Publication Date:
2014-07-22
Description:
The proton gradient is a principal energy source for respiration-dependent active transport, but the structural mechanisms of proton-coupled transport processes are poorly understood. YiiP is a proton-coupled zinc transporter found in the cytoplasmic membrane of Escherichia coli. Its transport site receives protons from water molecules that gain access to its hydrophobic environment and transduces the energy of an inward proton gradient to drive Zn(II) efflux. This membrane protein is a well-characterized member of the family of cation diffusion facilitators that occurs at all phylogenetic levels. Here we show, using X-ray-mediated hydroxyl radical labelling of YiiP and mass spectrometry, that Zn(II) binding triggers a highly localized, all-or-nothing change of water accessibility to the transport site and an adjacent hydrophobic gate. Millisecond time-resolved dynamics reveal a concerted and reciprocal pattern of accessibility changes along a transmembrane helix, suggesting a rigid-body helical re-orientation linked to Zn(II) binding that triggers the closing of the hydrophobic gate. The gated water access to the transport site enables a stationary proton gradient to facilitate the conversion of zinc-binding energy to the kinetic power stroke of a vectorial zinc transport. The kinetic details provide energetic insights into a proton-coupled active-transport reaction.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4144069/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4144069/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Gupta, Sayan -- Chai, Jin -- Cheng, Jie -- D'Mello, Rhijuta -- Chance, Mark R -- Fu, Dax -- P30 DK089502/DK/NIDDK NIH HHS/ -- P30-EB-09998/EB/NIBIB NIH HHS/ -- R01 GM065137/GM/NIGMS NIH HHS/ -- R01-EB-09688/EB/NIBIB NIH HHS/ -- R01GM065137/GM/NIGMS NIH HHS/ -- UL1 TR000439/TR/NCATS NIH HHS/ -- England -- Nature. 2014 Aug 7;512(7512):101-4. doi: 10.1038/nature13382. Epub 2014 Jun 22.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉1] Center for Synchrotron Biosciences and Center for Proteomics and Bioinformatics, Case Western Reserve University, Cleveland, Ohio 44109, USA [2] Berkeley Center for Structural Biology, Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA. ; Biology Department, Brookhaven National Laboratory, Upton, New York 11973, USA. ; Department of Physiology, Johns Hopkins School of Medicine, Baltimore, Maryland 21205, USA. ; Center for Synchrotron Biosciences and Center for Proteomics and Bioinformatics, Case Western Reserve University, Cleveland, Ohio 44109, USA. ; 1] Biology Department, Brookhaven National Laboratory, Upton, New York 11973, USA [2] Department of Physiology, Johns Hopkins School of Medicine, Baltimore, Maryland 21205, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/25043033" target="_blank"〉PubMed〈/a〉
Keywords:
Binding Sites
;
Biological Transport, Active
;
Escherichia coli Proteins/*chemistry/*metabolism
;
Hydrophobic and Hydrophilic Interactions
;
Hydroxyl Radical
;
Ion Transport
;
Kinetics
;
Mass Spectrometry
;
Membrane Transport Proteins/*chemistry/*metabolism
;
Models, Molecular
;
Protein Binding
;
Protein Conformation
;
*Protons
;
Pulse Radiolysis
;
Water/metabolism
;
X-Rays
;
Zinc/*metabolism
Print ISSN:
0028-0836
Electronic ISSN:
1476-4687
Topics:
Biology
,
Chemistry and Pharmacology
,
Medicine
,
Natural Sciences in General
,
Physics
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