The effect of local bending on gating of MscL using a representative volume element and finite element simulation

Channels

Volumn 8, Issue 4, 2014, Pages 344-349

  Bavi, Omid ^a   Vossoughi, Manouchehr ^a,b   Naghdabadi, Reza ^a   Jamali, Yousef ^c,d  

^a SHARIF UNIVERSITY OF TECHNOLOGY   (Iran)

^b Biochemical and Bioenvironmental Research Center (BBRC)   (Iran)

^c TARBIAT MODARES UNIVERSITY   (Iran)

^d INSTITUTE FOR RESEARCH IN FUNDAMENTAL SCIENCES IPM   (Iran)

Author keywords

Bending; Continuum mechanics; Finite element; Gating mechanism; Lipid bilayer; Local curvature; MscL

Indexed keywords

BACTERIAL PROTEIN; LIPID BILAYER; LYSOPHOSPHATIDYLCHOLINE;

BIOMECHANICS; CHANNEL GATING; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; FINITE ELEMENT ANALYSIS; LIPID BILAYER; METABOLISM; PRESSURE;

BACTERIAL PROTEINS; BIOMECHANICAL PHENOMENA; COMPUTER SIMULATION; FINITE ELEMENT ANALYSIS; ION CHANNEL GATING; LIPID BILAYERS; LYSOPHOSPHATIDYLCHOLINES; MOLECULAR CONFORMATION; PRESSURE;

EID: 84905824797     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.29572     Document Type: Article

References (41)

1. Phillips R, Ursell T, Wiggins P, Sens P. Emerging roles for lipids in shaping membrane-protein function. Nature 2009; 459:379-85; PMID:19458714; http://dx.doi.org/10.1038/nature08147
2. nd, Andersen OS. Hydrophobic coupling of lipid bilayer energetics to channel function. J Gen Physiol 2003; 121:477-93; PMID:12719487; http://dx.doi.org/10.1085/jgp.200308797
3. Meyer GR, Gullingsrud J, Schulten K, Martinac B. Molecular dynamics study of MscL interactions with a curved lipid bilayer. Biophys J 2006; 91:1630-7; PMID:16751236; http://dx.doi.org/10.1529/biophysj.106.080721
4. Nomura T, Cranfield CG, Deplazes E, Owen DM, Macmillan A, Battle AR, Constantine M, Sokabe M, Martinac B. Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci U S A 2012; 109:8770-5; PMID:22586095; http://dx.doi.org/10.1073/pnas.1200051109
5. Martinac B. The ion channels to cytoskeleton connection as potential mechanism of mechanosensitivity. Biochim Biophys Acta 2014;1838:682-91 PMID:23886913
6. Martinac B. Bacterial mechanosensitive channels as a paradigm for mechanosensory transduction. Cell Physiol Biochem 2011; 28:1051-60; PMID:22178995; http://dx.doi.org/10.1159/000335842
7. Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 1994; 368:265-8; PMID:7511799; http://dx.doi.org/10.1038/368265a0
8. Berrier C, Besnard M, Ajouz B, Coulombe A, Ghazi A. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J Membr Biol 1996; 151:175-87; PMID:8661505; http://dx.doi.org/10.1007/s002329900068
9. Martinac B, Hamill OP. Gramicidin A channels switch between stretch activation and stretch inactivation depending on bilayer thickness. Proc Natl Acad Sci U S A 2002; 99:4308-12; PMID:11904391; http://dx.doi.org/10.1073/pnas. 072632899
10. Corry B, Rigby P, Liu ZW, Martinac B. Conformational changes involved in MscL channel gating measured using FRET spectroscopy. Biophys J 2005; 89:L49-51; PMID:16199508; http://dx.doi.org/10.1529/biophysj.105.072009
11. Corry B, Hurst AC, Pal P, Nomura T, Rigby P, Martinac B. An improved open-channel structure of MscL determined from FRET confocal microscopy and simulation. J Gen Physiol 2010; 136:483-94; PMID:20876362; http://dx.doi.org/10. 1085/jgp.200910376
12. Perozo E, Cuello LG, Cortes DM, Liu YS, Sompornpisut P. EPR approaches to ion channel structure and function. Novartis Found Symp 2002; 245:146-58, discussion 158-64, 165-8; PMID:12027005; http://dx.doi.org/10.1002/0470868759. ch10
13. Perozo E, Cortes DM, Sompornpisut P, Kloda A, Martinac B. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 2002; 418:942-8; PMID:12198539; http://dx.doi.org/10.1038/nature00992
14. Sukharev S, Betanzos M, Chiang CS, Guy HR. The gating mechanism of the large mechanosensitive channel MscL. Nature 2001; 409:720-4; PMID:11217861; http://dx.doi.org/10.1038/35055559
15. Hamill OP, Martinac B. Molecular basis of mechanotransduction in living cells. Physiol Rev 2001; 81:685-740; PMID:11274342
16. Perozo E, Kloda A, Cortes DM, Martinac B. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 2002; 9:696-703; PMID:12172537; http://dx.doi.org/10. 1038/nsb827
17. Chen X, Cui Q, Tang Y, Yoo J, Yethiraj A. Gating mechanisms of mechanosensitive channels of large conductance, I: a continuum mechanics-based hierarchical framework. Biophys J 2008; 95:563-80; PMID:18390626; http://dx.doi.org/10.1529/biophysj.107.128488
18. ANSYS I. ANSYS 12.1 Manual. 2009.
19. Smart OS, Neduvelil JG, Wang X, Wallace BA, Sansom MS. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph 1996; 14:354-60, 376; PMID:9195488; http://dx.doi.org/10.1016/S0263- 7855(97)00009-X
20. Tang Y, Cao G, Chen X, Yoo J, Yethiraj A, Cui Q. A finite element framework for studying the mechanical response of macromolecules: application to the gating of the mechanosensitive channel MscL. Biophys J 2006; 91:1248-63; PMID:16731564; http://dx.doi.org/10.1529/biophysj.106.085985
21. Tang Y, Yoo J, Yethiraj A, Cui Q, Chen X. Gating mechanisms of mechanosensitive channels of large conductance, II: systematic study of conformational transitions. Biophys J 2008; 95:581-96; PMID:18390625; http://dx.doi.org/10.1529/biophysj.107.128496
22. Behfar K, Naghdabadi R. Nanoscale vibrational analysis of a multi-layered graphene sheet embedded in an elastic medium. Compos Sci Technol 2005; 65:1159-64; http://dx.doi.org/10.1016/j.compscitech.2004.11.011
23. Sadeghi M, Naghdabadi R. Nonlinear vibrational analysis of single-layer graphene sheets. Nanotechnology 2010; 21:105705; PMID:20154368; http://dx.doi.org/10.1088/0957-4484/21/10/105705
24. Wiggins P, Phillips R. Membrane-protein interactions in mechanosensitive channels. Biophys J 2005; 88:880-902; PMID:15542561; http://dx.doi.org/10.1529/ biophysj.104.047431
25. Tang Y, Cao G, Chen X, Yoo J, Yethiraj A, Cui Q. A finite element framework for studying the mechanical response of macromolecules: application to the gating of the mechanosensitive channel MscL. Biophys J 2006; 91:1248-63; PMID:16731564; http://dx.doi.org/10.1529/biophysj.106.085985
26. Yefimov S, van der Giessen E, Onck PR, Marrink SJ. Mechanosensitive membrane channels in action. Biophys J 2008; 94:2994-3002; PMID:18192351; http://dx.doi.org/10.1529/biophysj.107.119966
27. Rodowicz KA, Francisco H, Layton B. Determination of the mechanical properties of DOPC:DOPS liposomes using an image procession algorithm and micropipette-aspiration techniques. Chem Phys Lipids 2010; 163:787-93; PMID:20863821; http://dx.doi.org/10.1016/j.chemphyslip.2010.09.004
28. Cantor RS. Membrane lateral pressures: A physical mechanism of general anesthesia. [-Mpo.]. Biophys J 1997; 72:Mpo98
29. Sukharev S, Corey DP. Mechanosensitive channels: multiplicity of families and gating paradigms. Sci STKE 2004; 2004:re4; PMID:14872099
30. Patel AJ, Honoré E, Maingret F, Lesage F, Fink M, Duprat F, Lazdunski M. A mammalian two pore domain mechano-gated S-like K+ channel. EMBO J 1998; 17:4283-90; PMID:9687497; http://dx.doi.org/10.1093/emboj/17.15.4283
31. Kung C. A possible unifying principle for mechanosensation. Nature 2005; 436:647-54; PMID:16079835; http://dx.doi.org/10.1038/nature03896
32. Yoo J, Cui Q. Curvature generation and pressure profile modulation in membrane by lysolipids: insights from coarse-grained simulations. Biophys J 2009; 97:2267-76; PMID:19843459; http://dx.doi.org/10.1016/j.bpj.2009.07.051
33. Perozo E, Cortes DM, Sompornpisut P, Kloda A, Martinac B. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 2002; 418:942-8; PMID:12198539; http://dx.doi.org/10.1038/nature00992
34. Perozo E, Kloda A, Cortes DM, Martinac B. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 2002; 9:696-703; PMID:12172537; http://dx.doi.org/10. 1038/nsb827
35. Sheetz MP, Singer SJ. Biological membranes as bilayer couples. A molecular mechanism of drugerythrocyte interactions. Proc Natl Acad Sci U S A 1974; 71:4457-61; PMID:4530994; http://dx.doi.org/10.1073/pnas.71.11.4457
36. Martinac B, Adler J, Kung C. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 1990; 348:261-3; PMID:1700306; http://dx.doi.org/10.1038/348261a0
37. Brohawn SG, Su Z, MacKinnon R. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. Proc Natl Acad Sci U S A 2014; 111:3614-9; PMID:24550493; http://dx.doi.org/10.1073/pnas.1320768111
38. Shaikh S, Cox CD, Nomura T, Martinac B. Energetics of gating MscS by membrane tension in azolectin liposomes and giant spheroplasts. Channels (Austin) 2014; 8;In press; PMID:24758942; http://dx.doi.org/10.4161/chan.28366
39. Nilius B, Honoré E. Sensing pressure with ion channels. Trends Neurosci 2012; 35:477-86; PMID:22622029; http://dx.doi.org/10.1016/j.tins.2012. 04.002
40. Bähring R, Covarrubias M. Mechanisms of closed-state inactivation in voltage-gated ion channels. J Physiol 2011; 589:461-79; PMID:21098008; http://dx.doi.org/10.1113/jphysiol.2010.191965
41. Nomura T, Cranfield CG, Deplazes E, Owen DM, Macmillan A, Battle AR, Constantine M, Sokabe M, Martinac B. Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci U S A 2012; 109:8770-5; PMID:22586095; http://dx.doi.org/10.1073/pnas.1200051109