High-throughput simulations reveal membrane-mediated effects of alcohols on MscL gating

Melo, Manuel N.; Arnarez, Clement; Sikkema, Hendrik; Kumar, Neeraj; Walko, Martin; Berendsen, Herman J. C.; Kocer, Armagan; Marrink, Siewert J.; Ingolfsson, Helgi I.

doi:10.1021/jacs.6b11091

Title: High-throughput simulations reveal membrane-mediated effects of alcohols on MscL gating

Journal Article · 25 January 2017 · Journal of the American Chemical Society

DOI: https://doi.org/10.1021/jacs.6b11091 · OSTI ID:1346131

Melo, Manuel N. ^[1]; Arnarez, Clement ^[1]; Sikkema, Hendrik ^[1]; Kumar, Neeraj ^[1]; Walko, Martin ^[1]; Berendsen, Herman J. C. ^[1]; Kocer, Armagan ^[1]; Marrink, Siewert J. ^[1];

^[2]

Univ. of Groningen, Groningen (The Netherlands)
Univ. of Groningen, Groningen (The Netherlands); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

The mechanosensitive channels of large conductance (MscL) are bacterial membrane proteins that serve as last resort emergency release valves in case of severe osmotic downshock. Sensing bilayer tension, MscL channels are sensitive to changes in the bilayer environment and are, therefore, an ideal test case for exploring membrane protein coupling. Here, we use high-throughput coarse-grained molecular dynamics simulations to characterize MscL gating kinetics in different bilayer environments under the influence of alcohols. We performed over five hundred simulations to obtain sufficient statistics to reveal the subtle effects of changes in the membrane environment on MscL gating. MscL opening times were found to increase with the addition of the straight-chain alcohols ethanol, octanol, and to some extent dodecanol but not with hexadecanol. Increasing concentration of octanol increased the impeding effect, but only up to 10–20 mol %. Our in silico predictions were experimentally confirmed using reconstituted MscL in a liposomal fluorescent efflux assay. Our combined data reveal that the effect of alcohols on MscL gating arises not through specific binding sites but through a combination of the alcohol-induced changes to a number of bilayer properties and their alteration of the MscL–bilayer interface. Finally, our work provides a key example of how extensive molecular simulations can be used to predict the functional modification of membrane proteins by subtle changes in their bilayer environment.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1346131

Report Number(s):: LLNL-JRNL--715277

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 7 Vol. 139; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Packing properties of 1-alkanols and alkanes in a phospholipid membrane Aagaard, Thomas H.; Kristensen, Mette N.; Westh, Peter Biophysical Chemistry, Vol. 119, Issue 1 https://doi.org/10.1016/j.bpc.2005.09.003	journal	January 2006
Modulation of KvAP Unitary Conductance and Gating by 1-Alkanols and Other Surface Active Agents Finol-Urdaneta, Rocio K.; McArthur, Jeffrey R.; Juranka, Peter F. Biophysical Journal, Vol. 98, Issue 5 https://doi.org/10.1016/j.bpj.2009.10.053	journal	March 2010
Protein Shape Change Has a Major Effect on the Gating Energy of a Mechanosensitive Channel Samuli Ollila, O. H.; Louhivuori, Martti; Marrink, Siewert J. Biophysical Journal, Vol. 100, Issue 7 https://doi.org/10.1016/j.bpj.2011.02.027	journal	April 2011
Membrane Tension, Lipid Adaptation, Conformational Changes, and Energetics in MscL Gating Rui, Huan; Kumar, Ritesh; Im, Wonpil Biophysical Journal, Vol. 101, Issue 3 https://doi.org/10.1016/j.bpj.2011.06.029	journal	August 2011
Alcohol's Effects on Lipid Bilayer Properties Ingólfsson, Helgi I.; Andersen, Olaf S. Biophysical Journal, Vol. 101, Issue 4 https://doi.org/10.1016/j.bpj.2011.07.013	journal	August 2011
Sensing and Responding to Membrane Tension: The Bacterial MscL Channel as a Model System Iscla, Irene; Blount, Paul Biophysical Journal, Vol. 103, Issue 2 https://doi.org/10.1016/j.bpj.2012.06.021	journal	July 2012
The Nanomechanical Properties of Lipid Membranes are Significantly Influenced by the Presence of Ethanol Stetter, Frank W. S.; Hugel, Thorsten Biophysical Journal, Vol. 104, Issue 5 https://doi.org/10.1016/j.bpj.2013.01.021	journal	March 2013
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Computational Lipidomics with insane : A Versatile Tool for Generating Custom Membranes for Molecular Simulations Wassenaar, Tsjerk A.; Ingólfsson, Helgi I.; Böckmann, Rainer A. Journal of Chemical Theory and Computation, Vol. 11, Issue 5 https://doi.org/10.1021/acs.jctc.5b00209	journal	April 2015
Assessment of Potential Stimuli for Mechano-Dependent Gating of MscL: Effects of Pressure, Tension, and Lipid Headgroups ^† Moe, Paul; Blount, Paul Biochemistry, Vol. 44, Issue 36 https://doi.org/10.1021/bi0509649	journal	September 2005
Phytochemicals Perturb Membranes and Promiscuously Alter Protein Function Ingólfsson, Helgi I.; Thakur, Pratima; Herold, Karl F. ACS Chemical Biology, Vol. 9, Issue 8 https://doi.org/10.1021/cb500086e	journal	June 2014
Sidekick for Membrane Simulations: Automated Ensemble Molecular Dynamics Simulations of Transmembrane Helices Hall, Benjamin A.; Halim, Khairul Bariyyah Abd; Buyan, Amanda Journal of Chemical Theory and Computation, Vol. 10, Issue 5 https://doi.org/10.1021/ct500003g	journal	April 2014
High-Throughput Simulations of Dimer and Trimer Assembly of Membrane Proteins. The DAFT Approach Wassenaar, Tsjerk A.; Pluhackova, Kristyna; Moussatova, Anastassiia Journal of Chemical Theory and Computation, Vol. 11, Issue 5 https://doi.org/10.1021/ct5010092	journal	March 2015
GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation Hess, Berk; Kutzner, Carsten; van der Spoel, David Journal of Chemical Theory and Computation, Vol. 4, Issue 3 https://doi.org/10.1021/ct700301q	journal	February 2008
The MARTINI Coarse-Grained Force Field: Extension to Proteins Monticelli, Luca; Kandasamy, Senthil K.; Periole, Xavier Journal of Chemical Theory and Computation, Vol. 4, Issue 5 https://doi.org/10.1021/ct700324x	journal	April 2008
Coarse Grained Model for Semiquantitative Lipid Simulations Marrink, Siewert J.; de Vries, Alex H.; Mark, Alan E. The Journal of Physical Chemistry B, Vol. 108, Issue 2 https://doi.org/10.1021/jp036508g	journal	January 2004
The MARTINI Force Field: Coarse Grained Model for Biomolecular Simulations Marrink, Siewert J.; Risselada, H. Jelger; Yefimov, Serge The Journal of Physical Chemistry B, Vol. 111, Issue 27 https://doi.org/10.1021/jp071097f	journal	July 2007
Influence of Ethanol on Lipid Membranes: From Lateral Pressure Profiles to Dynamics and Partitioning Terama, Emma; Ollila, O. H. Samuli; Salonen, Emppu The Journal of Physical Chemistry B, Vol. 112, Issue 13 https://doi.org/10.1021/jp0750811	journal	April 2008
Lateral Pressures in Cell Membranes: A Mechanism for Modulation of Protein Function Cantor, Robert S. The Journal of Physical Chemistry B, Vol. 101, Issue 10 https://doi.org/10.1021/jp963911x	journal	March 1997
Mechanosensitive ion channels of E. coli activated by amphipaths Martinac, Boris; Adler, Julius; Kung, Ching Nature, Vol. 348, Issue 6298 https://doi.org/10.1038/348261a0	journal	November 1990
A large-conductance mechanosensitive channel in E. coli encoded by mscL alone Sukharev, Sergei I.; Blount, Paul; Martinac, Boris Nature, Vol. 368, Issue 6468 https://doi.org/10.1038/368265a0	journal	March 1994
Synthesis and utilization of reversible and irreversible light-activated nanovalves derived from the channel protein MscL Koçer, Armağan; Walko, Martin; Feringa, Ben L. Nature Protocols, Vol. 2, Issue 6 https://doi.org/10.1038/nprot.2007.196	journal	May 2007
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Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating Perozo, Eduardo; Kloda, Anna; Cortes, D. Marien Nature Structural Biology, Vol. 9, Issue 9 https://doi.org/10.1038/nsb827	journal	August 2002
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Coarse-grained simulation: a high-throughput computational approach to membrane proteins Sansom, Mark S. P.; Scott, Kathryn A.; Bond, Peter J. Biochemical Society Transactions, Vol. 36, Issue 1 https://doi.org/10.1042/BST0360027	journal	January 2008
Molecular dynamics with coupling to an external bath Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F. The Journal of Chemical Physics, Vol. 81, Issue 8 https://doi.org/10.1063/1.448118	journal	October 1984
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Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS Nomura, T.; Cranfield, C. G.; Deplazes, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 22 https://doi.org/10.1073/pnas.1200051109	journal	May 2012
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