.G. and P.J.K. (PLR-1341362) and from the Natural Sciences and Engineering Research Council of Canada to P.J.K. (RGPIN-2014-03994).
    Description: 2020-02-19
    Keywords: plastid endosymbiosis ; kleptoplasty ; dinoflagellates ; plastid integration
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  • 6
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    NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Diaz, J. M., Plummer, S., Hansel, C. M., Andeer, P. F., Saito, M. A., & McIlvin, M. R. NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica. Proceedings of the National Academy of Sciences of the United States of America, 116 (33), (2019): 16448-16453, doi: 10.1073/pnas.1821233116.
    Description: Reactive oxygen species (ROS) like superoxide drive rapid transformations of carbon and metals in aquatic systems and play dynamic roles in biological health, signaling, and defense across a diversity of cell types. In phytoplankton, however, the ecophysiological role(s) of extracellular superoxide production has remained elusive. Here, the mechanism and function of extracellular superoxide production by the marine diatom Thalassiosira oceanica are described. Extracellular superoxide production in T. oceanica exudates was coupled to the oxidation of NADPH. A putative NADPH-oxidizing flavoenzyme with predicted transmembrane domains and high sequence similarity to glutathione reductase (GR) was implicated in this process. GR was also linked to extracellular superoxide production by whole cells via quenching by the flavoenzyme inhibitor diphenylene iodonium (DPI) and oxidized glutathione, the preferred electron acceptor of GR. Extracellular superoxide production followed a typical photosynthesis-irradiance curve and increased by 30% above the saturation irradiance of photosynthesis, while DPI significantly impaired the efficiency of photosystem II under a wide range of light levels. Together, these results suggest that extracellular superoxide production is a byproduct of a transplasma membrane electron transport system that serves to balance the cellular redox state through the recycling of photosynthetic NADPH. This photoprotective function may be widespread, consistent with the presence of putative homologs to T. oceanica GR in other representative marine phytoplankton and ocean metagenomes. Given predicted climate-driven shifts in global surface ocean light regimes and phytoplankton community-level photoacclimation, these results provide implications for future ocean redox balance, ecological functioning, and coupled biogeochemical transformations of carbon and metals.
    Description: This work was supported by a postdoctoral fellowship from the Ford Foundation (to J.M.D.), the National Science Foundation (NSF) under grants OCE 1225801 (to J.M.D.) and OCE 1246174 (to C.M.H.), a Junior Faculty Seed Grant from the University of Georgia Research Foundation (to J.M.D.), and a National Science Foundation Graduate Research Fellowship (to S.P.). The FIRe was purchased through a NSF equipment improvement grant (1624593).The authors thank Melissa Soule for assistance with LC/MS/MS analysis of peptide samples.
    Keywords: Reactive oxygen species ; Photosynthesis ; Oxidative stress ; Biogeochemistry
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  • 7
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    Rapid mixing and exchange of deep-ocean waters in an abyssal boundary current. (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116(27), (2019): 13233-13238, doi: 10.1073/pnas.1904087116.
    Description: The overturning circulation of the global ocean is critically shaped by deep-ocean mixing, which transforms cold waters sinking at high latitudes into warmer, shallower waters. The effectiveness of mixing in driving this transformation is jointly set by two factors: the intensity of turbulence near topography and the rate at which well-mixed boundary waters are exchanged with the stratified ocean interior. Here, we use innovative observations of a major branch of the overturning circulation—an abyssal boundary current in the Southern Ocean—to identify a previously undocumented mixing mechanism, by which deep-ocean waters are efficiently laundered through intensified near-boundary turbulence and boundary–interior exchange. The linchpin of the mechanism is the generation of submesoscale dynamical instabilities by the flow of deep-ocean waters along a steep topographic boundary. As the conditions conducive to this mode of mixing are common to many abyssal boundary currents, our findings highlight an imperative for its representation in models of oceanic overturning.
    Description: The DynOPO project is supported by the UK Natural Environment Research Council (grants NE/K013181/1 and NE/K012843/1) and the US National Science Foundation (grants OCE-1536453 and OCE-1536779). A.C.N.G. acknowledges the support of the Royal Society and the Wolfson Foundation. S.L. acknowledges the support of award NA14OAR4320106 from the National Oceanic and Atmospheric Administration, US Department of Commerce. The statements, findings, conclusions, and recommendations are those of the authors, and do not necessarily reflect the views of the National Oceanic and Atmospheric Administration, or the US Department of Commerce. We are grateful to the scientific party, crew, and technicians on the RRS James Clark Ross for their hard work during data collection.
    Description: 2019-12-18
    Keywords: Ocean mixing ; Overturning circulation ; Submesoscale instabilities ; Turbulence
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  • 8
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    Ocean deoxygenation and zooplankton: Very small oxygen differences matter (2019)
    American Association for the Advancement of Science
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Science Advances, 4(12), (2018): eaau5180. doi: 10.1126/sciadv.aau5180.
    Description: Oxygen minimum zones (OMZs), large midwater regions of very low oxygen, are expected to expand as a result of climate change. While oxygen is known to be important in structuring midwater ecosystems, a precise and mechanistic understanding of the effects of oxygen on zooplankton is lacking. Zooplankton are important components of midwater food webs and biogeochemical cycles. Here, we show that, in the eastern tropical North Pacific OMZ, previously undescribed submesoscale oxygen variability has a direct effect on the distribution of many major zooplankton groups. Despite extraordinary hypoxia tolerance, many zooplankton live near their physiological limits and respond to slight (≤1%) changes in oxygen. Ocean oxygen loss (deoxygenation) may, thus, elicit major unanticipated changes to midwater ecosystem structure and function.
    Description: We thank the captain and crew of the R/V Sikuliaq (University of Alaska) and Scripps Institution of Oceanography for additional technical services. Thanks also to D. Ullman and D. Casagrande for Wire Flyer assistance; C. Matson and J. Calderwood for MOCNESS upgrades; S. Gordon (professional photographer, Open Boat Films LLC) for the photographs and movies; and A. Dymowska, J. Ivory, Y. Jin, J. McGreal, and N. Redmond for help at sea. Funding: Funding was provided by the NSF grants OCE1459243 (to K.F.W., C.R., and B.A.S.), OCE1458967 (to C.D.), DGE1244657 (to M.A.B.), and OCE1460819 (URI REU SURFO program to S.R.) plus funding from our respective institutions. Author contributions: K.F.W., B.A.S., C.R., and C.D. conceived the project. K.F.W. led the writing effort, with substantial contributions from all the authors. K.F.W. directed the MOCNESS component including zooplankton abundance and biomass quantification. B.A.S. directed the metabolic experiments and Tucker trawls. C.R. directed the Wire Flyer work. B.A.S., C.D., K.A.S.M., and M.A.B. developed the MI models. D.O., C.T.S., D.M., and S.R. processed and analyzed the zooplankton data. T.J.A. processed the MOCNESS hydrographic data. Competing interests: The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Extensive files of continuous hydrographic data from transects are available from C.R. (Wire Flyer) and K.F.W. (MOCNESS). Additional data related to this paper may be requested from the authors.
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  • 9
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    Formation of the Isthmus of Panama (2016)
    American Association for the Advancement of Science
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Science Advances 2 (2016): e1600883, doi:10.1126/sciadv.1600883.
    Description: The formation of the Isthmus of Panama stands as one of the greatest natural events of the Cenozoic, driving profound biotic transformations on land and in the oceans. Some recent studies suggest that the Isthmus formed many millions of years earlier than the widely recognized age of approximately 3 million years ago (Ma), a result that if true would revolutionize our understanding of environmental, ecological, and evolutionary change across the Americas. To bring clarity to the question of when the Isthmus of Panama formed, we provide an exhaustive review and reanalysis of geological, paleontological, and molecular records. These independent lines of evidence converge upon a cohesive narrative of gradually emerging land and constricting seaways, with formation of the Isthmus of Panama sensu stricto around 2.8 Ma. The evidence used to support an older isthmus is inconclusive, and we caution against the uncritical acceptance of an isthmus before the Pliocene.
    Description: This study was supported by the Smithsonian Tropical Research Institute to A.O., J.B.C.J., N.K., and H.A.L.; the NSF (EAR 1325683) to A.O., P.G.R.-D., and E.L.G.; the National System of Investigators to A.O.; the Secretaría Nacional de Ciencia, Tecnología e Innovación (Panamá) to A.O., H.A.L., and S.E.C.; the U.S. Geological Survey to R.F.S.; and the Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina) to A.L.C., G.M.G., E.S., and L.S.
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  • 10
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    On the occurrence of cytochrome P450 in viruses (2019)
    National Academy of Sciences
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    Publication Date: 2022-05-26
    Description: Author Posting. © The Author(s), 2019. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 116(25), (2019):12343-12352, doi:10.1073/pnas.1901080116.
    Description: Genes encoding cytochrome P450 (CYP; P450) enzymes occur widely in the Archaea, Bacteria, and Eukarya, where they play important roles in metabolism of endogenous regulatory molecules and exogenous chemicals. We now report that genes for multiple and unique P450s occur commonly in giant viruses in the Mimiviridae, Pandoraviridae, and other families in the proposed order Megavirales. P450 genes were also identified in a herpesvirus (Ranid herpesvirus 3) and a phage (Mycobacterium phage Adler). The Adler phage P450 was classified as CYP102L1, and the crystal structure of the open form was solved at 2.5 Å. Genes encoding known redox partners for P450s (cytochrome P450 reductase, ferredoxin and ferredoxin reductase, and flavodoxin and flavodoxin reductase) were not found in any viral genome so far described, implying that host redox partners may drive viral P450 activities. Giant virus P450 proteins share no more than 25% identity with the P450 gene products we identified in Acanthamoeba castellanii, an amoeba host for many giant viruses. Thus, the origin of the unique P450 genes in giant viruses remains unknown. If giant virus P450 genes were acquired from a host, we suggest it could have been from an as yet unknown and possibly ancient host. These studies expand the horizon in the evolution and diversity of the enormously important P450 superfamily. Determining the origin and function of P450s in giant viruses may help to discern the origin of the giant viruses themselves.
    Description: We thank Dr. David Nes (Texas Tech University) for providing sterols and Dr. Matthieu Legendre and Dr. Chantal Abergel (CNRS, Marseille) for access to the P. celtis sequences. Drs. Irina Arkhipova, Mark Hahn, Judith Luborsky, and Ann Bucklin commented on the manuscript. The research was supported by a USA-UK Fulbright Scholarship and a Royal Society grant (to D.C.L.), the Boston University Superfund Research Program [NIH Grant 5P42ES007381 (to J.J.S. and J.V.G.) and NIH Grant 5U41HG003345 (to J.V.G.)], the European Regional Development Fund and Welsh Government Project BEACON (S.L.K.), the Woods Hole Center for Oceans and Human Health [NIH Grant P01ES021923 and National Science Foundation Grant OCE-1314642 (to J.J.S.)], and NIH Grant R01GM53753 (to T.L.P.).
    Description: 2019-12-05
    Keywords: cytochrome P450 ; virus ; evolution ; domains of life ; redox partner
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  • 11
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    Archaea dominate oxic subseafloor communities over multimillion-year time scales (2019)
    American Association for the Advancement of Science
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).. The definitive version was published in Vuillemin, A., Wankel, S. D., Coskun, Ö. K., Magritsch, T., Vargas, S., Estes, E. R., Spivack, A. J., Smith, D. C., Pockalny, R., Murray, R. W., D'Hondt, S., & Orsi, W. D. Archaea dominate oxic subseafloor communities over multimillion-year time scales. Science Advances, 5(6), (2019): eaaw4108, doi: 10.1126/sciadv.aaw4108.
    Description: Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.
    Description: This work was supported primarily by the Deutsche Forschungsgemeinschaft (DFG) project OR 417/1-1 granted to W.D.O. Preliminary work was supported by the Center for Dark Energy Biosphere Investigations project OCE-0939564 also granted to W.D.O. Publication of the manuscript was supported by the LMU Mentoring Program. The expedition was funded by the US National Science Foundation through grant NSF-OCE-1433150 to A.J.S, S.D., and R.P. R.W.M. led the expedition. This is a contribution of the Deep Carbon Observatory (DCO). S.D.W. acknowledges partial support from NASA Exobiology (NNX15AM04G). This is Center for Dark Energy Biosphere Investigations (C-DEBI) publication number 463. Portions of this material are based on work supported while R.W.M. was serving at the National Science Foundation. A portion of this work was performed as part of the LMU Masters Program “Geobiology and Paleobiology” (MGAP).
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  • 12
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    Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116 (35), (2019): 17187-17192, doi:10.1073/pnas.1903067116.
    Description: Mesoscale eddies are critical components of the ocean’s “internal weather” system. Mixing and stirring by eddies exerts significant control on biogeochemical fluxes in the open ocean, and eddies may trap distinctive plankton communities that remain coherent for months and can be transported hundreds to thousands of kilometers. Debate regarding how and why predators use fronts and eddies, for example as a migratory cue, enhanced forage opportunities, or preferred thermal habitat, has been ongoing since the 1950s. The influence of eddies on the behavior of large pelagic fishes, however, remains largely unexplored. Here, we reconstruct movements of a pelagic predator, the blue shark (Prionace glauca), in the Gulf Stream region using electronic tags, earth-observing satellites, and data-assimilating ocean forecasting models. Based on 〉2,000 tracking days and nearly 500,000 high-resolution time series measurements collected by 15 instrumented individuals, we show that blue sharks seek out the interiors of anticyclonic eddies where they dive deep while foraging. Our observations counter the existing paradigm that anticyclonic eddies are unproductive ocean “deserts” and suggest anomalously warm temperatures in these features connect surface-oriented predators to the most abundant fish community on the planet in the mesopelagic. These results also shed light on the ecosystem services provided by mesopelagic prey. Careful consideration will be needed before biomass extraction from the ocean twilight zone to avoid interrupting a key link between planktonic production and top predators. Moreover, robust associations between targeted fish species and oceanographic features increase the prospects for effective dynamic ocean management.
    Description: We thank D. McGillicuddy, G. Lawson, and G. Flierl for helpful discussions while developing this work and 2 anonymous reviewers whose feedback significantly improved the manuscript. We also thank C. Fischer and the OCEARCH team for their support of this research. This work was funded by awards to C.D.B. from the Martin Family Society of Fellows for Sustainability Fellowship at the Massachusetts Institute of Technology; the Grassle Fellowship and Ocean Venture Fund at the Woods Hole Oceanographic Institution; and the National Aeronatics and Space Administration (NASA) Earth and Space Science Fellowship. C.D.B. and P.G. acknowledge support from the NASA New Investigator Program Award 80NSSC18K0757, and P.G. acknowledges support from NSF Award OCE-1558809. This research is partially supported by funding to S.R.T. as part of the Audacious Project, a collaborative endeavor, housed at TED. We thank donors to the Woods Hole Oceanographic Institution (WHOI) ProjectWHOI crowdfunding campaign: The Secret Lives of Sharks. Computational support was provided by the Amazon Web Services Cloud Credits for Research program. Funding for the development of HYCOM has been provided by the National Ocean Partnership Program and the Office of Naval Research.
    Description: 2020-02-06
    Keywords: remote sensing ; oceanographic model ; satellite telemetry ; marine predator ; mesopelagic
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  • 13
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    A productivity collapse to end earth's great oxidation (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116 (35), (2019): 17207-17212, doi:10.1073/pnas.1900325116.
    Description: It has been hypothesized that the overall size of—or efficiency of carbon export from—the biosphere decreased at the end of the Great Oxidation Event (GOE) (ca. 2,400 to 2,050 Ma). However, the timing, tempo, and trigger for this decrease remain poorly constrained. Here we test this hypothesis by studying the isotope geochemistry of sulfate minerals from the Belcher Group, in subarctic Canada. Using insights from sulfur and barium isotope measurements, combined with radiometric ages from bracketing strata, we infer that the sulfate minerals studied here record ambient sulfate in the immediate aftermath of the GOE (ca. 2,018 Ma). These sulfate minerals captured negative triple-oxygen isotope anomalies as low as ∼ −0.8‰. Such negative values occurring shortly after the GOE require a rapid reduction in primary productivity of 〉80%, although even larger reductions are plausible. Given that these data imply a collapse in primary productivity rather than export efficiency, the trigger for this shift in the Earth system must reflect a change in the availability of nutrients, such as phosphorus. Cumulatively, these data highlight that Earth’s GOE is a tale of feast and famine: A geologically unprecedented reduction in the size of the biosphere occurred across the end-GOE transition.
    Description: Olivia M. J. Dagnaud assisted during fieldwork. S. V. Lalonde and E. A. Sperling provided helpful comments on an early version of the manuscript. We thank N. J. Planavsky and an anonymous reviewer for their constructive feedback. M.S.W.H. was supported by an NSERC PGS-D and student research grants from National Geographic, the APS Lewis and Clark Fund, Northern Science Training Program, McGill University Graduate Research Enhancement and Travel Awards, Geological Society of America, Mineralogical Association of Canada, and Stanford University. P.W.C. acknowledges support from the University of Colorado Boulder, the Agouron Institute Geobiology postdoctoral Fellowship program, a Natural Sciences and Engineering Council of Canada Postgraduate Scholarship–Doctoral Program scholarship, and the NSTP. Y.P. was supported by the Strategic Priority Research Program of CAS (XDB26000000). T.J.H. thanks Maureen E. Auro for laboratory assistance and the NSF for supporting isotope research in the NIRVANA Labs.
    Description: 2020-02-12
    Keywords: Proterozoic ; primary productivity ; Great Oxidation Event ; triple-oxygen isotopes ; nutrient limitation
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    Sustained wood burial in the Bengal Fan over the last 19 My (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116(45), (2019): 22518-22525, doi:10.1073/pnas.1913714116.
    Description: The Ganges–Brahmaputra (G-B) River system transports over a billion tons of sediment every year from the Himalayan Mountains to the Bay of Bengal and has built the world’s largest active sedimentary deposit, the Bengal Fan. High sedimentation rates drive exceptional organic matter preservation that represents a long-term sink for atmospheric CO2. While much attention has been paid to organic-rich fine sediments, coarse sediments have generally been overlooked as a locus of organic carbon (OC) burial. However, International Ocean Discovery Program Expedition 354 recently discovered abundant woody debris (millimeter- to centimeter-sized fragments) preserved within the coarse sediment layers of turbidite beds recovered from 6 marine drill sites along a transect across the Bengal Fan (∼8°N, ∼3,700-m water depth) with recovery spanning 19 My. Analysis of bulk wood and lignin finds mostly lowland origins of wood delivered episodically. In the last 5 My, export included C4 plants, implying that coarse woody, lowland export continued after C4 grassland expansion, albeit in reduced amounts. Substantial export of coarse woody debris in the last 1 My included one wood-rich deposit (∼0.05 Ma) that encompassed coniferous wood transported from the headwaters. In coarse layers, we found on average 0.16 weight % OC, which is half the typical biospheric OC content of sediments exported by the modern G-B Rivers. Wood burial estimates are hampered by poor drilling recovery of sands. However, high-magnitude, low-frequency wood export events are shown to be a key mechanism for C burial in turbidites.
    Description: This work was funded by National Science Foundation Grants OCE-1401217 and COL-T354A55 to S.J.F. and OCE-1400805 to V.G. Graduate student participation in the project received support from University of Southern California Provost’s Fellowship to H.L. Samples were provided by the International Ocean Discovery Program. We are grateful for the efforts of the Expedition 354 Science Party, Carl Johnson, and Zongguang Liu. C.F.-L. and A.G. were supported by IODP-France. We thank Colin Osborne and Maria Vorontsova for helpful discussions.
    Description: 2020-04-21
    Keywords: carbon cycle ; wood ; lignin ; Himalaya ; Bengal Fan
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    Abiotic methane synthesis and serpentinization in olivine-hosted fluid inclusions (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 116(36), (2019): 17666-17672. doi:10.1073/pnas.1907871116.
    Description: The conditions of methane (CH4) formation in olivine-hosted secondary fluid inclusions and their prevalence in peridotite and gabbroic rocks from a wide range of geological settings were assessed using confocal Raman spectroscopy, optical and scanning electron microscopy, electron microprobe analysis, and thermodynamic modeling. Detailed examination of 160 samples from ultraslow- to fast-spreading midocean ridges, subduction zones, and ophiolites revealed that hydrogen (H2) and CH4 formation linked to serpentinization within olivine-hosted secondary fluid inclusions is a widespread process. Fluid inclusion contents are dominated by serpentine, brucite, and magnetite, as well as CH4(g) and H2(g) in varying proportions, consistent with serpentinization under strongly reducing, closed-system conditions. Thermodynamic constraints indicate that aqueous fluids entering the upper mantle or lower oceanic crust are trapped in olivine as secondary fluid inclusions at temperatures higher than ∼400 °C. When temperatures decrease below ∼340 °C, serpentinization of olivine lining the walls of the fluid inclusions leads to a near-quantitative consumption of trapped liquid H2O. The generation of molecular H2 through precipitation of Fe(III)-rich daughter minerals results in conditions that are conducive to the reduction of inorganic carbon and the formation of CH4. Once formed, CH4(g) and H2(g) can be stored over geological timescales until extracted by dissolution or fracturing of the olivine host. Fluid inclusions represent a widespread and significant source of abiotic CH4 and H2 in submarine and subaerial vent systems on Earth, and possibly elsewhere in the solar system.
    Description: We are indebted to J. Eckert for his support with FE-EMPA; to K. Aquinho and E. Codillo for providing samples from Zambales; to K. Aquinho for Raman analysis of some of the samples from Zambales and Mt. Dent; to H. Dick for providing access to his thin section collection; to the curators of the IODP core repositories for providing access to Ocean Drilling Program (ODP) and Integrated Ocean Drilling Program (IODP) samples; and to the captains and crews of the many cruises without whom the collection of these samples would not have been possible. Reviews by Peter Kelemen and an anonymous referee greatly improved this manuscript. This study is supported with funds provided by the National Science Foundation (NSF-OCE Award 1634032 to F.K. and J.S.S.).
    Description: 2020-02-19
    Keywords: Abiotic methane ; Fluid inclusions ; Serpentinization ; Methane seeps ; Carbon cycling
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    Complete arsenic-based respiratory cycle in the marine microbial communities of pelagic oxygen-deficient zones. (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © The Author(s), 2019. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 116(20), (2019):9925-9930, doi:10.1073/pnas.1818349116.
    Description: Microbial capacity to metabolize arsenic is ancient, arising in response to its pervasive presence in the environment, which was largely in the form of As(III) in the early anoxic ocean. Many biological arsenic transformations are aimed at mitigating toxicity; however, some microorganisms can respire compounds of this redox-sensitive element to reap energetic gains. In several modern anoxic marine systems concentrations of As(V) are higher relative to As(III) than what would be expected from the thermodynamic equilibrium, but the mechanism for this discrepancy has remained unknown. Here we present evidence of a complete respiratory arsenic cycle, consisting of dissimilatory As(V) reduction and chemoautotrophic As(III) oxidation, in the pelagic ocean. We identified the presence of genes encoding both subunits of the respiratory arsenite oxidase AioA and the dissimilatory arsenate reductase ArrA in the Eastern Tropical North Pacific (ETNP) oxygen-deficient zone (ODZ). The presence of the dissimilatory arsenate reductase gene arrA was enriched on large particles (〉30 um), similar to the forward bacterial dsrA gene of sulfate-reducing bacteria, which is involved in the cryptic cycling of sulfur in ODZs. Arsenic respiratory genes were expressed in metatranscriptomic libraries from the ETNP and the Eastern Tropical South Pacific (ETSP) ODZ, indicating arsenotrophy is a metabolic pathway actively utilized in anoxic marine water columns. Together these results suggest arsenic-based metabolisms support organic matter production and impact nitrogen biogeochemical cycling in modern oceans. In early anoxic oceans, especially during periods of high marine arsenic concentrations, they may have played a much larger role.
    Description: We thank John Baross and Rika Anderson for helpful discussions and feedback on this project. We also thank the chief scientists of the research cruise, Al Devol and Bess Ward, as well as the captain and crew of the R/V Thomas G. Thompson. This work was supported through a NASA Earth and Space Sciences Graduate Research Fellowship to J.K.S. and National Science Foundation Grant OCE-1138368 (to G.R.).
    Description: 2019-10-29
    Keywords: Oxygen deficient zones ; Arsenic ; Chemoautotrophy ; Dissimilatory arsenate reduction ; Marine metagenome
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    Decadal trends in the ocean carbon sink (2019)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116 (24), (2019):11646-11651, doi:10.1073/pnas.1900371116.
    Description: Measurements show large decadal variability in the rate of CO2 accumulation in the atmosphere that is not driven by CO2 emissions. The decade of the 1990s experienced enhanced carbon accumulation in the atmosphere relative to emissions, while in the 2000s, the atmospheric growth rate slowed, even though emissions grew rapidly. These variations are driven by natural sources and sinks of CO2 due to the ocean and the terrestrial biosphere. In this study, we compare three independent methods for estimating oceanic CO2 uptake and find that the ocean carbon sink could be responsible for up to 40% of the observed decadal variability in atmospheric CO2 accumulation. Data-based estimates of the ocean carbon sink from pCO2 mapping methods and decadal ocean inverse models generally agree on the magnitude and sign of decadal variability in the ocean CO2 sink at both global and regional scales. Simulations with ocean biogeochemical models confirm that climate variability drove the observed decadal trends in ocean CO2 uptake, but also demonstrate that the sensitivity of ocean CO2 uptake to climate variability may be too weak in models. Furthermore, all estimates point toward coherent decadal variability in the oceanic and terrestrial CO2 sinks, and this variability is not well-matched by current global vegetation models. Reconciling these differences will help to constrain the sensitivity of oceanic and terrestrial CO2 uptake to climate variability and lead to improved climate projections and decadal climate predictions.
    Description: We thank Rebecca Wright and Erik Buitenhuis at University of East Anglia, Norwich, for providing updated runs from the NEMO-PlankTOM5 model. T.D. was supported by NSF Grant OCE-1658392. C.L.Q. thanks the UK Natural Environment Research Council for supporting the SONATA Project (Grant NE/P021417/1). P.L. was supported by the Max Planck Society for the Advancement of Science. J.H. was supported under Helmholtz Young Investigator Group Marine Carbon and Ecosystem Feedbacks in the Earth System (MarESys) Grant VH-NG-1301. S.B. and R.S. were supported by the H2020 project CRESCENDO “Coordinated Research in Earth Systems and Climate: Experiments, Knowledge, Dissemination and Outreach,” which received funding from the European Union’s Horizon 2020 research and innovation program under Grant No 641816. SOCAT is an international effort, endorsed by the International Ocean Carbon Coordination Project, the Surface Ocean-Lower Atmosphere Study, and the Integrated Marine Biosphere Research program, to deliver a uniformly quality-controlled surface ocean CO2 database. The many researchers and funding agencies responsible for the collection of data and quality control are thanked for their contributions to SOCAT.
    Description: 2019-11-28
    Keywords: Carbon dioxide ; Ocean carbon sink ; Terrestrial carbon sink ; Climate variability ; Carbon budget
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    Selective expression of mutant huntingtin during development recapitulates characteristic features of Huntington’s disease (2016)
    National Academy of Sciences
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    Publication Date: 2016-05-02
    Description: Recent studies have identified impairments in neural induction and in striatal and cortical neurogenesis in Huntington’s disease (HD) knock-in mouse models and associated embryonic stem cell lines. However, the potential role of these developmental alterations for HD pathogenesis and progression is currently unknown. To address this issue, we used BACHD:CAG-CreERT2 mice, which carry mutant huntingtin (mHtt) modified to harbor a floxed exon 1 containing the pathogenic polyglutamine expansion (Q97). Upon tamoxifen administration at postnatal day 21, the floxed mHtt-exon1 was removed and mHtt expression was terminated (Q97CRE). These conditional mice displayed similar profiles of impairments to those mice expressing mHtt throughout life: (i) striatal neurodegeneration, (ii) early vulnerability to NMDA-mediated excitotoxicity, (iii) impairments in motor coordination, (iv) temporally distinct abnormalities in striatal electrophysiological activity, and (v) altered corticostriatal functional connectivity and plasticity. These findings strongly suggest that developmental aberrations may play important roles in HD pathogenesis and progression.
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    Peptidoglycan hydrolase of an unusual cross-link cleavage specificity contributes to bacterial cell wall synthesis (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-02
    Description: Bacteria are surrounded by a protective exoskeleton, peptidoglycan (PG), a cross-linked mesh-like macromolecule consisting of glycan strands interlinked by short peptides. Because PG completely encases the cytoplasmic membrane, cleavage of peptide cross-links is a prerequisite to make space for incorporation of nascent glycan strands for its successful expansion during cell growth. In most bacteria, the peptides consist of l-alanine, d-glutamate, meso-diaminopimelic acid (mDAP) and d-alanine (d-Ala) with cross-links occurring either between d-Ala and mDAP or two mDAP residues. In Escherichia coli, the d-Ala−mDAP cross-links whose cleavage by specialized endopeptidases is crucial for expansion of PG predominate. However, a small proportion of mDAP−mDAP cross-links also exist, yet their role in the context of PG expansion or the hydrolase(s) capable of catalyzing their cleavage is not known. Here, we identified an ORF of unknown function, YcbK (renamed MepK), as an mDAP−mDAP cross-link cleaving endopeptidase working in conjunction with other elongation-specific endopeptidases to make space for efficient incorporation of nascent PG strands into the sacculus. E. coli mutants lacking mepK and another d-Ala−mDAP–specific endopeptidase (mepS) were synthetic sick, and the defects were abrogated by lack of l,d-transpeptidases, enzymes catalyzing the formation of mDAP cross-links. Purified MepK was able to cleave the mDAP cross-links of soluble muropeptides and of intact PG sacculi. Overall, this study describes a PG hydrolytic enzyme with a hitherto unknown substrate specificity that contributes to expansion of the PG sacculus, emphasizing the fundamental importance of cross-link cleavage in bacterial peptidoglycan synthesis.
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    Insight into the flagella type III export revealed by the complex structure of the type III ATPase and its regulator (2016)
    National Academy of Sciences
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    Publication Date: 2016-03-16
    Description: FliI and FliJ form the FliI6FliJ ATPase complex of the bacterial flagellar export apparatus, a member of the type III secretion system. The FliI6FliJ complex is structurally similar to the α3β3γ complex of F1-ATPase. The FliH homodimer binds to FliI to connect the ATPase complex to the flagellar base, but the details are unknown. Here we report the structure of the homodimer of a C-terminal fragment of FliH (FliHC2) in complex with FliI. FliHC2shows an unusually asymmetric homodimeric structure that markedly resembles the peripheral stalk of the A/V-type ATPases. The FliHC2–FliI hexamer model reveals that the C-terminal domains of the FliI ATPase face the cell membrane in a way similar to the F/A/V-type ATPases. We discuss the mechanism of flagellar ATPase complex formation and a common origin shared by the type III secretion system and the F/A/V-type ATPases.
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    Shockley–Queisser triangle predicts the thermodynamic efficiency limits of arbitrarily complex multijunction bifacial solar cells (2019)
    National Academy of Sciences
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    Publication Date: 2019-11-12
    Description: As monofacial, single-junction solar cells approach their fundamental limits, there has been significant interest in tandem solar cells in the presence of concentrated sunlight or tandem bifacial solar cells with back-reflected albedo. The bandgap sequence and thermodynamic efficiency limits of these complex cell configurations require sophisticated numerical calculation. Therefore, the analyses of specialized cases are scattered throughout the literature. In this paper, we show that a powerful graphical approach called the normalized “Shockley–Queisser (S-Q) triangle” (i.e., imp=1−vmp) is sufficient to calculate the bandgap sequence and efficiency limits of arbitrarily complex photovoltaic (PV) topologies. The results are validated against a wide variety of specialized cases reported in the literature and are accurate within a few percent. We anticipate that the widespread use of the S-Q triangle will illuminate the deeper physical principles and design trade-offs involved in the design of bifacial tandem solar cells under arbitrary concentration and series resistance.
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    Insulin signaling in the hippocampus and amygdala regulates metabolism and neurobehavior (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-14
    Description: Previous studies have shown that insulin and IGF-1 signaling in the brain, especially the hypothalamus, is important for regulation of systemic metabolism. Here, we develop mice in which we have specifically inactivated both insulin receptors (IRs) and IGF-1 receptors (IGF1Rs) in the hippocampus (Hippo-DKO) or central amygdala (CeA-DKO) by stereotaxic delivery of AAV-Cre into IRlox/lox/IGF1Rlox/loxmice. Consequently, both Hippo-DKO and CeA-DKO mice have decreased levels of the GluA1 subunit of glutamate AMPA receptor and display increased anxiety-like behavior, impaired cognition, and metabolic abnormalities, including glucose intolerance. Hippo-DKO mice also display abnormal spatial learning and memory whereas CeA-DKO mice have impaired cold-induced thermogenesis. Thus, insulin/IGF-1 signaling has common roles in the hippocampus and central amygdala, affecting synaptic function, systemic glucose homeostasis, behavior, and cognition. In addition, in the hippocampus, insulin/IGF-1 signaling is important for spatial learning and memory whereas insulin/IGF-1 signaling in the central amygdala controls thermogenesis via regulation of neural circuits innervating interscapular brown adipose tissue.
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    A fully resolved backbone phylogeny reveals numerous dispersals and explosive diversifications throughout the history of Asteraceae (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-17
    Description: The sunflower family, Asteraceae, comprises 10% of all flowering plant species and displays an incredible diversity of form. Asteraceae are clearly monophyletic, yet resolving phylogenetic relationships within the family has proven difficult, hindering our ability to understand its origin and diversification. Recent molecular clock dating has suggested a Cretaceous origin, but the lack of deep sampling of many genes and representative taxa from across the family has impeded the resolution of migration routes and diversifications that led to its global distribution and tremendous diversity. Here we use genomic data from 256 terminals to estimate evolutionary relationships, timing of diversification(s), and biogeographic patterns. Our study places the origin of Asteraceae at ∼83 MYA in the late Cretaceous and reveals that the family underwent a series of explosive radiations during the Eocene which were accompanied by accelerations in diversification rates. The lineages that gave rise to nearly 95% of extant species originated and began diversifying during the middle Eocene, coincident with the ensuing marked cooling during this period. Phylogenetic and biogeographic analyses support a South American origin of the family with subsequent dispersals into North America and then to Asia and Africa, later followed by multiple worldwide dispersals in many directions. The rapid mid-Eocene diversification is aligned with the biogeographic range shift to Africa where many of the modern-day tribes appear to have originated. Our robust phylogeny provides a framework for future studies aimed at understanding the role of the macroevolutionary patterns and processes that generated the enormous species diversity of Asteraceae.
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    Science, health, and cultural literacy in a rapidly changing communications landscape (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-15
    Description: There is a gap between how many scientists communicate and how most people understand and interpret messages. This article argues that the extensive science communications literature needs to be joined by the health literacy literature and anthropological work on cultural variations in hearing and understanding messages. Rapid changes and differences in how people in the United States get information are also discussed. Better understanding of how people get and perceive messages, and how access to information and to health services affects their behavior, should be an iterative and interdisciplinary effort. Community involvement in developing communication strategies is strongly encouraged.
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    A functional enrichment test for molecular convergent evolution finds a clear protein-coding signal in echolocating bats and whales (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-30
    Description: Distantly related species entering similar biological niches often adapt by evolving similar morphological and physiological characters. How much genomic molecular convergence (particularly of highly constrained coding sequence) contributes to convergent phenotypic evolution, such as echolocation in bats and whales, is a long-standing fundamental question. Like others, we find that convergent amino acid substitutions are not more abundant in echolocating mammals compared to their outgroups. However, we also ask a more informative question about the genomic distribution of convergent substitutions by devising a test to determine which, if any, of more than 4,000 tissue-affecting gene sets is most statistically enriched with convergent substitutions. We find that the gene set most overrepresented (q-value = 2.2e-3) with convergent substitutions in echolocators, affecting 18 genes, regulates development of the cochlear ganglion, a structure with empirically supported relevance to echolocation. Conversely, when comparing to nonecholocating outgroups, no significant gene set enrichment exists. For aquatic and high-altitude mammals, our analysis highlights 15 and 16 genes from the gene sets most affected by molecular convergence which regulate skin and lung physiology, respectively. Importantly, our test requires that the most convergence-enriched set cannot also be enriched for divergent substitutions, such as in the pattern produced by inactivated vision genes in subterranean mammals. Showing a clear role for adaptive protein-coding molecular convergence, we discover nearly 2,600 convergent positions, highlight 77 of them in 3 organs, and provide code to investigate other clades across the tree of life.
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    Tubulin lattice in cilia is in a stressed form regulated by microtubule inner proteins (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-16
    Description: Cilia, the hair-like protrusions that beat at high frequencies to propel a cell or move fluid around are composed of radially bundled doublet microtubules. In this study, we present a near-atomic resolution map of the Tetrahymena doublet microtubule by cryoelectron microscopy. The map demonstrates that the network of microtubule inner proteins weaves into the tubulin lattice and forms an inner sheath. From mass spectrometry data and de novo modeling, we identified Rib43a proteins as the filamentous microtubule inner proteins in the protofilament ribbon region. The Rib43a–tubulin interaction leads to an elongated tubulin dimer distance every 2 dimers. In addition, the tubulin lattice structure with missing microtubule inner proteins (MIPs) by sarkosyl treatment shows significant longitudinal compaction and lateral angle change between protofilaments. These results are evidence that the MIPs directly affect and stabilize the tubulin lattice. It suggests that the doublet microtubule is an intrinsically stressed filament and that this stress could be manipulated in the regulation of ciliary waveforms.
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    Interspecies analysis of MYC targets identifies tRNA synthetases as mediators of growth and survival in MYC-overexpressing cells (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-01
    Description: Aberrant MYC oncogene activation is one of the most prevalent characteristics of cancer. By overlapping datasets of Drosophila genes that are insulin-responsive and also regulate nucleolus size, we enriched for Myc target genes required for cellular biosynthesis. Among these, we identified the aminoacyl tRNA synthetases (aaRSs) as essential mediators of Myc growth control in Drosophila and found that their pharmacologic inhibition is sufficient to kill MYC-overexpressing human cells, indicating that aaRS inhibitors might be used to selectively target MYC-driven cancers. We suggest a general principle in which oncogenic increases in cellular biosynthesis sensitize cells to disruption of protein homeostasis.
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    Optimizing organic electrosynthesis through controlled voltage dosing and artificial intelligence (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-21
    Description: Organic electrosynthesis can transform the chemical industry by introducing electricity-driven processes that are more energy efficient and that can be easily integrated with renewable energy sources. However, their deployment is severely hindered by the difficulties of controlling selectivity and achieving a large energy conversion efficiency at high current density due to the low solubility of organic reactants in practical electrolytes. This control can be improved by carefully balancing the mass transport processes and electrocatalytic reaction rates at the electrode diffusion layer through pulsed electrochemical methods. In this study, we explore these methods in the context of the electrosynthesis of adiponitrile (ADN), the largest organic electrochemical process in industry. Systematically exploring voltage pulses in the timescale between 5 and 150 ms led to a 20% increase in production of ADN and a 250% increase in relative selectivity with respect to the state-of-the-art constant voltage process. Moreover, combining this systematic experimental investigation with artificial intelligence (AI) tools allowed us to rapidly discover drastically improved electrosynthetic conditions, reaching improvements of 30 and 325% in ADN production rates and selectivity, respectively. This powerful AI-enhanced experimental approach represents a paradigm shift in the design of electrified chemical transformations, which can accelerate the deployment of more sustainable electrochemical manufacturing processes.
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    Parallel spatial channels converge at a bottleneck in anterior word-selective cortex (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-08
    Description: In most environments, the visual system is confronted with many relevant objects simultaneously. That is especially true during reading. However, behavioral data demonstrate that a serial bottleneck prevents recognition of more than one word at a time. We used fMRI to investigate how parallel spatial channels of visual processing converge into a serial bottleneck for word recognition. Participants viewed pairs of words presented simultaneously. We found that retinotopic cortex processed the two words in parallel spatial channels, one in each contralateral hemisphere. Responses were higher for attended than for ignored words but were not reduced when attention was divided. We then analyzed two word-selective regions along the occipitotemporal sulcus (OTS) of both hemispheres (subregions of the visual word form area, VWFA). Unlike retinotopic regions, each word-selective region responded to words on both sides of fixation. Nonetheless, a single region in the left hemisphere (posterior OTS) contained spatial channels for both hemifields that were independently modulated by selective attention. Thus, the left posterior VWFA supports parallel processing of multiple words. In contrast, activity in a more anterior word-selective region in the left hemisphere (mid OTS) was consistent with a single channel, showing (i) limited spatial selectivity, (ii) no effect of spatial attention on mean response amplitudes, and (iii) sensitivity to lexical properties of only one attended word. Therefore, the visual system can process two words in parallel up to a late stage in the ventral stream. The transition to a single channel is consistent with the observed bottleneck in behavior.
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    Highly specific SNP detection using 2D graphene electronics and DNA strand displacement (2016)
    National Academy of Sciences
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    Publication Date: 2016-06-13
    Description: Single-nucleotide polymorphisms (SNPs) in a gene sequence are markers for a variety of human diseases. Detection of SNPs with high specificity and sensitivity is essential for effective practical implementation of personalized medicine. Current DNA sequencing, including SNP detection, primarily uses enzyme-based methods or fluorophore-labeled assays that are time-consuming, need laboratory-scale settings, and are expensive. Previously reported electrical charge-based SNP detectors have insufficient specificity and accuracy, limiting their effectiveness. Here, we demonstrate the use of a DNA strand displacement-based probe on a graphene field effect transistor (FET) for high-specificity, single-nucleotide mismatch detection. The single mismatch was detected by measuring strand displacement-induced resistance (and hence current) change and Dirac point shift in a graphene FET. SNP detection in large double-helix DNA strands (e.g., 47 nt) minimize false-positive results. Our electrical sensor-based SNP detection technology, without labeling and without apparent cross-hybridization artifacts, would allow fast, sensitive, and portable SNP detection with single-nucleotide resolution. The technology will have a wide range of applications in digital and implantable biosensors and high-throughput DNA genotyping, with transformative implications for personalized medicine.
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    Assembly of long error-prone reads using de Bruijn graphs (2016)
    National Academy of Sciences
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    Publication Date: 2016-12-12
    Description: The recent breakthroughs in assembling long error-prone reads were based on the overlap-layout-consensus (OLC) approach and did not utilize the strengths of the alternative de Bruijn graph approach to genome assembly. Moreover, these studies often assume that applications of the de Bruijn graph approach are limited to short and accurate reads and that the OLC approach is the only practical paradigm for assembling long error-prone reads. We show how to generalize de Bruijn graphs for assembling long error-prone reads and describe the ABruijn assembler, which combines the de Bruijn graph and the OLC approaches and results in accurate genome reconstructions.
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    Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles (2016)
    National Academy of Sciences
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    Publication Date: 2016-12-07
    Description: Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called odontodes. Although homology of oral teeth in jawed vertebrates is well supported, the evolutionary origin of teeth and their relationship with other odontode types is less clear. We compared the cellular and molecular mechanisms directing development of teeth and skin denticles in sharks, where both odontode types are retained. We show that teeth and denticles are deeply homologous developmental modules with equivalent underlying odontode gene regulatory networks (GRNs). Notably, the expression of the epithelial progenitor and stem cell marker sex-determining region Y-related box 2 (sox2) was tooth-specific and this correlates with notable differences in odontode regenerative ability. Whereas shark teeth retain the ancestral gnathostome character of continuous successional regeneration, new denticles arise only asynchronously with growth or after wounding. Sox2+ putative stem cells associated with the shark dental lamina (DL) emerge from a field of epithelial progenitors shared with anteriormost taste buds, before establishing within slow-cycling cell niches at the (i) superficial taste/tooth junction (T/TJ), and (ii) deep successional lamina (SL) where tooth regeneration initiates. Furthermore, during regeneration, cells from the superficial T/TJ migrate into the SL and contribute to new teeth, demonstrating persistent contribution of taste-associated progenitors to tooth regeneration in vivo. This data suggests a trajectory for tooth evolution involving cooption of the odontode GRN from nonregenerating denticles bysox2+ progenitors native to the oral taste epithelium, facilitating the evolution of a novel regenerative module of odontodes in the mouth of early jawed vertebrates: the teeth.
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    Histone H2B monoubiquitination regulates heart development via epigenetic control of cilia motility (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-24
    Description: Genomic analyses of patients with congenital heart disease (CHD) have identified significant contribution from mutations affecting cilia genes and chromatin remodeling genes; however, the mechanism(s) connecting chromatin remodeling to CHD is unknown. Histone H2B monoubiquitination (H2Bub1) is catalyzed by the RNF20 complex consisting of RNF20, RNF40, and UBE2B. Here, we show significant enrichment of loss-of-function mutations affecting H2Bub1 in CHD patients (enrichment 6.01,P= 1.67 × 10−03), some of whom had abnormal laterality associated with ciliary dysfunction. InXenopus, knockdown ofrnf20andrnf40results in abnormal heart looping, defective development of left–right (LR) asymmetry, and impaired cilia motility. Rnf20, Rnf40, and Ube2b affect LR patterning and cilia synergistically. Examination of global H2Bub1 level inXenopusembryos shows that H2Bub1 is developmentally regulated and requires Rnf20. To examine gene-specific H2Bub1, we performed ChIP-seq of mouse ciliated and nonciliated tissues and showed tissue-specific H2Bub1 marks significantly enriched at cilia genes including the transcription factorRfx3. Rnf20 knockdown results in decreased levels ofrfx3mRNA inXenopus, and exogenousrfx3can rescue the Rnf20 depletion phenotype. These data suggest that Rnf20 functions at theRfx3locus regulating cilia motility and cardiac situs and identify H2Bub1 as an upstream transcriptional regulator controlling tissue-specific expression of cilia genes. Our findings mechanistically link the two functional gene ontologies that have been implicated in human CHD: chromatin remodeling and cilia function.
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    Cu isotopes in marine black shales record the Great Oxidation Event (2016)
    National Academy of Sciences
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    Publication Date: 2016-04-18
    Description: The oxygenation of the atmosphere ∼2.45–2.32 billion years ago (Ga) is one of the most significant geological events to have affected Earth’s redox history. Our understanding of the timing and processes surrounding this key transition is largely dependent on the development of redox-sensitive proxies, many of which remain unexplored. Here we report a shift from negative to positive copper isotopic compositions (δ65CuERM-AE633) in organic carbon-rich shales spanning the period 2.66–2.08 Ga. We suggest that, before 2.3 Ga, a muted oxidative supply of weathering-derived copper enriched in 65Cu, along with the preferential removal of 65Cu by iron oxides, left seawater and marine biomass depleted in 65Cu but enriched in 63Cu. As banded iron formation deposition waned and continentally sourced Cu became more important, biomass sampled a dissolved Cu reservoir that was progressively less fractionated relative to the continental pool. This evolution toward heavy δ65Cu values coincides with a shift to negative sedimentary δ56Fe values and increased marine sulfate after the Great Oxidation Event (GOE), and is traceable through Phanerozoic shales to modern marine settings, where marine dissolved and sedimentary δ65Cu values are universally positive. Our finding of an important shift in sedimentary Cu isotope compositions across the GOE provides new insights into the Precambrian marine cycling of this critical micronutrient, and demonstrates the proxy potential for sedimentary Cu isotope compositions in the study of biogeochemical cycles and oceanic redox balance in the past.
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    Conditional vulnerability of plant diversity to atmospheric nitrogen deposition across the United States (2016)
    National Academy of Sciences
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    Publication Date: 2016-03-28
    Description: Atmospheric nitrogen (N) deposition has been shown to decrease plant species richness along regional deposition gradients in Europe and in experimental manipulations. However, the general response of species richness to N deposition across different vegetation types, soil conditions, and climates remains largely unknown even though responses may be contingent on these environmental factors. We assessed the effect of N deposition on herbaceous richness for 15,136 forest, woodland, shrubland, and grassland sites across the continental United States, to address how edaphic and climatic conditions altered vulnerability to this stressor. In our dataset, with N deposition ranging from 1 to 19 kg N⋅ha−1⋅y−1, we found a unimodal relationship; richness increased at low deposition levels and decreased above 8.7 and 13.4 kg N⋅ha−1⋅y−1 in open and closed-canopy vegetation, respectively. N deposition exceeded critical loads for loss of plant species richness in 24% of 15,136 sites examined nationwide. There were negative relationships between species richness and N deposition in 36% of 44 community gradients. Vulnerability to N deposition was consistently higher in more acidic soils whereas the moderating roles of temperature and precipitation varied across scales. We demonstrate here that negative relationships between N deposition and species richness are common, albeit not universal, and that fine-scale processes can moderate vegetation responses to N deposition. Our results highlight the importance of contingent factors when estimating ecosystem vulnerability to N deposition and suggest that N deposition is affecting species richness in forested and nonforested systems across much of the continental United States.
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    Mitochondrial Hsp90 is a ligand-activated molecular chaperone coupling ATP binding to dimer closure through a coiled-coil intermediate (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-29
    Description: Heat-shock protein of 90 kDa (Hsp90) is an essential molecular chaperone that adopts different 3D structures associated with distinct nucleotide states: a wide-open, V-shaped dimer in the apo state and a twisted, N-terminally closed dimer with ATP. Although the N domain is known to mediate ATP binding, how Hsp90 senses the bound nucleotide and facilitates dimer closure remains unclear. Here we present atomic structures of human mitochondrial Hsp90N (TRAP1N) and a composite model of intact TRAP1 revealing a previously unobserved coiled-coil dimer conformation that may precede dimer closure and is conserved in intact TRAP1 in solution. Our structure suggests that TRAP1 normally exists in an autoinhibited state with the ATP lid bound to the nucleotide-binding pocket. ATP binding displaces the ATP lid that signals the cis-bound ATP status to the neighboring subunit in a highly cooperative manner compatible with the coiled-coil intermediate state. We propose that TRAP1 is a ligand-activated molecular chaperone, which couples ATP binding to dramatic changes in local structure required for protein folding.
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    Deep learning predicts path-dependent plasticity (2019)
    National Academy of Sciences
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    Publication Date: 2019-12-16
    Description: Plasticity theory aims at describing the yield loci and work hardening of a material under general deformation states. Most of its complexity arises from the nontrivial dependence of the yield loci on the complete strain history of a material and its microstructure. This motivated 3 ingenious simplifications that underpinned a century of developments in this field: 1) yield criteria describing yield loci location; 2) associative or nonassociative flow rules defining the direction of plastic flow; and 3) effective stress–strain laws consistent with the plastic work equivalence principle. However, 2 key complications arise from these simplifications. First, finding equations that describe these 3 assumptions for materials with complex microstructures is not trivial. Second, yield surface evolution needs to be traced iteratively, i.e., through a return mapping algorithm. Here, we show that these assumptions are not needed in the context of sequence learning when using recurrent neural networks, diverting the above-mentioned complications. This work offers an alternative to currently established plasticity formulations by providing the foundations for finding history- and microstructure-dependent constitutive models through deep learning.
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    Human phosphatase CDC14A is recruited to the cell leading edge to regulate cell migration and adhesion (2016)
    National Academy of Sciences
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    Publication Date: 2016-01-08
    Description: Cell adhesion and migration are highly dynamic biological processes that play important roles in organ development and cancer metastasis. Their tight regulation by small GTPases and protein phosphorylation make interrogation of these key processes of great importance. We now show that the conserved dual-specificity phosphatase human cell-division cycle 14A (hCDC14A) associates with the actin cytoskeleton of human cells. To understand hCDC14A function at this location, we manipulated native loci to ablate hCDC14A phosphatase activity (hCDC14APD) in untransformed hTERT-RPE1 and colorectal cancer (HCT116) cell lines and expressed the phosphatase in HeLa FRT T-Rex cells. Ectopic expression of hCDC14A induced stress fiber formation, whereas stress fibers were diminished in hCDC14APD cells. hCDC14APD cells displayed faster cell migration and less adhesion than wild-type controls. hCDC14A colocalized with the hCDC14A substrate kidney- and brain-expressed protein (KIBRA) at the cell leading edge and overexpression of KIBRA was able to reverse the phenotypes of hCDC14APD cells. Finally, we show that ablation of hCDC14A activity increased the aggressive nature of cells in an in vitro tumor formation assay. Consistently, hCDC14A is down-regulated in many tumor tissues and reduced hCDC14A expression is correlated with poorer survival of patients with cancer, to suggest that hCDC14A may directly contribute to the metastatic potential of tumors. Thus, we have uncovered an unanticipated role for hCDC14A in cell migration and adhesion that is clearly distinct from the mitotic and cytokinesis functions of Cdc14/Flp1 in budding and fission yeast.
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    Graphene-like monolayer monoxides and monochlorides (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-12
    Description: Two-dimensional monolayer materials, with thicknesses of up to several atoms, can be obtained from almost every layer-structured material. It is believed that the catalogs of known 2D materials are almost complete, with fewer new graphene-like materials being discovered. Here, we report 2D graphene-like monolayers from monoxides such as BeO, MgO, CaO, SrO, BaO, and rock-salt structured monochlorides such as LiCl, and NaCl using first-principle calculations. Two-dimensional materials containing d-orbital atoms such as HfO, CdO, and AgCl are predicted. Adopting the same strategy, 2D graphene-like monolayers from mononitrides such as scandium nitride (ScN) and monoselenides such as cadmium selenide (CdSe) are discovered. Stress engineering is found to help stabilize 2D monolayers, through canceling the imaginary frequency of phonon dispersion relation. These 2D monolayers show high dynamic, thermal, kinetic, and mechanic stabilities due to atomic hybridization, and electronic delocalization.
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    Light-triggered thermal conductivity switching in azobenzene polymers (2019)
    National Academy of Sciences
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    Publication Date: 2019-03-08
    Description: Materials that can be switched between low and high thermal conductivity states would advance the control and conversion of thermal energy. Employing in situ time-domain thermoreflectance (TDTR) and in situ synchrotron X-ray scattering, we report a reversible, light-responsive azobenzene polymer that switches between high (0.35 W m−1K−1) and low thermal conductivity (0.10 W m−1K−1) states. This threefold change in the thermal conductivity is achieved by modulation of chain alignment resulted from the conformational transition between planar (trans) and nonplanar (cis) azobenzene groups under UV and green light illumination. This conformational transition leads to changes in the π-π stacking geometry and drives the crystal-to-liquid transition, which is fully reversible and occurs on a time scale of tens of seconds at room temperature. This result demonstrates an effective control of the thermophysical properties of polymers by modulating interchain π-π networks by light.
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    Cell contact and Nf2/Merlin-dependent regulation of TEAD palmitoylation and activity (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-01
    Description: The Hippo pathway is involved in regulating contact inhibition of proliferation and organ size control and responds to various physical and biochemical stimuli. It is a kinase cascade that negatively regulates the activity of cotranscription factors YAP and TAZ, which interact with DNA binding transcription factors including TEAD and activate the expression of target genes. In this study, we show that the palmitoylation of TEAD, which controls the activity and stability of TEAD proteins, is actively regulated by cell density independent of Lats, the key kinase of the Hippo pathway. The expression of fatty acid synthase and acetyl-CoA carboxylase involved in de novo biosynthesis of palmitate is reduced by cell density in an Nf2/Merlin-dependent manner. Depalmitoylation of TEAD is mediated by depalmitoylases including APT2 and ABHD17A. Palmitoylation-deficient TEAD4 mutant is unstable and degraded by proteasome through the activity of the E3 ubiquitin ligase CHIP. These findings show that TEAD activity is tightly controlled through the regulation of palmitoylation and stability via the orchestration of FASN, depalmitoylases, and E3 ubiquitin ligase in response to cell contact.
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    Self-regulation and theforaginggene (PRKG1) in humans (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-19
    Description: Foraging is a goal-directed behavior that balances the need to explore the environment for resources with the need to exploit those resources. InDrosophila melanogaster, distinct phenotypes have been observed in relation to theforaginggene (for), labeled the rover and sitter. Adult rovers explore their environs more extensively than do adult sitters. We explored whether this distinction would be conserved in humans. We made use of a distinction from regulatory mode theory between those who “get on with it,” so-called locomotors, and those who prefer to ensure they “do the right thing,” so-called assessors. In this logic, rovers and locomotors share similarities in goal pursuit, as do sitters and assessors. We showed that genetic variation inPRKG1, the human ortholog offor, is associated with preferential adoption of a specific regulatory mode. Next, participants performed a foraging task to see whether genetic differences associated with distinct regulatory modes would be associated with distinct goal pursuit patterns. Assessors tended to hug the boundary of the foraging environment, much like behaviors seen inDrosophilaadult sitters. In a patchy foraging environment, assessors adopted more cautious search strategies maximizing exploitation. These results show that distinct patterns of goal pursuit are associated with particular genotypes ofPRKG1, the human ortholog offor.
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    Intragenomic variability and extended sequence patterns in the mutational signature of ultraviolet light (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-23
    Description: Mutational signatures can reveal properties of underlying mutational processes and are important when assessing signals of selection in cancer. Here, we describe the sequence characteristics of mutations induced by ultraviolet (UV) light, a major mutagen in several human cancers, in terms of extended (longer than trinucleotide) patterns as well as variability of the signature across chromatin states. Promoter regions display a distinct UV signature with reduced TCG 〉 TTG transitions, and genome-wide mapping of UVB-induced DNA photoproducts (pyrimidine dimers) showed that this may be explained by decreased damage formation at hypomethylated promoter CpG sites. Further, an extended signature model encompassing additional information from longer contextual patterns improves modeling of UV mutations, which may enhance discrimination between drivers and passenger events. Our study presents a refined picture of the UV signature and underscores that the characteristics of a single mutational process may vary across the genome.
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    Structure of the Brd4 ET domain bound to a C-terminal motif from γ-retroviral integrases reveals a conserved mechanism of interaction (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-08
    Description: The bromodomain and extraterminal domain (BET) protein family are promising therapeutic targets for a range of diseases linked to transcriptional activation, cancer, viral latency, and viral integration. Tandem bromodomains selectively tether BET proteins to chromatin by engaging cognate acetylated histone marks, and the extraterminal (ET) domain is the focal point for recruiting a range of cellular and viral proteins. BET proteins guide γ-retroviral integration to transcription start sites and enhancers through bimodal interaction with chromatin and the γ-retroviral integrase (IN). We report the NMR-derived solution structure of the Brd4 ET domain bound to a conserved peptide sequence from the C terminus of murine leukemia virus (MLV) IN. The complex reveals a protein–protein interaction governed by the binding-coupled folding of disordered regions in both interacting partners to form a well-structured intermolecular three-stranded β sheet. In addition, we show that a peptide comprising the ET binding motif (EBM) of MLV IN can disrupt the cognate interaction of Brd4 with NSD3, and that substitutions of Brd4 ET residues essential for binding MLV IN also impair interaction of Brd4 with a number of cellular partners involved in transcriptional regulation and chromatin remodeling. This suggests that γ-retroviruses have evolved the EBM to mimic a cognate interaction motif to achieve effective integration in host chromatin. Collectively, our findings identify key structural features of the ET domain of Brd4 that allow for interactions with both cellular and viral proteins.
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    Origins of ultralow velocity zones through slab-derived metallic melt (2016)
    National Academy of Sciences
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    Publication Date: 2016-05-03
    Description: Understanding the ultralow velocity zones (ULVZs) places constraints on the chemical composition and thermal structure of deep Earth and provides critical information on the dynamics of large-scale mantle convection, but their origin has remained enigmatic for decades. Recent studies suggest that metallic iron and carbon are produced in subducted slabs when they sink beyond a depth of 250 km. Here we show that the eutectic melting curve of the iron−carbon system crosses the current geotherm near Earth’s core−mantle boundary, suggesting that dense metallic melt may form in the lowermost mantle. If concentrated into isolated patches, such melt could produce the seismically observed density and velocity features of ULVZs. Depending on the wetting behavior of the metallic melt, the resultant ULVZs may be short-lived domains that are replenished or regenerated through subduction, or long-lasting regions containing both metallic and silicate melts. Slab-derived metallic melt may produce another type of ULVZ that escapes core sequestration by reacting with the mantle to form iron-rich postbridgmanite or ferropericlase. The hypotheses connect peculiar features near Earth's core−mantle boundary to subduction of the oceanic lithosphere through the deep carbon cycle.
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    OAS-RNase L innate immune pathway mediates the cytotoxicity of a DNA-demethylating drug (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-27
    Description: Drugs that reverse epigenetic silencing, such as the DNA methyltransferase inhibitor (DNMTi) 5-azacytidine (AZA), have profound effects on transcription and tumor cell survival. AZA is an approved drug for myelodysplastic syndromes and acute myeloid leukemia, and is under investigation for different solid malignant tumors. AZA treatment generates self, double-stranded RNA (dsRNA), transcribed from hypomethylated repetitive elements. Self dsRNA accumulation in DNMTi-treated cells leads to type I IFN production and IFN-stimulated gene expression. Here we report that cell death in response to AZA treatment occurs through the 2′,5′-oligoadenylate synthetase (OAS)-RNase L pathway. OASs are IFN-induced enzymes that synthesize the RNase L activator 2-5A in response to dsRNA. Cells deficient in RNase L or OAS1 to 3 are highly resistant to AZA, as are wild-type cells treated with a small-molecule inhibitor of RNase L. A small-molecule inhibitor of c-Jun NH2-terminal kinases (JNKs) also antagonizes RNase L-dependent cell death in response to AZA, consistent with a role for JNK in RNase L-induced apoptosis. In contrast, the rates of AZA-induced and RNase L-dependent cell death were increased by transfection of 2-5A, by deficiencies in ADAR1 (which edits and destabilizes dsRNA), PDE12 or AKAP7 (which degrade 2-5A), or by ionizing radiation (which induces IFN-dependent signaling). Finally, OAS1 expression correlates with AZA sensitivity in the NCI-60 set of tumor cell lines, suggesting that the level of OAS1 can be a biomarker for predicting AZA sensitivity of tumor cells. These studies may eventually lead to pharmacologic strategies for regulating the antitumor activity and toxicity of AZA and related drugs.
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    Isotopic evidence for primordial molecular cloud material in metal-rich carbonaceous chondrites (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-08
    Description: The short-lived 26Al radionuclide is thought to have been admixed into the initially 26Al-poor protosolar molecular cloud before or contemporaneously with its collapse. Bulk inner Solar System reservoirs record positively correlated variability in mass-independent 54Cr and 26Mg*, the decay product of 26Al. This correlation is interpreted as reflecting progressive thermal processing of in-falling 26Al-rich molecular cloud material in the inner Solar System. The thermally unprocessed molecular cloud matter reflecting the nucleosynthetic makeup of the molecular cloud before the last addition of stellar-derived 26Al has not been identified yet but may be preserved in planetesimals that accreted in the outer Solar System. We show that metal-rich carbonaceous chondrites and their components have a unique isotopic signature extending from an inner Solar System composition toward a 26Mg*-depleted and 54Cr-enriched component. This composition is consistent with that expected for thermally unprocessed primordial molecular cloud material before its pollution by stellar-derived 26Al. The 26Mg* and 54Cr compositions of bulk metal-rich chondrites require significant amounts (25–50%) of primordial molecular cloud matter in their precursor material. Given that such high fractions of primordial molecular cloud material are expected to survive only in the outer Solar System, we infer that, similarly to cometary bodies, metal-rich carbonaceous chondrites are samples of planetesimals that accreted beyond the orbits of the gas giants. The lack of evidence for this material in other chondrite groups requires isolation from the outer Solar System, possibly by the opening of disk gaps from the early formation of gas giants.
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    Thermalization and possible signatures of quantum chaos in complex crystalline materials (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-12
    Description: Analyses of thermal diffusivity data on complex insulators and on strongly correlated electron systems hosted in similar complex crystal structures suggest that quantum chaos is a good description for thermalization processes in these systems, particularly in the high-temperature regime where the many phonon bands and their interactions dominate the thermal transport. Here we observe that for these systems diffusive thermal transport is controlled by a universal Planckian timescale τ∼ℏ/kBT and a unique velocity vE. Specifically, vE≈vph for complex insulators, and vph≲vE≪vF in the presence of strongly correlated itinerant electrons (vph and vF are the phonon and electron velocities, respectively). For the complex correlated electron systems we further show that charge diffusivity, while also reaching the Planckian relaxation bound, is largely dominated by the Fermi velocity of the electrons, hence suggesting that it is only the thermal (energy) diffusivity that describes chaos diffusivity.
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    Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellularSalmonellaTyphimurium (2019)
    National Academy of Sciences
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    Publication Date: 2019-03-12
    Description: SalmonellaTyphimurium can invade and survive within macrophages where the bacterium encounters a range of host environmental conditions. Like many bacteria,S.Typhimurium rapidly responds to changing environments by the use of second messengers such as cyclic di-GMP (c-di-GMP). Here, we generate a fluorescent biosensor to measure c-di-GMP concentrations in thousands of individual bacteria during macrophage infection and to define the sensor enzymes important to c-di-GMP regulation. Three sensor phosphodiesterases were identified as critical to maintaining low c-di-GMP concentrations generated after initial phagocytosis by macrophages. Maintenance of low c-di-GMP concentrations by these phosphodiesterases was required to promote survival within macrophages and virulence for mice. Attenuation ofS. Typhimurium virulence was due to overproduction of c-di-GMP−regulated cellulose, as deletion of the cellulose synthase machinery restored virulence to a strain lacking enzymatic activity of the three phosphodiesterases. We further identified that the cellulose-mediated reduction in survival was constrained to a slow-replicating persister population ofS.Typhimurium induced within the macrophage intracellular environment. As utilization of glucose has been shown to be required forS.Typhimurium macrophage survival, one possible hypothesis is that this persister population requires the glucose redirected to the synthesis of cellulose to maintain a slow-replicating, metabolically active state.
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    Brief intervention to encourage empathic discipline cuts suspension rates in half among adolescents (2016)
    National Academy of Sciences
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    Publication Date: 2016-04-25
    Description: Growing suspension rates predict major negative life outcomes, including adult incarceration and unemployment. Experiment 1 tested whether teachers (n = 39) could be encouraged to adopt an empathic rather than punitive mindset about discipline—to value students’ perspectives and sustain positive relationships while encouraging better behavior. Experiment 2 tested whether an empathic response to misbehavior would sustain students’ (n = 302) respect for teachers and motivation to behave well in class. These hypotheses were confirmed. Finally, a randomized field experiment tested a brief, online intervention to encourage teachers to adopt an empathic mindset about discipline. Evaluated at five middle schools in three districts (Nteachers = 31; Nstudents = 1,682), this intervention halved year-long student suspension rates from 9.6% to 4.8%. It also bolstered respect the most at-risk students, previously suspended students, perceived from teachers. Teachers’ mindsets about discipline directly affect the quality of teacher–student relationships and student suspensions and, moreover, can be changed through scalable intervention.
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    MZB1 promotes the secretion of J-chain–containing dimeric IgA and is critical for the suppression of gut inflammation (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-24
    Description: IgA is the most abundantly produced antibody in the body and plays a crucial role in gut homeostasis and mucosal immunity. IgA forms a dimer that covalently associates with the joining (J) chain, which is essential for IgA transport into the mucosa. Here, we demonstrate that the marginal zone B and B-1 cell-specific protein (MZB1) interacts with IgA through the α-heavy-chain tailpiece dependent on the penultimate cysteine residue and prevents the intracellular degradation of α-light-chain complexes. Moreover, MZB1 promotes J-chain binding to IgA and the secretion of dimeric IgA. MZB1-deficient mice are impaired in secreting large amounts of IgA into the gut in response to acute inflammation and develop severe colitis. Oral administration of a monoclonal IgA significantly ameliorated the colitis, accompanied by normalization of the gut microbiota composition. The present study identifies a molecular chaperone that promotes J-chain binding to IgA and reveals an important mechanism that controls the quantity, quality, and function of IgA.
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    Biosynthetic investigation of phomopsins reveals a widespread pathway for ribosomal natural products in Ascomycetes (2016)
    National Academy of Sciences
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    Publication Date: 2016-03-15
    Description: Production of ribosomally synthesized and posttranslationally modified peptides (RiPPs) has rarely been reported in fungi, even though organisms of this kingdom have a long history as a prolific source of natural products. Here we report an investigation of the phomopsins, antimitotic mycotoxins. We show that phomopsin is a fungal RiPP and demonstrate the widespread presence of a pathway for the biosynthesis of a family of fungal cyclic RiPPs, which we term dikaritins. We characterize PhomM as an S-adenosylmethionine–dependent α-N-methyltransferase that converts phomopsin A to anN,N-dimethylated congener (phomopsin E), and show that the methyltransferases involved in dikaritin biosynthesis have evolved differently and likely have broad substrate specificities. Genome mining studies identified eight previously unknown dikaritins in different strains, highlighting the untapped capacity of RiPP biosynthesis in fungi and setting the stage for investigating the biological activities and unknown biosynthetic transformations of this family of fungal natural products.
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    Vortex-induced dispersal of a plant pathogen by raindrop impact (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-25
    Description: Raindrop impact on infected plants can disperse micron-sized propagules of plant pathogens (e.g., spores of fungi). Little is known about the mechanism of how plant pathogens are liberated and transported due to raindrop impact. We used high-speed photography to observe thousands of dry-dispersed spores of the rust fungus Puccinia triticina being liberated from infected wheat plants following the impact of a single raindrop. We revealed that an air vortex ring was formed during the raindrop impact and carried the dry-dispersed spores away from the surface of the host plant. The maximum height and travel distance of the airborne spores increased with the aid of the air vortex. This unique mechanism of vortex-induced dispersal dynamics was characterized to predict trajectories of spores. Finally, we found that the spores transported by the air vortex can reach beyond the laminar boundary layer of leaves, which would enable the long-distance transport of plant pathogens through the atmosphere.
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    Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs (2019)
    National Academy of Sciences
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    Publication Date: 2019-11-18
    Description: The avian predentary is a small skeletal structure located rostral to the paired dentaries found only in Mesozoic ornithuromorphs. The evolution and function of this enigmatic element is unknown. Skeletal tissues forming the predentary and the lower jaws in the basal ornithuromorph Yanornis martini are identified using computed-tomography, scanning electron microscopy, and histology. On the basis of these data, we propose hypotheses for the development, structure, and function of this element. The predentary is composed of trabecular bone. The convex caudal surface articulates with rostromedial concavities on the dentaries. These articular surfaces are covered by cartilage, which on the dentaries is divided into 3 discrete patches: 1 rostral articular cartilage and 2 symphyseal cartilages. The mechanobiology of avian cartilage suggests both compression and kinesis were present at the predentary–dentary joint, therefore suggesting a yet unknown form of avian cranial kinesis. Ontogenetic processes of skeletal formation occurring within extant taxa do not suggest the predentary originates within the dentaries, nor Meckel’s cartilage. We hypothesize that the predentary is a biomechanically induced sesamoid that arose within the soft connective tissues located rostral to the dentaries. The mandibular canal hosting the alveolar nerve suggests that the dentary teeth and predentary of Yanornis were proprioceptive. This whole system may have increased foraging efficiency. The Mesozoic avian predentary apparently coevolved with an edentulous portion of the premaxilla, representing a unique kinetic morphotype that combined teeth with a small functional beak and persisted successfully for ∼60 million years.
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    The functional importance of human foot muscles for bipedal locomotion (2019)
    National Academy of Sciences
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    Publication Date: 2019-01-17
    Description: Human feet have evolved to facilitate bipedal locomotion, losing an opposable digit that grasped branches in favor of a longitudinal arch (LA) that stiffens the foot and aids bipedal gait. Passive elastic structures are credited with supporting the LA, but recent evidence suggests that plantar intrinsic muscles (PIMs) within the foot actively contribute to foot stiffness. To test the functional significance of the PIMs, we compared foot and lower limb mechanics with and without a tibial nerve block that prevented contraction of these muscles. Comparisons were made during controlled limb loading, walking, and running in healthy humans. An inability to activate the PIMs caused slightly greater compression of the LA when controlled loads were applied to the lower limb by a linear actuator. However, when greater loads were experienced during ground contact in walking and running, the stiffness of the LA was not altered by the block, indicating that the PIMs’ contribution to LA stiffness is minimal, probably because of their small size. With the PIMs blocked, the distal joints of the foot could not be stiffened sufficiently to provide normal push-off against the ground during late stance. This led to an increase in stride rate and compensatory power generated by the hip musculature, but no increase in the metabolic cost of transport. The results reveal that the PIMs have a minimal effect on the stiffness of the LA when absorbing high loads, but help stiffen the distal foot to aid push-off against the ground when walking or running bipedally.
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    Autonomic activity during sleep predicts memory consolidation in humans (2016)
    National Academy of Sciences
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    Publication Date: 2016-06-13
    Description: Throughout history, psychologists and philosophers have proposed that good sleep benefits memory, yet current studies focusing on the relationship between traditionally reported sleep features (e.g., minutes in sleep stages) and changes in memory performance show contradictory findings. This discrepancy suggests that there are events occurring during sleep that have not yet been considered. The autonomic nervous system (ANS) shows strong variation across sleep stages. Also, increases in ANS activity during waking, as measured by heart rate variability (HRV), have been correlated with memory improvement. However, the role of ANS in sleep-dependent memory consolidation has never been examined. Here, we examined whether changes in cardiac ANS activity (HRV) during a daytime nap were related to performance on two memory conditions (Primed and Repeated) and a nonmemory control condition on the Remote Associates Test. In line with prior studies, we found sleep-dependent improvement in the Primed condition compared with the Quiet Wake control condition. Using regression analyses, we compared the proportion of variance in performance associated with traditionally reported sleep features (model 1) vs. sleep features and HRV during sleep (model 2). For both the Primed and Repeated conditions, model 2 (sleep + HRV) predicted performance significantly better (73% and 58% of variance explained, respectively) compared with model 1 (sleep only, 46% and 26% of variance explained, respectively). These findings present the first evidence, to our knowledge, that ANS activity may be one potential mechanism driving sleep-dependent plasticity.
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    Adolescents growing up amidst intractable conflict attenuate brain response to pain of outgroup (2016)
    National Academy of Sciences
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    Publication Date: 2016-11-14
    Description: Adolescents’ participation in intergroup conflicts comprises an imminent global risk, and understanding its neural underpinnings may open new perspectives. We assessed Jewish-Israeli and Arab-Palestinian adolescents for brain response to the pain of ingroup/outgroup protagonists using magnetoencephalography (MEG), one-on-one positive and conflictual interactions with an outgroup member, attitudes toward the regional conflict, and oxytocin levels. A neural marker of ingroup bias emerged, expressed via alpha modulations in the somatosensory cortex (S1) that characterized an automatic response to the pain of all protagonists followed by rebound/enhancement to ingroup pain only. Adolescents’ hostile social interactions with outgroup members and uncompromising attitudes toward the conflict influenced this neural marker. Furthermore, higher oxytocin levels in the Jewish-Israeli majority and tighter brain-to-brain synchrony among group members in the Arab-Palestinian minority enhanced the neural ingroup bias. Findings suggest that in cases of intractable intergroup conflict, top-down control mechanisms may block the brain’s evolutionary-ancient resonance to outgroup pain, pinpointing adolescents’ interpersonal and sociocognitive processes as potential targets for intervention.
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    Origins of the brain networks for advanced mathematics in expert mathematicians (2016)
    National Academy of Sciences
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    Publication Date: 2016-04-11
    Description: The origins of human abilities for mathematics are debated: Some theories suggest that they are founded upon evolutionarily ancient brain circuits for number and space and others that they are grounded in language competence. To evaluate what brain systems underlie higher mathematics, we scanned professional mathematicians and mathematically naive subjects of equal academic standing as they evaluated the truth of advanced mathematical and nonmathematical statements. In professional mathematicians only, mathematical statements, whether in algebra, analysis, topology or geometry, activated a reproducible set of bilateral frontal, Intraparietal, and ventrolateral temporal regions. Crucially, these activations spared areas related to language and to general-knowledge semantics. Rather, mathematical judgments were related to an amplification of brain activity at sites that are activated by numbers and formulas in nonmathematicians, with a corresponding reduction in nearby face responses. The evidence suggests that high-level mathematical expertise and basic number sense share common roots in a nonlinguistic brain circuit.
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    Neurodevelopmental origins of lifespan changes in brain and cognition (2016)
    National Academy of Sciences
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    Publication Date: 2016-07-18
    Description: Neurodevelopmental origins of functional variation in older age are increasingly being acknowledged, but identification of how early factors impact human brain and cognition throughout life has remained challenging. Much focus has been on age-specific mechanisms affecting neural foundations of cognition and their change. In contrast to this approach, we tested whether cerebral correlates of general cognitive ability (GCA) in development could be extended to the rest of the lifespan, and whether early factors traceable to prenatal stages, such as birth weight and parental education, may exert continuous influences. We measured the area of the cerebral cortex in a longitudinal sample of 974 individuals aged 4–88 y (1,633 observations). An extensive cortical region was identified wherein area related positively to GCA in development. By tracking area of the cortical region identified in the child sample throughout the lifespan, we showed that the cortical change trajectories of higher and lower GCA groups were parallel through life, suggesting continued influences of early life factors. Birth weight and parental education obtained from the Norwegian Mother–Child Cohort study were identified as such early factors of possible life-long influence. Support for a genetic component was obtained in a separate twin sample (Vietnam Era Twin Study of Aging), but birth weight in the child sample had an effect on cortical area also when controlling for possible genetic differences in terms of parental height. Our results provide novel evidence for stability in brain–cognition relationships throughout life, and indicate that early life factors impact brain and cognition for the entire life course.
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    Electrochemical nanoimprinting of silicon (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-08
    Description: Scalable nanomanufacturing enables the commercialization of nanotechnology, particularly in applications such as nanophotonics, silicon photonics, photovoltaics, and biosensing. Nanoimprinting lithography (NIL) was the first scalable process to introduce 3D nanopatterning of polymeric films. Despite efforts to extend NIL’s library of patternable media, imprinting of inorganic semiconductors has been plagued by concomitant generation of crystallography defects during imprinting. Here, we use an electrochemical nanoimprinting process—called Mac-Imprint—for directly patterning electronic-grade silicon with 3D microscale features. It is shown that stamps made of mesoporous metal catalysts allow for imprinting electronic-grade silicon without the concomitant generation of porous silicon damage while introducing mesoscale roughness. Unlike most NIL processes, Mac-Imprint does not rely on plastic deformation, and thus, it allows for replicating hard and brittle materials, such as silicon, from a reusable polymeric mold, which can be manufactured by almost any existing microfabrication technique.
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    Pressure-induced superconductivity in a three-dimensional topological material ZrTe5 (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-29
    Description: As a new type of topological materials, ZrTe5 shows many exotic properties under extreme conditions. Using resistance and ac magnetic susceptibility measurements under high pressure, while the resistance anomaly near 128 K is completely suppressed at 6.2 GPa, a fully superconducting transition emerges. The superconducting transition temperature Tc increases with applied pressure, and reaches a maximum of 4.0 K at 14.6 GPa, followed by a slight drop but remaining almost constant value up to 68.5 GPa. At pressures above 21.2 GPa, a second superconducting phase with the maximum Tc of about 6.0 K appears and coexists with the original one to the maximum pressure studied in this work. In situ high-pressure synchrotron X-ray diffraction and Raman spectroscopy combined with theoretical calculations indicate the observed two-stage superconducting behavior is correlated to the structural phase transition from ambient Cmcm phase to high-pressure C2/m phase around 6 GPa, and to a mixture of two high-pressure phases of C2/m and P-1 above 20 GPa. The combination of structure, transport measurement, and theoretical calculations enable a complete understanding of the emerging exotic properties in 3D topological materials under extreme environments.
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    Steering CO2electroreduction toward ethanol production by a surface-bound Ru polypyridyl carbene catalyst on N-doped porous carbon (2019)
    National Academy of Sciences
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    Publication Date: 2019-12-10
    Description: Electrochemical reduction of CO2to multicarbon products is a significant challenge, especially for molecular complexes. We report here CO2reduction to multicarbon products based on a Ru(II) polypyridyl carbene complex that is immobilized on an N-doped porous carbon (RuPC/NPC) electrode. The catalyst utilizes the synergistic effects of the Ru(II) polypyridyl carbene complex and the NPC interface to steer CO2reduction toward C2 production at low overpotentials. In 0.5 M KHCO3/CO2aqueous solutions, Faradaic efficiencies of 31.0 to 38.4% have been obtained for C2 production at −0.87 to −1.07 V (vs. normal hydrogen electrode) with 21.0 to 27.5% for ethanol and 7.1 to 12.5% for acetate. Syngas is also produced with adjustable H2/CO mole ratios of 2.0 to 2.9. The RuPC/NPC electrocatalyst maintains its activity during 3-h CO2-reduction periods.
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    Implications of lemuriform extinctions for the Malagasy flora (2016)
    National Academy of Sciences
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    Publication Date: 2016-04-11
    Description: Madagascar’s lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar’s lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.
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    Kin of coauthorship in five decades of health science literature (2016)
    National Academy of Sciences
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    Publication Date: 2016-07-25
    Description: Family background—kinship—can propagate careers. The evidence for academic nepotism is littered with complex associations and disputed causal inferences. Surname clustering, albeit with very careful consideration of surnames’ flows across regions and time periods, can be used to reflect family ties. We examined surname patterns in the health science literature, by country, across five decades. Over 21 million papers indexed in the MEDLINE/PubMed database were analyzed. We identified relevant country-specific kinship trends over time and found that authors who are part of a kin tend to occupy central positions in their collaborative networks. Just as kin build potent academic networks with their own resources, societies may do well to provide equivalent support for talented individuals with fewer resources, on the periphery of networks.
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    Impact of jamming criticality on low-temperature anomalies in structural glasses (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-24
    Description: We present a mechanism for the anomalous behavior of the specific heat in low-temperature amorphous solids. The analytic solution of a mean-field model belonging to the same universality class as high-dimensional glasses, the spherical perceptron, suggests that there exists a cross-over temperature above which the specific heat scales linearly with temperature, while below it, a cubic scaling is displayed. This relies on two crucial features of the phase diagram: (i) the marginal stability of the free-energy landscape, which induces a gapless phase responsible for the emergence of a power-law scaling; and (ii) the vicinity of the classical jamming critical point, as the cross-over temperature gets lowered when approaching it. This scenario arises from a direct study of the thermodynamics of the system in the quantum regime, where we show that, contrary to crystals, the Debye approximation does not hold.
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    Observation of Rydberg exciton polaritons and their condensate in a perovskite cavity (2019)
    National Academy of Sciences
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    Publication Date: 2019-09-23
    Description: The condensation of half-light half-matter exciton polaritons in semiconductor optical cavities is a striking example of macroscopic quantum coherence in a solid-state platform. Quantum coherence is possible only when there are strong interactions between the exciton polaritons provided by their excitonic constituents. Rydberg excitons with high principal value exhibit strong dipole–dipole interactions in cold atoms. However, polaritons with the excitonic constituent that is an excited state, namely Rydberg exciton polaritons (REPs), have not yet been experimentally observed. Here, we observe the formation of REPs in a single crystal CsPbBr3 perovskite cavity without any external fields. These polaritons exhibit strong nonlinear behavior that leads to a coherent polariton condensate with a prominent blue shift. Furthermore, the REPs in CsPbBr3 are highly anisotropic and have a large extinction ratio, arising from the perovskite’s orthorhombic crystal structure. Our observation not only sheds light on the importance of many-body physics in coherent polariton systems involving higher-order excited states, but also paves the way for exploring these coherent interactions for solid-state quantum optical information processing.
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    Outflanking immunodominance to target subdominant broadly neutralizing epitopes (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-18
    Description: A major obstacle to vaccination against antigenically variable viruses is skewing of antibody responses to variable immunodominant epitopes. For influenza virus hemagglutinin (HA), the immunodominance of the variable head impairs responses to the highly conserved stem. Here, we show that head immunodominance depends on the physical attachment of head to stem. Stem immunogenicity is enhanced by immunizing with stem-only constructs or by increasing local HA concentration in the draining lymph node. Surprisingly, coimmunization of full-length HA and stem alters stem-antibody class switching. Our findings delineate strategies for overcoming immunodominance, with important implications for human vaccination.
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    Mechanism of substrate specificity of phosphatidylinositol phosphate kinases (2016)
    National Academy of Sciences
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    Publication Date: 2016-07-20
    Description: The phosphatidylinositol phosphate kinase (PIPK) family of enzymes is primarily responsible for converting singly phosphorylated phosphatidylinositol derivatives to phosphatidylinositol bisphosphates. As such, these kinases are central to many signaling and membrane trafficking processes in the eukaryotic cell. The three types of phosphatidylinositol phosphate kinases are homologous in sequence but differ in catalytic activities and biological functions. Type I and type II kinases generate phosphatidylinositol 4,5-bisphosphate from phosphatidylinositol 4-phosphate and phosphatidylinositol 5-phosphate, respectively, whereas the type III kinase produces phosphatidylinositol 3,5-bisphosphate from phosphatidylinositol 3-phosphate. Based on crystallographic analysis of the zebrafish type I kinase PIP5Kα, we identified a structural motif unique to the kinase family that serves to recognize the monophosphate on the substrate. Our data indicate that the complex pattern of substrate recognition and phosphorylation results from the interplay between the monophosphate binding site and the specificity loop: the specificity loop functions to recognize different orientations of the inositol ring, whereas residues flanking the phosphate binding Arg244 determine whether phosphatidylinositol 3-phosphate is exclusively bound and phosphorylated at the 5-position. This work provides a thorough picture of how PIPKs achieve their exquisite substrate specificity.
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    Transient HIV-1 Gag–protease interactions revealed by paramagnetic NMR suggest origins of compensatory drug resistance mutations (2016)
    National Academy of Sciences
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    Publication Date: 2016-10-17
    Description: Cleavage of the group-specific antigen (Gag) polyprotein by HIV-1 protease represents the critical first step in the conversion of immature noninfectious viral particles to mature infectious virions. Selective pressure exerted by HIV-1 protease inhibitors, a mainstay of current anti–HIV-1 therapies, results in the accumulation of drug resistance mutations in both protease and Gag. Surprisingly, a large number of these mutations (known as secondary or compensatory mutations) occur outside the active site of protease or the cleavage sites of Gag (located within intrinsically disordered linkers connecting the globular domains of Gag to one another), suggesting that transient encounter complexes involving the globular domains of Gag may play a role in guiding and facilitating access of the protease to the Gag cleavage sites. Here, using large fragments of Gag, as well as catalytically inactive and active variants of protease, we probe the nature of such rare encounter complexes using intermolecular paramagnetic relaxation enhancement, a highly sensitive technique for detecting sparsely populated states. We show that Gag-protease encounter complexes are primarily mediated by interactions between protease and the globular domains of Gag and that the sites of transient interactions are correlated with surface exposed regions that exhibit a high propensity to mutate in the presence of HIV-1 protease inhibitors.
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    L-type voltage-gated Ca2+ channel CaV1.2 regulates chondrogenesis during limb development (2019)
    National Academy of Sciences
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    Publication Date: 2019-10-07
    Description: All cells, including nonexcitable cells, maintain a discrete transmembrane potential (Vmem), and have the capacity to modulate Vmem and respond to their own and neighbors’ changes in Vmem. Spatiotemporal variations have been described in developing embryonic tissues and in some cases have been implicated in influencing developmental processes. Yet, how such changes in Vmem are converted into intracellular inputs that in turn regulate developmental gene expression and coordinate patterned tissue formation, has remained elusive. Here we document that the Vmem of limb mesenchyme switches from a hyperpolarized to depolarized state during early chondrocyte differentiation. This change in Vmem increases intracellular Ca2+ signaling through Ca2+ influx, via CaV1.2, 1 of L-type voltage-gated Ca2+ channels (VGCCs). We find that CaV1.2 activity is essential for chondrogenesis in the developing limbs. Pharmacological inhibition by an L-type VGCC specific blocker, or limb-specific deletion of CaV1.2, down-regulates expression of genes essential for chondrocyte differentiation, including Sox9, Col2a1, and Agc1, and thus disturbs proper cartilage formation. The Ca2+-dependent transcription factor NFATc1, which is a known major transducer of intracellular Ca2+ signaling, partly rescues Sox9 expression. These data reveal instructive roles of CaV1.2 in limb development, and more generally expand our understanding of how modulation of membrane potential is used as a mechanism of developmental regulation.
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    Tumor-associated fibroblasts predominantly come from local and not circulating precursors (2016)
    National Academy of Sciences
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    Publication Date: 2016-06-17
    Description: Fibroblasts are common cell types in cancer stroma and lay down collagen required for survival and growth of cancer cells. Although some cancer therapy strategies target tumor fibroblasts, their origin remains controversial. Multiple publications suggest circulating mesenchymal precursors as a source of tumor-associated fibroblasts. However, we show by three independent approaches that tumor fibroblasts derive primarily from local, sessile precursors. First, transplantable tumors developing in a mouse expressing green fluorescent reporter protein (EGFP) under control of the type I collagen (Col-I) promoter (COL-EGFP) had green stroma, whereas we could not find COL-EGFP+ cells in tumors developing in the parabiotic partner lacking the fluorescent reporter. Lack of incorporation of COL-EGFP+ cells from the circulation into tumors was confirmed in parabiotic pairs of COL-EGFP mice and transgenic mice developing autochthonous intestinal adenomas. Second, transplantable tumors developing in chimeric mice reconstituted with bone marrow cells from COL-EGFP mice very rarely showed stromal fibroblasts expressing EGFP. Finally, cancer cells injected under full-thickness COL-EGFP skin grafts transplanted in nonreporter mice developed into tumors containing green stromal cells. Using multicolor in vivo confocal microscopy, we found that Col-I–expressing fibroblasts constituted approximately one-third of the stromal mass and formed a continuous sheet wrapping the tumor vessels. In summary, tumors form their fibroblastic stroma predominantly from precursors present in the local tumor microenvironment, whereas the contribution of bone marrow-derived circulating precursors is rare.
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    A large-scale analysis of task switching practice effects across the lifespan (2019)
    National Academy of Sciences
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    Publication Date: 2019-08-19
    Description: An important feature of human cognition is the ability to flexibly and efficiently adapt behavior in response to continuously changing contextual demands. We leverage a large-scale dataset from Lumosity, an online cognitive-training platform, to investigate how cognitive processes involved in cued switching between tasks are affected by level of task practice across the adult lifespan. We develop a computational account of task switching that specifies the temporal dynamics of activating task-relevant representations and inhibiting task-irrelevant representations and how they vary with extended task practice across a number of age groups. Practice modulates the level of activation of the task-relevant representation and improves the rate at which this information becomes available, but has little effect on the task-irrelevant representation. While long-term practice improves performance across all age groups, it has a greater effect on older adults. Indeed, extensive task practice can make older individuals functionally similar to less-practiced younger individuals, especially for cognitive measures that focus on the rate at which task-relevant information becomes available.
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    Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-29
    Description: In flowering plants, pollen tubes are guided into ovules by multiple attractants from female gametophytes to release paired sperm cells for double fertilization. It has been well-established that Ca2+ gradients in the pollen tube tips are essential for pollen tube guidance and that plasma membrane Ca2+ channels in pollen tube tips are core components that regulate Ca2+ gradients by mediating and regulating external Ca2+ influx. Therefore, Ca2+ channels are the core components for pollen tube guidance. However, there is still no genetic evidence for the identification of the putative Ca2+ channels essential for pollen tube guidance. Here, we report that the point mutations R491Q or R578K in cyclic nucleotide-gated channel 18 (CNGC18) resulted in abnormal Ca2+ gradients and strong pollen tube guidance defects by impairing the activation of CNGC18 in Arabidopsis. The pollen tube guidance defects of cngc18-17 (R491Q) and of the transfer DNA (T-DNA) insertion mutant cngc18-1 (+/−) were completely rescued by CNGC18. Furthermore, domain-swapping experiments showed that CNGC18’s transmembrane domains are indispensable for pollen tube guidance. Additionally, we found that, among eight Ca2+ channels (including six CNGCs and two glutamate receptor-like channels), CNGC18 was the only one essential for pollen tube guidance. Thus, CNGC18 is the long-sought essential Ca2+ channel for pollen tube guidance in Arabidopsis.
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    Evolution of a mass spectrometry-grade protease with PTM-directed specificity (2016)
    National Academy of Sciences
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    Publication Date: 2016-12-08
    Description: Mapping posttranslational modifications (PTMs), which diversely modulate biological functions, represents a significant analytical challenge. The centerpiece technology for PTM site identification, mass spectrometry (MS), requires proteolytic cleavage in the vicinity of a PTM to yield peptides for sequencing. This requirement catalyzed our efforts to evolve MS-grade mutant PTM-directed proteases. Citrulline, a PTM implicated in epigenetic and immunological function, made an ideal first target, because citrullination eliminates arginyl tryptic sites. Bead-displayed trypsin mutant genes were translated in droplets, the mutant proteases were challenged to cleave bead-bound fluorogenic probes of citrulline-dependent proteolysis, and the resultant beads (1.3 million) were screened. The most promising mutant efficiently catalyzed citrulline-dependent peptide bond cleavage (kcat/KM= 6.9 × 105M−1⋅s−1). The resulting C-terminally citrullinated peptides generated characteristic isotopic patterns in MALDI-TOF MS, and both a fragmentation producty1ion corresponding to citrulline (176.1030m/z) and diagnostic peak pairs in the extracted ion chromatograms of LC-MS/MS analysis. Using these signatures, we identified citrullination sites in protein arginine deiminase 4 (12 sites) and in fibrinogen (25 sites, two previously unknown). The unique mass spectral features of PTM-dependent proteolytic digest products promise a generalized PTM site-mapping strategy based on a toolbox of such mutant proteases, which are now accessible by laboratory evolution.
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    Canonical and noncanonical intraflagellar transport regulates craniofacial skeletal development (2016)
    National Academy of Sciences
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    Publication Date: 2016-04-26
    Description: The primary cilium is a cellular organelle that coordinates signaling pathways critical for cell proliferation, differentiation, survival, and homeostasis. Intraflagellar transport (IFT) plays a pivotal role in assembling primary cilia. Disruption and/or dysfunction of IFT components can cause multiple diseases, including skeletal dysplasia. However, the mechanism by which IFT regulates skeletogenesis remains elusive. Here, we show that a neural crest-specific deletion of intraflagellar transport 20 (Ift20) in mice compromises ciliogenesis and intracellular transport of collagen, which leads to osteopenia in the facial region. Whereas platelet-derived growth factor receptor alpha (PDGFRα) was present on the surface of primary cilia in wild-type osteoblasts, disruption ofIft20down-regulated PDGFRα production, which caused suppression of PDGF-Akt signaling, resulting in decreased osteogenic proliferation and increased cell death. Although osteogenic differentiation in cranial neural crest (CNC)-derived cells occurred normally inIft20-mutant cells, the process of mineralization was severely attenuated due to delayed secretion of type I collagen. In control osteoblasts, procollagen was easily transported from the endoplasmic reticulum (ER) to the Golgi apparatus. By contrast, despite having similar levels of collagen type 1 alpha 1 (Col1a1) expression,Ift20mutants did not secrete procollagen because of dysfunctional ER-to-Golgi trafficking. These data suggest that in the multipotent stem cells of CNCs, IFT20 is indispensable for regulating not only ciliogenesis but also collagen intracellular trafficking. Our study introduces a unique perspective on the canonical and noncanonical functions of IFT20 in craniofacial skeletal development.
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    Equilibrium structure and deformation response of 2D kinetoplast sheets (2019)
    National Academy of Sciences
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    Publication Date: 2019-12-06
    Description: The considerable interest in two-dimensional (2D) materials and complex molecular topologies calls for a robust experimental system for single-molecule studies. In this work, we study the equilibrium properties and deformation response of a complex DNA structure called a kinetoplast, a 2D network of thousands of linked rings akin to molecular chainmail. Examined in good solvent conditions, kinetoplasts appear as a wrinkled hemispherical sheet. The conformation of each kinetoplast is dictated by its network topology, giving it a unique shape, which undergoes small-amplitude thermal fluctuations at subsecond timescales, with a wide separation between fluctuation and diffusion timescales. They deform elastically when weakly confined and swell to their equilibrium dimensions when the confinement is released. We hope that, in the same way that linear DNA became a canonical model system on the first investigations of its polymer-like behavior, kinetoplasts can serve that role for 2D and catenated polymer systems.
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    Functional malignant cell heterogeneity in pancreatic neuroendocrine tumors revealed by targeting of PDGF-DD (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-01
    Description: Intratumoral heterogeneity is an inherent feature of most human cancers and has profound implications for cancer therapy. As a result, there is an emergent need to explore previously unmapped mechanisms regulating distinct subpopulations of tumor cells and to understand their contribution to tumor progression and treatment response. Aberrant platelet-derived growth factor receptor beta (PDGFRβ) signaling in cancer has motivated the development of several antagonists currently in clinical use, including imatinib, sunitinib, and sorafenib. The discovery of a novel ligand for PDGFRβ, platelet-derived growth factor (PDGF)-DD, opened the possibility of a previously unidentified signaling pathway involved in tumor development. However, the precise function of PDGF-DD in tumor growth and invasion remains elusive. Here, making use of a newly generated Pdgfd knockout mouse, we reveal a functionally important malignant cell heterogeneity modulated by PDGF-DD signaling in pancreatic neuroendocrine tumors (PanNET). Our analyses demonstrate that tumor growth was delayed in the absence of signaling by PDGF-DD. Surprisingly, ablation of PDGF-DD did not affect the vasculature or stroma of PanNET; instead, we found that PDGF-DD stimulated bulk tumor cell proliferation by induction of paracrine mitogenic signaling between heterogeneous malignant cell clones, some of which expressed PDGFRβ. The presence of a subclonal population of tumor cells characterized by PDGFRβ expression was further validated in a cohort of human PanNET. In conclusion, we demonstrate a previously unrecognized heterogeneity in PanNET characterized by signaling through the PDGF-DD/PDGFRβ axis.
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    Transcriptional control of amino acid homeostasis is disrupted in Huntington’s disease (2016)
    National Academy of Sciences
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    Publication Date: 2016-07-19
    Description: Disturbances in amino acid metabolism, which have been observed in Huntington’s disease (HD), may account for the profound inanition of HD patients. HD is triggered by an expansion of polyglutamine repeats in the protein huntingtin (Htt), impacting diverse cellular processes, ranging from transcriptional regulation to cognitive and motor functions. We show here that the master regulator of amino acid homeostasis, activating transcription factor 4 (ATF4), is dysfunctional in HD because of oxidative stress contributed by aberrant cysteine biosynthesis and transport. Consistent with these observations, antioxidant supplementation reverses the disordered ATF4 response to nutrient stress. Our findings establish a molecular link between amino acid disposition and oxidative stress leading to cytotoxicity. This signaling cascade may be relevant to other diseases involving redox imbalance and deficits in amino acid metabolism.
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    Spontaneous mutations in maize pollen are frequent in some lines and arise mainly from retrotranspositions and deletions (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-16
    Description: While studying spontaneous mutations at the maize bronze (bz) locus, we made the unexpected discovery that specific low-copy number retrotransposons are mobile in the pollen of some maize lines, but not of others. We conducted large-scale genetic experiments to isolate new bz mutations from several Bz stocks and recovered spontaneous stable mutations only in the pollen parent in reciprocal crosses. Most of the new stable bz mutations resulted from either insertions of low-copy number long terminal repeat (LTR) retrotransposons or deletions, the same two classes of mutations that predominated in a collection of spontaneous wx mutations [Wessler S (1997) The Mutants of Maize, pp 385–386]. Similar mutations were recovered at the closely linked sh locus. These events occurred with a frequency of 2–4 × 10−5 in two lines derived from W22 and in 4Co63, but not at all in B73 or Mo17, two inbreds widely represented in Corn Belt hybrids. Surprisingly, the mutagenic LTR retrotransposons differed in the active lines, suggesting differences in the autonomous element make-up of the lines studied. Some active retrotransposons, like Hopscotch, Magellan, and Bs2, a Bs1 variant, were described previously; others, like Foto and Focou in 4Co63, were not. By high-throughput sequencing of retrotransposon junctions, we established that retrotranposition of Hopscotch, Magellan, and Bs2 occurs genome-wide in the pollen of active lines, but not in the female germline or in somatic tissues. We discuss here the implications of these results, which shed light on the source, frequency, and nature of spontaneous mutations in maize.
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    Preclinical efficacy of a RAF inhibitor that evades paradoxical MAPK pathway activation in protein kinaseBRAF-mutant lung cancer (2016)
    National Academy of Sciences
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    Publication Date: 2016-11-09
    Description: Oncogenic activation of protein kinaseBRAFdrives tumor growth by promoting mitogen-activated protein kinase (MAPK) pathway signaling. Because oncogenic mutations inBRAFoccur in ∼2–7% of lung adenocarcinoma (LA),BRAF-mutant LA is the most frequent cause ofBRAF-mutant cancer mortality worldwide. Whereas most tumor types harbor predominantly theBRAFV600E-mutant allele, the spectrum ofBRAFmutations in LA includesBRAFV600E(∼60% of cases) and non-V600E mutant alleles (∼40% of cases) such asBRAFG469AandBRAFG466V. The presence ofBRAFV600Ein LA has prompted clinical trials testing selective BRAF inhibitors such as vemurafenib inBRAFV600E-mutant patients. Despite promising clinical efficacy, both innate and acquired resistance often result from reactivation of MAPK pathway signaling, thus limiting durable responses to the current BRAF inhibitors. Further, the optimal therapeutic strategy to block non-V600EBRAF-mutant LA remains unclear. Here, we report the efficacy of the Raf proto-oncogene serine/threonine protein kinase (RAF) inhibitor, PLX8394, that evades MAPK pathway reactivation inBRAF-mutant LA models. We show that PLX8394 treatment is effective in bothBRAFV600Eand certain non-V600 LA models, in vitro and in vivo. PLX8394 was effective against treatment-naiveBRAF-mutant LAs and those with acquired vemurafenib resistance caused by an alternatively spliced, truncatedBRAFV600Ethat promotes vemurafenib-insensitive MAPK pathway signaling. We further show that acquired PLX8394 resistance occurs via EGFR-mediated RAS-mTOR signaling and is prevented by upfront combination therapy with PLX8394 and either an EGFR or mTOR inhibitor. Our study provides a biological rationale and potential polytherapy strategy to aid the deployment of PLX8394 in lung cancer patients.
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    Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation (2016)
    National Academy of Sciences
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    Publication Date: 2016-10-24
    Description: Brown planthopper (BPH), Nilaparvata lugens Stål, is one of the most devastating insect pests of rice (Oryza sativa L.). Currently, 30 BPH-resistance genes have been genetically defined, most of which are clustered on specific chromosome regions. Here, we describe molecular cloning and characterization of a BPH-resistance gene, BPH9, mapped on the long arm of rice chromosome 12 (12L). BPH9 encodes a rare type of nucleotide-binding and leucine-rich repeat (NLR)-containing protein that localizes to the endomembrane system and causes a cell death phenotype. BPH9 activates salicylic acid- and jasmonic acid-signaling pathways in rice plants and confers both antixenosis and antibiosis to BPH. We further demonstrated that the eight BPH-resistance genes that are clustered on chromosome 12L, including the widely used BPH1, are allelic with each other. To honor the priority in the literature, we thus designated this locus as BPH1/9. These eight genes can be classified into four allelotypes, BPH1/9-1, -2, -7, and -9. These allelotypes confer varying levels of resistance to different biotypes of BPH. The coding region of BPH1/9 shows a high level of diversity in rice germplasm. Homologous fragments of the nucleotide-binding (NB) and leucine-rich repeat (LRR) domains exist, which might have served as a repository for generating allele diversity. Our findings reveal a rice plant strategy for modifying the genetic information to gain the upper hand in the struggle against insect herbivores. Further exploration of natural allelic variation and artificial shuffling within this gene may allow breeding to be tailored to control emerging biotypes of BPH.
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    Mapping hole hopping escape routes in proteins (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-24
    Description: A recently proposed oxidative damage protection mechanism in proteins relies on hole hopping escape routes formed by redox-active amino acids. We present a computational tool to identify the dominant charge hopping pathways through these residues based on the mean residence times of the transferring charge along these hopping pathways. The residence times are estimated by combining a kinetic model with well-known rate expressions for the charge-transfer steps in the pathways. We identify the most rapid hole hopping escape routes in cytochrome P450 monooxygenase, cytochrome c peroxidase, and benzylsuccinate synthase (BSS). This theoretical analysis supports the existence of hole hopping chains as a mechanism capable of providing hole escape from protein catalytic sites on biologically relevant timescales. Furthermore, we find that pathways involving the [4Fe4S] cluster as the terminal hole acceptor in BSS are accessible on the millisecond timescale, suggesting a potential protective role of redox-active cofactors for preventing protein oxidative damage.
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    Reply to Wager et al.: Pain and the dACC: The importance of hit rate-adjusted effects and posterior probabilities with fair priors (2016)
    National Academy of Sciences
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    Publication Date: 2016-04-19
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    Insights into the origin of the high energy-conversion efficiency of F1-ATPase (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-24
    Description: Our understanding of the rotary-coupling mechanism of F1-ATPase has been greatly enhanced in the last decade by advances in X-ray crystallography, single-molecular imaging, and theoretical models. Recently, Volkán-Kacsó and Marcus [S. Volkán-Kacsó, R. A. Marcus, Proc. Natl. Acad. Sci. U.S.A. 112, 14230 (2015)] presented an insightful thermodynamic model based on the Marcus reaction theory coupled with an elastic structural deformation term to explain the observed γ-rotation angle dependence of the adenosine triphosphate (ATP)/adenosine diphosphate (ADP) exchange rates of F1-ATPase. Although the model is successful in correlating single-molecule data, it is not in agreement with the available theoretical results. We describe a revision of the model, which leads to consistency with the simulation results and other experimental data on the F1-ATPase rotor compliance. Although the free energy liberated on ATP hydrolysis by F1-ATPase is rapidly dissipated as heat and so cannot contribute directly to the rotation, we show how, nevertheless, F1-ATPase functions near the maximum possible efficiency. This surprising result is a consequence of the differential binding of ATP and its hydrolysis products ADP and Pi along a well-defined pathway.
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    Homotypic cooperativity and collective binding are determinants of bHLH specificity and function (2019)
    National Academy of Sciences
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    Publication Date: 2019-07-24
    Description: Eukaryotic cells express transcription factor (TF) paralogues that bind to nearly identical DNA sequences in vitro but bind at different genomic loci and perform different functions in vivo. Predicting how 2 paralogous TFs bind in vivo using DNA sequence alone is an important open problem. Here, we analyzed 2 yeast bHLH TFs, Cbf1p and Tye7p, which have highly similar binding preferences in vitro, yet bind at almost completely nonoverlapping target loci in vivo. We dissected the determinants of specificity for these 2 proteins by making a number of chimeric TFs in which we swapped different domains of Cbf1p and Tye7p and determined the effects on in vivo binding and cellular function. From these experiments, we learned that the Cbf1p dimer achieves its specificity by binding cooperatively with other Cbf1p dimers bound nearby. In contrast, we found that Tye7p achieves its specificity by binding cooperatively with 3 other DNA-binding proteins, Gcr1p, Gcr2p, and Rap1p. Remarkably, most promoters (63%) that are bound by Tye7p do not contain a consensus Tye7p binding site. Using this information, we were able to build simple models to accurately discriminate bound and unbound genomic loci for both Cbf1p and Tye7p. We then successfully reprogrammed the human bHLH NPAS2 to bind Cbf1p in vivo targets and a Tye7p target intergenic region to be bound by Cbf1p. These results demonstrate that the genome-wide binding targets of paralogous TFs can be discriminated using sequence information, and provide lessons about TF specificity that can be applied across the phylogenetic tree.
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    IDH1 deficiency attenuates gluconeogenesis in mouse liver by impairing amino acid utilization (2016)
    National Academy of Sciences
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    Publication Date: 2016-12-23
    Description: Although the enzymatic activity of isocitrate dehydrogenase 1 (IDH1) was defined decades ago, its functions in vivo are not yet fully understood. Cytosolic IDH1 converts isocitrate to α-ketoglutarate (α-KG), a key metabolite regulating nitrogen homeostasis in catabolic pathways. It was thought that IDH1 might enhance lipid biosynthesis in liver or adipose tissue by generating NADPH, but we show here that lipid contents are relatively unchanged in both IDH1-null mouse liver and IDH1-deficient HepG2 cells generated using the CRISPR-Cas9 system. Instead, we found that IDH1 is critical for liver amino acid (AA) utilization. Body weights of IDH1-null mice fed a high-protein diet (HPD) were abnormally low. After prolonged fasting, IDH1-null mice exhibited decreased blood glucose but elevated blood alanine and glycine compared with wild-type (WT) controls. Similarly, in IDH1-deficient HepG2 cells, glucose consumption was increased, but alanine utilization and levels of intracellular α-KG and glutamate were reduced. In IDH1-deficient primary hepatocytes, gluconeogenesis as well as production of ammonia and urea were decreased. In IDH1-deficient whole livers, expression levels of genes involved in AA metabolism were reduced, whereas those involved in gluconeogenesis were up-regulated. Thus, IDH1 is critical for AA utilization in vivo and its deficiency attenuates gluconeogenesis primarily by impairing α-KG–dependent transamination of glucogenic AAs such as alanine.
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    Effective treatment of steatosis and steatohepatitis by fibroblast growth factor 1 in mouse models of nonalcoholic fatty liver disease (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-08
    Description: Nonalcoholic fatty liver disease (NAFLD) is the most common chronic liver disorder and is strongly associated with obesity and type 2 diabetes. Currently, there is no approved pharmacological treatment for this disease, but improvement of insulin resistance using peroxisome proliferator-activated receptor-γ (PPARγ) agonists, such as thiazolidinediones (TZDs), has been shown to reduce steatosis and steatohepatitis effectively and to improve liver function in patients with obesity-related NAFLD. However, this approach is limited by adverse effects of TZDs. Recently, we have identified fibroblast growth factor 1 (FGF1) as a target of nuclear receptor PPARγ in visceral adipose tissue and as a critical factor in adipose remodeling. Because FGF1 is situated downstream of PPARγ, it is likely that therapeutic targeting of the FGF1 pathway will eliminate some of the serious adverse effects associated with TZDs. Here we show that pharmacological administration of recombinant FGF1 (rFGF1) effectively improves hepatic inflammation and damage in leptin-deficient ob/ob mice and in choline-deficient mice, two etiologically different models of NAFLD. Hepatic steatosis was effectively reduced only in ob/ob mice, suggesting that rFGF1 stimulates hepatic lipid catabolism. Potentially adverse effects such as fibrosis or proliferation were not observed in these models. Because the anti-inflammatory effects were observed in both the presence and absence of the antisteatotic effects, our findings further suggest that the anti-inflammatory property of rFGF1 is independent of its effect on lipid catabolism. Our current findings indicate that, in addition to its potent glucose-lowering and insulin-sensitizing effects, rFGF1 could be therapeutically effective in the treatment of NAFLD.
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    Illusory Late Heavy Bombardments (2016)
    National Academy of Sciences
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    Publication Date: 2016-09-12
    Description: The Late Heavy Bombardment (LHB), a hypothesized impact spike at ∼3.9 Ga, is one of the major scientific concepts to emerge from Apollo-era lunar exploration. A significant portion of the evidence for the existence of the LHB comes from histograms of 40Ar/39Ar “plateau” ages (i.e., regions selected on the basis of apparent isochroneity). However, due to lunar magmatism and overprinting from subsequent impact events, virtually all Apollo-era samples show evidence for 40Ar/39Ar age spectrum disturbances, leaving open the possibility that partial 40Ar* resetting could bias interpretation of bombardment histories due to plateaus yielding misleadingly young ages. We examine this possibility through a physical model of 40Ar* diffusion in Apollo samples and test the uniqueness of the impact histories obtained by inverting plateau age histograms. Our results show that plateau histograms tend to yield age peaks, even in those cases where the input impact curve did not contain such a spike, in part due to the episodic nature of lunar crust or parent body formation. Restated, monotonically declining impact histories yield apparent age peaks that could be misinterpreted as LHB-type events. We further conclude that the assignment of apparent 40Ar/39Ar plateau ages bears an undesirably high degree of subjectivity. When compounded by inappropriate interpretations of histograms constructed from plateau ages, interpretation of apparent, but illusory, impact spikes is likely.
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    Agency plus automation: Designing artificial intelligence into interactive systems (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-04
    Description: Much contemporary rhetoric regards the prospects and pitfalls of using artificial intelligence techniques to automate an increasing range of tasks, especially those once considered the purview of people alone. These accounts are often wildly optimistic, understating outstanding challenges while turning a blind eye to the human labor that undergirds and sustains ostensibly “automated” services. This long-standing focus on purely automated methods unnecessarily cedes a promising design space: one in which computational assistance augments and enriches, rather than replaces, people’s intellectual work. This tension between human agency and machine automation poses vital challenges for design and engineering. In this work, we consider the design of systems that enable rich, adaptive interaction between people and algorithms. We seek to balance the often-complementary strengths and weaknesses of each, while promoting human control and skillful action. We share case studies of interactive systems we have developed in three arenas—data wrangling, exploratory analysis, and natural language translation—that integrate proactive computational support into interactive systems. To improve outcomes and support learning by both people and machines, we describe the use of shared representations of tasks augmented with predictive models of human capabilities and actions. We conclude with a discussion of future prospects and scientific frontiers for intelligence augmentation research.
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    Promoting axon regeneration in the adult CNS by modulation of the melanopsin/GPCR signaling (2016)
    National Academy of Sciences
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    Publication Date: 2016-02-01
    Description: Cell-type–specific G protein-coupled receptor (GPCR) signaling regulates distinct neuronal responses to various stimuli and is essential for axon guidance and targeting during development. However, its function in axonal regeneration in the mature CNS remains elusive. We found that subtypes of intrinsically photosensitive retinal ganglion cells (ipRGCs) in mice maintained high mammalian target of rapamycin (mTOR) levels after axotomy and that the light-sensitive GPCR melanopsin mediated this sustained expression. Melanopsin overexpression in the RGCs stimulated axonal regeneration after optic nerve crush by up-regulating mTOR complex 1 (mTORC1). The extent of the regeneration was comparable to that observed after phosphatase and tensin homolog (Pten) knockdown. Both the axon regeneration and mTOR activity that were enhanced by melanopsin required light stimulation and Gq/11 signaling. Specifically, activating Gq in RGCs elevated mTOR activation and promoted axonal regeneration. Melanopsin overexpression in RGCs enhanced the amplitude and duration of their light response, and silencing them with Kir2.1 significantly suppressed the increased mTOR signaling and axon regeneration that were induced by melanopsin. Thus, our results provide a strategy to promote axon regeneration after CNS injury by modulating neuronal activity through GPCR signaling.
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    Musashi-2 (MSI2) supports TGF-β signaling and inhibits claudins to promote non-small cell lung cancer (NSCLC) metastasis (2016)
    National Academy of Sciences
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    Publication Date: 2016-06-06
    Description: Non-small cell lung cancer (NSCLC) has a 5-y survival rate of ∼16%, with most deaths associated with uncontrolled metastasis. We screened for stem cell identity-related genes preferentially expressed in a panel of cell lines with high versus low metastatic potential, derived from NSCLC tumors of KrasLA1/+;P53R172HΔG/+ (KP) mice. The Musashi-2 (MSI2) protein, a regulator of mRNA translation, was consistently elevated in metastasis-competent cell lines. MSI2 was overexpressed in 123 human NSCLC tumor specimens versus normal lung, whereas higher expression was associated with disease progression in an independent set of matched normal/primary tumor/lymph node specimens. Depletion of MSI2 in multiple independent metastatic murine and human NSCLC cell lines reduced invasion and metastatic potential, independent of an effect on proliferation. MSI2 depletion significantly induced expression of proteins associated with epithelial identity, including tight junction proteins [claudin 3 (CLDN3), claudin 5 (CLDN5), and claudin 7 (CLDN7)] and down-regulated direct translational targets associated with epithelial–mesenchymal transition, including the TGF-β receptor 1 (TGFβR1), the small mothers against decapentaplegic homolog 3 (SMAD3), and the zinc finger proteins SNAI1 (SNAIL) and SNAI2 (SLUG). Overexpression of TGFβRI reversed the loss of invasion associated with MSI2 depletion, whereas overexpression of CLDN7 inhibited MSI2-dependent invasion. Unexpectedly, MSI2 depletion reduced E-cadherin expression, reflecting a mixed epithelial–mesenchymal phenotype. Based on this work, we propose that MSI2 provides essential support for TGFβR1/SMAD3 signaling and contributes to invasive adenocarcinoma of the lung and may serve as a predictive biomarker of NSCLC aggressiveness.
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    Histone H2AX promotes neuronal health by controlling mitochondrial homeostasis (2019)
    National Academy of Sciences
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    Publication Date: 2019-03-25
    Description: Phosphorylation of histone H2AX is a major contributor to efficient DNA repair. We recently reported neurobehavioral deficits in mice lacking H2AX. Here we establish that this neural failure stems from impairment of mitochondrial function and repression of the mitochondrial biogenesis gene PGC-1α. H2AX loss leads to reduced levels of the major subunits of the mitochondrial respiratory complexes in mouse embryonic fibroblasts and in the striatum, a brain region particularly vulnerable to mitochondrial damage. These defects are substantiated by disruption of the mitochondrial shape in H2AX mutant cells. Ectopic expression of PGC-1α restores mitochondrial oxidative phosphorylation complexes and mitigates cell death. H2AX knockout mice display increased neuronal death in the brain when challenged with 3-nitropronionic acid, which targets mitochondria. This study establishes a role for H2AX in mitochondrial homeostasis associated with neuroprotection.
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    Stepwise isotope editing of [FeFe]-hydrogenases exposes cofactor dynamics (2016)
    National Academy of Sciences
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    Publication Date: 2016-07-18
    Description: The six-iron cofactor of [FeFe]-hydrogenases (H-cluster) is the most efficient H2-forming catalyst in nature. It comprises a diiron active site with three carbon monoxide (CO) and two cyanide (CN−) ligands in the active oxidized state (Hox) and one additional CO ligand in the inhibited state (Hox-CO). The diatomic ligands are sensitive reporter groups for structural changes of the cofactor. Their vibrational dynamics were monitored by real-time attenuated total reflection Fourier-transform infrared spectroscopy. Combination of 13CO gas exposure, blue or red light irradiation, and controlled hydration of three different [FeFe]-hydrogenase proteins produced 8 Hox and 16 Hox-CO species with all possible isotopic exchange patterns. Extensive density functional theory calculations revealed the vibrational mode couplings of the carbonyl ligands and uniquely assigned each infrared spectrum to a specific labeling pattern. For Hox-CO, agreement between experimental and calculated infrared frequencies improved by up to one order of magnitude for an apical CN− at the distal iron ion of the cofactor as opposed to an apical CO. For Hox, two equally probable isomers with partially rotated ligands were suggested. Interconversion between these structures implies dynamic ligand reorientation at the H-cluster. Our experimental protocol for site-selective 13CO isotope editing combined with computational species assignment opens new perspectives for characterization of functional intermediates in the catalytic cycle.
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    PML plays both inimical and beneficial roles in HSV-1 replication (2016)
    National Academy of Sciences
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    Publication Date: 2016-05-09
    Description: After entry into the nucleus, herpes simplex virus (HSV) DNA is coated with repressive proteins and becomes the site of assembly of nuclear domain 10 (ND10) bodies. These small (0.1–1 μM) nuclear structures contain both constant [e.g., promyelocytic leukemia protein (PML), Sp100, death-domain associated protein (Daxx), and so forth] and variable proteins, depending on the function of the cells or the stress to which they are exposed. The amounts of PML and the number of ND10 structures increase in cells exposed to IFN-β. On initiation of HSV-1 gene expression, ICP0, a viral E3 ligase, degrades both PML and Sp100. The earlier report that IFN-β is significantly more effective in blocking viral replication in murinePML+/+cells than in siblingPML−/−cells, reproduced here with human cells, suggests that PML acts as an effector of antiviral effects of IFN-β. To define more precisely the function of PML in HSV-1 replication, we constructed aPML−/−human cell line. We report that inPML−/−cells, Sp100 degradation is delayed, possibly because colocalization and merger of ICP0 with nuclear bodies containing Sp100 and Daxx is ineffective, and that HSV-1 replicates equally well in parental HEp-2 andPML−/−cells infected at 5 pfu wild-type virus per cell, but poorly inPML−/−cells exposed to 0.1 pfu per cell. Finally, ICP0 accumulation is reduced inPML−/−infected at low, but not high, multiplicities of infection. In essence, the very mechanism that serves to degrade an antiviral IFN-β effector is exploited by HSV-1 to establish an efficient replication domain in the nucleus.
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    SIP/CacyBP promotes autophagy by regulating levels of BRUCE/Apollon, which stimulates LC3-I degradation (2019)
    National Academy of Sciences
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    Publication Date: 2019-06-18
    Description: BRUCE/Apollon is a membrane-associated inhibitor of apoptosis protein that is essential for viability and has ubiquitin-conjugating activity. On initiation of apoptosis, the ubiquitin ligase Nrdp1/RNF41 promotes proteasomal degradation of BRUCE. Here we demonstrate that BRUCE together with the proteasome activator PA28γ causes proteasomal degradation of LC3-I and thus inhibits autophagy. LC3-I on the phagophore membrane is conjugated to phosphatidylethanolamine to form LC3-II, which is required for the formation of autophagosomes and selective recruitment of substrates. SIP/CacyBP is a ubiquitination-related protein that is highly expressed in neurons and various tumors. Under normal conditions, SIP inhibits the ubiquitination and degradation of BRUCE, probably by blocking the binding of Nrdp1 to BRUCE. On DNA damage by topoisomerase inhibitors, Nrdp1 causes monoubiquitination of SIP and thus promotes apoptosis. However, on starvation, SIP together with Rab8 enhances the translocation of BRUCE into the recycling endosome, formation of autophagosomes, and degradation of BRUCE by optineurin-mediated autophagy. Accordingly, deletion of SIP in cultured cells reduces the autophagic degradation of damaged mitochondria and cytosolic protein aggregates. Thus, by stimulating proteasomal degradation of LC3-I, BRUCE also inhibits autophagy. Conversely, SIP promotes autophagy by blocking BRUCE-dependent degradation of LC3-I and by enhancing autophagosome formation and autophagic destruction of BRUCE. These actions of BRUCE and SIP represent mechanisms that link the regulation of autophagy and apoptosis under different conditions.
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    Learning the space-time phase diagram of bacterial swarm expansion (2019)
    National Academy of Sciences
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    Publication Date: 2019-01-11
    Description: Coordinated dynamics of individual components in active matter are an essential aspect of life on all scales. Establishing a comprehensive, causal connection between intracellular, intercellular, and macroscopic behaviors has remained a major challenge due to limitations in data acquisition and analysis techniques suitable for multiscale dynamics. Here, we combine a high-throughput adaptive microscopy approach with machine learning, to identify key biological and physical mechanisms that determine distinct microscopic and macroscopic collective behavior phases which develop as Bacillus subtilis swarms expand over five orders of magnitude in space. Our experiments, continuum modeling, and particle-based simulations reveal that macroscopic swarm expansion is primarily driven by cellular growth kinetics, whereas the microscopic swarming motility phases are dominated by physical cell–cell interactions. These results provide a unified understanding of bacterial multiscale behavioral complexity in swarms.
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    Quantum parity Hall effect in Bernal-stacked trilayer graphene (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-03
    Description: The quantum Hall effect has recently been generalized from transport of conserved charges to include transport of other approximately conserved-state variables, including spin and valley, via spin- or valley-polarized boundary states with different chiralities. Here, we report a class of quantum Hall effect in Bernal- or ABA-stacked trilayer graphene (TLG), the quantum parity Hall (QPH) effect, in which boundary channels are distinguished by even or odd parity under the system’s mirror reflection symmetry. At the charge neutrality point, the longitudinal conductance σxx is first quantized to 4e2/h at a small perpendicular magnetic field B⊥, establishing the presence of four edge channels. As B⊥ increases, σxx first decreases to 2e2/h, indicating spin-polarized counterpropagating edge states, and then, to approximately zero. These behaviors arise from level crossings between even- and odd-parity bulk Landau levels driven by exchange interactions with the underlying Fermi sea, which favor an ordinary insulator ground state in the strong B⊥ limit and a spin-polarized state at intermediate fields. The transitions between spin-polarized and -unpolarized states can be tuned by varying Zeeman energy. Our findings demonstrate a topological phase that is protected by a gate-controllable symmetry and sensitive to Coulomb interactions.
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    Motional dynamics of single Patched1 molecules in cilia are controlled by Hedgehog and cholesterol (2019)
    National Academy of Sciences
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    Publication Date: 2019-02-28
    Description: The Hedgehog-signaling pathway is an important target in cancer research and regenerative medicine; yet, on the cellular level, many steps are still poorly understood. Extensive studies of the bulk behavior of the key proteins in the pathway established that during signal transduction they dynamically localize in primary cilia, antenna-like solitary organelles present on most cells. The secreted Hedgehog ligand Sonic Hedgehog (SHH) binds to its receptor Patched1 (PTCH1) in primary cilia, causing its inactivation and delocalization from cilia. At the same time, the transmembrane protein Smoothened (SMO) is released of its inhibition by PTCH1 and accumulates in cilia. We used advanced, single molecule-based microscopy to investigate these processes in live cells. As previously observed for SMO, PTCH1 molecules in cilia predominantly move by diffusion and less frequently by directional transport, and spend a fraction of time confined. After treatment with SHH we observed two major changes in the motional dynamics of PTCH1 in cilia. First, PTCH1 molecules spend more time as confined, and less time freely diffusing. This result could be mimicked by a depletion of cholesterol from cells. Second, after treatment with SHH, but not after cholesterol depletion, the molecules that remain in the diffusive state showed a significant increase in the diffusion coefficient. Therefore, PTCH1 inactivation by SHH changes the diffusive motion of PTCH1, possibly by modifying the membrane microenvironment in which PTCH1 resides.
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    Segregation through the multiscalar lens (2019)
    National Academy of Sciences
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    Publication Date: 2019-05-30
    Description: We introduce a mathematical framework that allows one to carry out multiscalar and multigroup spatial exploratory analysis across urban regions. By producing coefficients that integrate information across all scales and that are normalized with respect to theoretical maximally segregated configurations, this framework provides a practical and powerful tool for the comparative empirical analysis of urban segregation. We illustrate our method with a study of ethnic mixing in the Los Angeles metropolitan area.
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    Large bandgap of pressurized trilayer graphene (2019)
    National Academy of Sciences
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    Publication Date: 2019-04-19
    Description: Graphene-based nanodevices have been developed rapidly and are now considered a strong contender for postsilicon electronics. However, one challenge facing graphene-based transistors is opening a sizable bandgap in graphene. The largest bandgap achieved so far is several hundred meV in bilayer graphene, but this value is still far below the threshold for practical applications. Through in situ electrical measurements, we observed a semiconducting character in compressed trilayer graphene by tuning the interlayer interaction with pressure. The optical absorption measurements demonstrate that an intrinsic bandgap of 2.5 ± 0.3 eV could be achieved in such a semiconducting state, and once opened could be preserved to a few GPa. The realization of wide bandgap in compressed trilayer graphene offers opportunities in carbon-based electronic devices.
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