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Cooperative Gating and Spatial Organization of Membrane Proteins through Elastic Interactions

Ursell, Tristan and Huang, Kerwin Casey and Peterson, Eric and Phillips, Rob (2007) Cooperative Gating and Spatial Organization of Membrane Proteins through Elastic Interactions. PLoS Computational Biology, 3 (5). pp. 803-812. ISSN 1553-734X. https://resolver.caltech.edu/CaltechAUTHORS:URSploscb07

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Abstract

Biological membranes are elastic media in which the presence of a transmembrane protein leads to local bilayer deformation. The energetics of deformation allow two membrane proteins in close proximity to influence each other's equilibrium conformation via their local deformations, and spatially organize the proteins based on their geometry. We use the mechanosensitive channel of large conductance (MscL) as a case study to examine the implications of bilayer-mediated elastic interactions on protein conformational statistics and clustering. The deformations around MscL cost energy on the order of 10 kBT and extend ∼3 nm from the protein edge, as such elastic forces induce cooperative gating, and we propose experiments to measure these effects. Additionally, since elastic interactions are coupled to protein conformation, we find that conformational changes can severely alter the average separation between two proteins. This has important implications for how conformational changes organize membrane proteins into functional groups within membranes.


Item Type:Article
Additional Information:© 2007 Ursell et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: February 5, 2007; Accepted: March 21, 2007; Published: May 4, 2007. We would like to thank Doug Rees, Olaf Andersen, Pierre Sens, Sergei Sukharev, Nily Dan, Jennifer Stockdill, and Ned Wingreen for their thoughtful comments on the manuscript, Chris Gandhi for his input into possible experiments, Ben Freund for useful discussion, and the useful comments of our anonymous reviewers. RP acknowledges the support of the US National Science Foundation (NSF) award CMS-0301657. TU and RP acknowledge the support of the NSF CIMMS award ACI-0204932 and NIRT award CMS-0404031, as well as the US National Institutes of Health (NIH) Director's Pioneer Award. EP was supported by the US Department of Homeland Security Graduate Fellowship program and the NIH Director's Pioneer award. KCH was supported by NIH award A1K25 GM75000. Part of this work took place at the Kavli Institute for Theoretical Physics, Santa Barbara, California, and the Aspen Center for Physics, Aspen, Colorado. Author contributions. TU conceived and designed the experiments. TU, KCH, and EP performed the experiments. TU, KCH, EP, and RP analyzed the data and contributed to writing the paper. Funding. The authors received no specific funding for this study. Competing interests. The authors have declared that no competing interests exist. The primary accession numbers (in parentheses) from the Protein Data Bank (http://www.pdb.org) are: MscL (2OAR; formerly 1MSL), gramicidin A ion channel (1GRM), bacterial potassium ion channel KscA (1F6G), and bovine rhodopsin (1GZM).
Issue or Number:5
Record Number:CaltechAUTHORS:URSploscb07
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:URSploscb07
Alternative URL:http://dx.doi.org/10.1371/journal.pcbi.0030081
Official Citation:Ursell T, Huang KC, Peterson E, Phillips R (2007) Cooperative Gating and Spatial Organization of Membrane Proteins through Elastic Interactions. PLoS Comput Biol 3(5): e81 doi:10.1371/journal.pcbi.0030081
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:8064
Collection:CaltechAUTHORS
Deposited By: Archive Administrator
Deposited On:18 Jul 2007
Last Modified:02 Oct 2019 23:47

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