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  • 1
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    Influence of spatially segregated IP3-producing pathways on spike generation and transmitter release in Purkinje cell axons (2020)
    National Academy of Sciences
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    Publication Date: 2020-05-01
    Description: It has been known for a long time that inositol-trisphosphate (IP3) receptors are present in the axon of certain types of mammalian neurons, but their functional role has remained unexplored. Here we show that localized photolysis of IP3 induces spatially constrained calcium rises in Purkinje cell axons. Confocal immunohistology reveals that the axon initial segment (AIS), as well as terminals onto deep cerebellar cells, express specific subtypes of Gα/q and phospholipase C (PLC) molecules, together with the upstream purinergic receptor P2Y1. By contrast, intermediate parts of the axon express another set of Gα/q and PLC molecules, indicating two spatially segregated signaling cascades linked to IP3 generation. This prompted a search for distinct actions of IP3 in different parts of Purkinje cell axons. In the AIS, we found that local applications of the specific P2Y1R agonist MRS2365 led to calcium elevation, and that IP3 photolysis led to inhibition of action potential firing. In synaptic terminals on deep cerebellar nuclei neurons, we found that photolysis of both IP3 and ATP led to GABA release. We propose that axonal IP3 receptors can inhibit action potential firing and increase neurotransmitter release, and that these effects are likely controlled by purinergic receptors. Altogether our results suggest a rich and diverse functional role of IP3 receptors in axons of mammalian neurons.
    Print ISSN: 0027-8424
    Electronic ISSN: 1091-6490
    Topics: Biology , Medicine , Natural Sciences in General
    Published by National Academy of Sciences
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  • 2
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    Calcium activates the light-dependent conductance in melanopsin-expressing photoreceptors of amphioxus (2015)
    National Academy of Sciences
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    Publication Date: 2015-06-08
    Description: Melanopsin, the photopigment of the “circadian” receptors that regulate the biological clock and the pupillary reflex in mammals, is homologous to invertebrate rhodopsins. Evidence supporting the involvement of phosphoinositides in light-signaling has been garnered, but the downstream effectors that control the light-dependent conductance remain unknown. Microvillar photoreceptors of the primitive chordate amphioxus also express melanopsin and transduce light via phospholipase-C, apparently not acting through diacylglycerol. We therefore examined the role of calcium in activating the photoconductance, using simultaneous, high time-resolution measurements of membrane current and Ca2+ fluorescence. The light-induced calcium rise precedes the onset of the photocurrent, making it a candidate in the activation chain. Moreover, photolysis of caged Ca elicits an inward current of similar size, time course and pharmacology as the physiological photoresponse, but with a much shorter latency. Internally released calcium thus emerges as a key messenger to trigger the opening of light-dependent channels in melanopsin-expressing microvillar photoreceptors of early chordates.
    Print ISSN: 0027-8424
    Electronic ISSN: 1091-6490
    Topics: Biology , Medicine , Natural Sciences in General
    Published by National Academy of Sciences
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  • 3
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    Activation of light-dependent K+ channels in ciliary invertebrate photoreceptors involves cGMP but not the IP3/Ca2+ cascade (1995)
    Cell Press
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    Publication Date: 1995-09-01
    Print ISSN: 0896-6273
    Electronic ISSN: 1097-4199
    Topics: Biology , Medicine
    Published by Cell Press
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  • 4
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    Light control of G protein signaling pathways by a novel photopigment (2018)
    Public Library of Science
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    Publication Date: 2018-10-01
    Electronic ISSN: 1932-6203
    Topics: Medicine , Natural Sciences in General
    Published by Public Library of Science
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  • 5
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    Identification of a Pseudotetrameric K+-Selective CNG Channel in Amphioxus (2014)
    Cell Press
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    Publication Date: 2014-01-01
    Print ISSN: 0006-3495
    Electronic ISSN: 1542-0086
    Topics: Biology , Physics
    Published by Cell Press
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  • 6
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    A direct signaling role for phosphatidylinositol 4,5-bisphosphate (PIP2) in the visual excitation process of microvillar receptors (2009)
    American Society for Biochemistry and Molecular Biology
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    Publication Date: 2022-05-25
    Description: Author Posting. © American Society for Biochemistry and Molecular Biology, 2005. This article is posted here by permission of American Society for Biochemistry and Molecular Biology for personal use, not for redistribution. The definitive version was published in Journal of Biological Chemistry 280 (2005): 16784-16789, doi:10.1074/jbc.M414538200.
    Description: In microvillar photoreceptors the pivotal role of phospholipase C in light transduction is undisputed, but previous attempts to account for the photoresponse solely in terms of downstream products of phosphatidylinositol 4,5-bisphosphate (PIP2) hydrolysis have proved wanting. In other systems PIP2 has been shown to possess signaling functions of its own, rather than simply serving as a precursor molecule. Because illumination of microvillar photoreceptors cells leads to PIP2 break-down, a potential role for this phospholipid in phototransduction would be to help maintain some element(s) of the transduction cascade in the inactive state. We tested the effect of intracellular dialysis of PIP2 on voltage-clamped molluscan photoreceptors and found a marked reduction in the amplitude of the photocurrent; by contrast, depolarization-activated calcium and potassium currents were unaffected, thus supporting the notion of a specific effect on light signaling. In the dark, PIP2 caused a gradual outward shift of the holding current; this change was due to a decrease in membrane conductance and may reflect the suppression of basal openings of the light-sensitive conductance. The consequences of depleting PIP2 were examined in patches of light-sensitive microvillar membrane screened for the exclusive presence of light-activated ion channels. After excision, superfusion with anti-PIP2 antibodies induced the appearance of single-channel currents. Replenishment of PIP2 by exogenous application reverted the effect. These data support the notion that PIP2, in addition to being the source of inositol trisphosphate and diacylglycerol, two messengers of visual excitation, may also participate in a direct fashion in the control of the light-sensitive conductance
    Description: This work was supported by National Institutes of Health Grant EY07559.
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 7
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    Light control of G protein signaling pathways by a novel photopigment (2018)
    Public Library of Science
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 13 (2018): e0205015, doi:10.1371/journal.pone.0205015.
    Description: Channelopsins and photo-regulated ion channels make it possible to use light to control electrical activity of cells. This powerful approach has lead to a veritable explosion of applications, though it is limited to changing membrane voltage of the target cells. An enormous potential could be tapped if similar opto-genetic techniques could be extended to the control of chemical signaling pathways. Photopigments from invertebrate photoreceptors are an obvious choice—as they do not bleach upon illumination -however, their functional expression has been problematic. We exploited an unusual opsin, pScop2, recently identified in ciliary photoreceptors of scallop. Phylogenetically, it is closer to vertebrate opsins, and offers the advantage of being a bi-stable photopigment. We inserted its coding sequence and a fluorescent protein reporter into plasmid vectors and demonstrated heterologous expression in various mammalian cell lines. HEK 293 cells were selected as a heterologous system for functional analysis, because wild type cells displayed the largest currents in response to the G-protein activator, GTP-γ-S. A line of HEK cells stably transfected with pScop2 was generated; after reconstitution of the photopigment with retinal, light responses were obtained in some cells, albeit of modest amplitude. In native photoreceptors pScop2 couples to Go; HEK cells express poorly this G-protein, but have a prominent Gq/PLC pathway linked to internal Ca mobilization. To enhance pScop2 competence to tap into this pathway, we swapped its third intracellular loop—important to confer specificity of interaction between 7TMDRs and G-proteins—with that of a Gq-linked opsin which we cloned from microvillar photoreceptors present in the same retina. The chimeric construct was evaluated by a Ca fluorescence assay, and was shown to mediate a robust mobilization of internal calcium in response to illumination. The results project pScop2 as a potentially powerful optogenetic tool to control signaling pathways.
    Description: This work was funded by Colciencias grant FP44842-010-2015 and Connecticut Fund for Science.
    Repository Name: Woods Hole Open Access Server
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  • 8
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    On the gating mechanisms of the light-dependent conductance in Pecten hyperpolarizing photoreceptors : does light remove inactivation in voltage-dependent K channels? (2008)
    Rockefeller University Press
    Details
    Publication Date: 2022-05-25
    Description: © 2005 Gomez et al. This article is distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License. The definitive version was published in Journal of General Physiology 125 (2005): 455-464, doi:10.1085/jgp.200509269.
    Description: The hyperpolarizing receptor potential of ciliary photoreceptors of scallop and other mollusks is mediated by a cGMP-activated K conductance; these cells also express a transient potassium current triggered by depolarization. During steady illumination, the outward currents elicited by voltage steps lose their decay kinetics. One interesting conjecture that has been proposed is that the currents triggered by light and by depolarization are mediated by the same population of channels, and that illumination evokes the receptor potential by removing their steady-state inactivation. Exploiting the information that has become available on the phototransduction cascade of ciliary photoreceptors, we demonstrated that the same downstream signaling elements are implicated in the modulation of voltage-elicited currents: direct chemical stimulation both at the level of the G protein and of the final messenger that controls the light-dependent channels (cGMP) also attenuate the falling phase of the voltage-activated current. Application of a protein kinase G antagonist was ineffective, suggesting that a cGMP-initiated phosphorylation step is not implicated. To ascertain the commonality of ionic pathways we used pharmacological blockers. Although millimolar 4-aminopyridine (4-AP) suppressed both currents, at micromolar concentrations only the photocurrent was blocked. Conversely, barium completely and reversibly antagonized the transient voltage-activated current with no detectable effect on the light-evoked current. These results rule out that the same ionic pores mediate both currents; the mechanism of light modulation of the depolarization-evoked K current was elucidated as a time-dependent increase in the light-sensitive conductance that is superimposed on the inactivating K current.
    Description: Supported by National Institutes of Health grant EY07559
    Keywords: Photoreceptors ; CNG channel ; Potassium ion channels ; Gating, ion channels ; Blockers, potassium channel
    Repository Name: Woods Hole Open Access Server
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  • 9
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    Calcium-independent, cGMP-mediated light adaptation in invertebrate ciliary photoreceptors (2009)
    Society for Neuroscience
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    Publication Date: 2022-05-25
    Description: Author Posting. © Society for Neuroscience, 2005. This article is posted here by permission of Society for Neuroscience for personal use, not for redistribution. The definitive version was published in Journal of Neuroscience 25 (2005): 2042-2049, doi:10.1523/JNEUROSCI.5129-04.2005.
    Description: Calcium is thought to be essential for adaptation of sensory receptor cells. However, the transduction cascade of hyperpolarizing, ciliary photoreceptors of the scallop does not use IP3-mediated Ca release, and the light-sensitive conductance is not measurably permeable to Ca2+. Therefore, two typical mechanisms that couple the light response to [Ca]i changes seem to be lacking in these photoreceptors. Using fluorescent indicators, we determined that, unlike in their microvillar counterparts, photostimulation of ciliary cells under voltage clamp indeed evokes no detectable change in cytosolic Ca. Notwithstanding, these cells exhibit all of the hallmarks of light adaptation, including response range compression, sensitivity shift, and photoresponse acceleration. A possible mediator of Ca-independent sensory adaptation is cGMP, the second messenger that regulates the light-sensitive conductance; cGMP and 8-bromo cGMP not only activate light-dependent K channels but also reduce the amplitude of the light response to an extent greatly in excess of that expected from simple occlusion between light and chemical stimulation. In addition, these substances accelerate the time course of the photocurrent. Tests with pharmacological antagonists suggest that protein kinase G may be a downstream effector that controls, in part, the cGMP-triggered changes in photoresponse properties during light adaptation. However, additional messengers are likely to be implicated, especially in the regulation of response kinetics. These observations suggest a novel feedback inhibition pathway for signaling sensory adaptation.
    Description: This work was supported by National Institutes of Health Grant RO1-EY07559.
    Keywords: Photoreceptors ; Light adaptation ; Photosensitivity ; Cyclic nucleotides ; Sensory transduction ; Calcium
    Repository Name: Woods Hole Open Access Server
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  • 10
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    Prolonged calcium influx after termination of light-induced calcium release in invertebrate photoreceptors (2010)
    Rockefeller University Press
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    Publication Date: 2022-05-25
    Description: © The Authors, 2009 . This article is distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License. The definitive version was published in Journal of General Physiology 134 (2009): 177-189, doi:10.1085/jgp.200910214.
    Description: In microvillar photoreceptors, light stimulates the phospholipase C cascade and triggers an elevation of cytosolic Ca2+ that is essential for the regulation of both visual excitation and sensory adaptation. In some organisms, influx through light-activated ion channels contributes to the Ca2+ increase. In contrast, in other species, such as Lima, Ca2+ is initially only released from an intracellular pool, as the light-sensitive conductance is negligibly permeable to calcium ions. As a consequence, coping with sustained stimulation poses a challenge, requiring an alternative pathway for further calcium mobilization. We observed that after bright or prolonged illumination, the receptor potential of Lima photoreceptors is followed by the gradual development of an after-depolarization that decays in 1–4 minutes. Under voltage clamp, a graded, slow inward current (Islow) can be reproducibly elicited by flashes that saturate the photocurrent, and can reach a peak amplitude in excess of 200 pA. Islow obtains after replacing extracellular Na+ with Li+, guanidinium, or N-methyl-D-glucamine, indicating that it does not reflect the activation of an electrogenic Na/Ca exchange mechanism. An increase in membrane conductance accompanies the slow current. Islow is impervious to anion replacements and can be measured with extracellular Ca2+ as the sole permeant species; Ba can substitute for Ca2+ but Mg2+ cannot. A persistent Ca2+ elevation parallels Islow, when no further internal release takes place. Thus, this slow current could contribute to sustained Ca2+ mobilization and the concomitant regulation of the phototransduction machinery. Although reminiscent of the classical store depletion–operated calcium influx described in other cells, Islow appears to diverge in some significant aspects, such as its large size and insensitivity to SKF96365 and lanthanum; therefore, it may reflect an alternative mechanism for prolonged increase of cytosolic calcium in photoreceptors.
    Description: This work was supported by National Science Foundation grant 0639774.
    Repository Name: Woods Hole Open Access Server
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