Force transduction and lipid binding in MscL: A continuum-molecular approach

Vanegas, Juan M.; Arroyo, Marino; Fotiadis, Dimitrios

doi:10.1371/journal.pone.0113947

Force transduction and lipid binding in MscL: A continuum-molecular approach

Journal Article · Mon Dec 01 00:00:00 EST 2014 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0113947· OSTI ID:1214236

Vanegas, Juan M. ^[1]; Arroyo, Marino ^[1]; Fotiadis, Dimitrios ^[2]

Univ. Politecnica de Catalunya-Barcelona Tech, Barcelona (Spain)
Univ. of Bern (Switzerland)

The bacterial mechanosensitive channel MscL, a small protein mainly activated by membrane tension, is a central model system to study the transduction of mechanical stimuli into chemical signals. Mutagenic studies suggest that MscL gating strongly depends on both intra-protein and interfacial lipid-protein interactions. However, there is a gap between this detailed chemical information and current mechanical models of MscL gating. Here, we investigate the MscL bilayer-protein interface through molecular dynamics simulations, and take a combined continuum-molecular approach to connect chemistry and mechanics. We quantify the effect of membrane tension on the forces acting on the surface of the channel, and identify interactions that may be critical in the force transduction between the membrane and MscL. We find that the local stress distribution on the protein surface is largely asymmetric, particularly under tension, with the cytoplasmic side showing significantly larger and more localized forces, which pull the protein radially outward. The molecular interactions that mediate this behavior arise from hydrogen bonds between the electronegative oxygens in the lipid headgroup and a cluster of positively charged lysine residues on the amphipathic S1 domain and the C-terminal end of the second trans-membrane helix. We take advantage of this strong interaction (estimated to be 10–13 kT per lipid) to actuate the channel (by applying forces on protein-bound lipids) and explore its sensitivity to the pulling magnitude and direction. We conclude by highlighting the simple motif that confers MscL with strong anchoring to the bilayer, and its presence in various integral membrane proteins including the human mechanosensitive channel K2P1 and bovine rhodopsin.

View Accepted Manuscript (DOE)

Research Organization:: Sandia National Laboratories (SNL), Albuquerque, NM, and Livermore, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1214236

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 12 Vol. 9; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
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Force transduction and lipid binding in MscL: A continuum-molecular approach

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