Gating of the mechanosensitive channel protein MscL: The interplay of membrane and protein

Biophysical Journal

Volumn 94, Issue 9, 2008, Pages 3497-3511

  Jeon, Jonggu ^a,b   Voth, Gregory A ^a  

^a UNIVERSITY OF UTAH   (United States)

^b Korea University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

1 PALMITOYL 2 OLEOYLPHOSPHATIDYLETHANOLAMINE; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLETHANOLAMINE; BACTERIAL PROTEIN; ION CHANNEL; PHOSPHATIDYLETHANOLAMINE; TB MSCL PROTEIN, MYCOBACTERIUM TUBERCULOSIS; TB-MSCL PROTEIN, MYCOBACTERIUM TUBERCULOSIS;

ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE; CHANNEL GATING; CHEMISTRY; ELASTICITY; LIPID BILAYER; MECHANOTRANSDUCTION; METABOLISM; MYCOBACTERIUM TUBERCULOSIS; ROTATION;

BACTERIAL PROTEINS; CELL MEMBRANE; ELASTICITY; ION CHANNEL GATING; ION CHANNELS; LIPID BILAYERS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; MYCOBACTERIUM TUBERCULOSIS; PHOSPHATIDYLETHANOLAMINES; ROTATION;

EID: 43649090741     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.109850     Document Type: Article

References (57)

1. Hamill, O. P., and B. Martinac. 2001. Molecular basis of mechano-transduction in living cells. Physiol. Rev. 81:685-740.
2. Sukharev, S., and D. P. Corey. 2004. Mechanosensitive channels: multiplicity of families and gating paradigms. Sci. STKE. 219:re4.
3. Kung, C. 2005. A possible unifying principle for mechanosensation. Nature. 436:647-654.
4. Cruickshank, C. C., R. F. Minchin, A. C. Le Dain, and B. Martinac. 1997. Estimation of the pore size of the large-conductance mechano-sensitive ion channel of Escherichia coli. Biophys. J. 73:1925-1931.
5. Sukharev, S. I., B. Martinac, V. Y. Arshavsky, and C. Kung. 1993. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys. J. 65: 177-183.
6. Perozo, E., and D. C. Rees. 2003. Structure and mechanism in prokary-otic mechanosensitive channels. Curr. Opin. Struct. Biol. 13:432-442.
7. Chang, G., R. H. Spencer, A. T. Lee, M. T. Barclay, and D. C. Rees. 1998. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science. 282:2220-2226.
8. Steinbacher, S., R. Bass, P. Strop, and D. C. Rees. 2007. Structures of the prokaryotic mechanosensitive channels MscL and MscS. Curr. Top. Membranes. 58:1-24.
9. Sukharev, S., W. J. Sigurdson, C. Kung, and F. Sachs. 1999. Energetic and spatial parameters for gating of he bacterial large conductance mechanosensitive channel, MscL. J. Gen. Physiol. 113:525-539.
10. Moe, P. C., G. Levin, and P. Blount. 2000. Correlating a protein structure with function of a bacterial mechanosensitive channel. J. Biol. Chem. 275:31121-31127.
11. Evans, E., V. Heinrich, F. Ludwig, and W. Rawicz. 2003. Dynamic tension spectroscopy and strength of biomembranes. Biophys. J. 85: 2342-2350.
12. Perozo, E., D. M. Cortes, P. Sompornpisut, A. Kloda, and B. Martinac. 2002. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature. 418:942-948.
13. Perozo, E., A. Kloda, D. M. Cortes, and B. Martinac. 2002. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9:696-703.
14. Sukharev, S., M. Betanzos, C.-S. Chiang, and H. R. Guy. 2001. The gating mechanism of the large mechanosensitive channel MscL. Nature. 409:720-724.
15. Betanzos, M., C.-S. Chiang, H. R. Guy, and S. Sukharev. 2002. A large iris-like expansion of a mechanosensitive channel protein induced by membrane tension. Nat. Struct. Biol. 9:704-710.
16. Cantor, R. S. 1997. Lateral pressures in cell membranes: a mechanism for modulation of protein function. J. Phys. Chem. B. 101:1723-1725.
17. Gullingsrud, J., and K. Schulten. 2004. Lipid bilayer pressure profiles and mechanosensitive channel gating. Biophys. J. 86:3496-3509.
18. Iscla, I., G. Levin, R. Wray, and P. Blount. 2007. Disulfide trapping the mechanosensitive channel MscL into a gating-transition state. Biophys. J. 92:1224-1232.
19. Gullingsrud, J., D. Kosztin, and K. Schulten. 2001. Structural determinants of MscL gating studied by molecular dynamics simulations. Biophys. J. 80:2074-2081.
20. Elmore, D. E., and D. A. Dougherty. 2001. Molecular dynamics simulations of wild-type and mutant forms of the Mycobacterium tuberculosis MscL channel. Biophys. J. 81:1345-1359.
21. Bilston, L. E., and K. Mylvaganam. 2002. Molecular simulations of the large conductance mechanosensitive (MscL) channel under mechanical loading. FEBS Lett. 512:185-190.
22. Kong, Y., Y. Shen, T. E. Warth, and J. Ma. 2002. Conformational pathways in the gating of Escherichia coli mechanosensitive channel. Proc. Natl. Acad. Sci. USA. 99:5999-6004.
23. Sukharev, S., S. R. Durell, and H. R. Guy. 2001. Structural models of the MscL gating mechanism. Biophys. J. 81:917-936.
24. Elmore, D. E., and D. A. Dougherty. 2003. Investigating lipid composition effects on the mechanosensitive channel of large conductance (MscL). Using molecular dynamics simulations. Biophys. J. 85:15121524.
25. Colombo, G., S. J. Marrink, and A. E. Mark. 2003. Simulation of MscL gating in a bilayer under stress. Biophys. J. 84:2331-2337.
26. Gullingsrud, J., and K. Schulten. 2003. Gating of MscL studied by steered molecular dynamics. Biophys. J. 85:2087-2099.
27. Meyer, G. R., J. Gullingsrud, K. Schulten, and B. Martinac. 2006. Molecular dynamics study of MscL interactions with a curved lipid bilayer. Biophys. J. 91:1630-1637.
28. Sotomayor, M., V. Vasquez, E. Perozo, and K. Schulten. 2007. Ion conduction through MscS as determined by electrophysiology and simulation. Biophys. J. 92:886-902.
29. Valadié, H., J. J. Lacapčre, Y.-H. Sanejouand, and C. Etchebest. 2003. Dynamical properties of the MscL of Escherichia coli: a normal mode analysis. J. Mol. Biol. 332:657-674.
30. Markin, V. S., and F. Sachs. 2004. Thermodynamics of mechanosen-sitivity. Phys. Biol. 1:110-124.
31. Wiggins, P., and R. Phillips. 2004. Analytic models for mechano-transduction: Gating a mechanosensitive channel. Proc. Natl. Acad. Sci. USA. 101:4071-1076.
32. Wiggins, P., and R. Phillips. 2005. Membrane-protein interactions in mechanosensitive channels. Biophys. J. 88:880-902.
33. Tang, Y., G. Cao, X. Chen, J. Yoo, A. Yethiraj, and Q. Cui. 2006. A finite element framework for studying the mechanical response of macromolecules: application to the gating of the mechanosensitive channel MscL. Biophys. J. 91:1248-1263.
34. Jeon, J., and G. A. Voth. 2005. The dynamic stress responses to area change in planar lipid bilayer membranes. Biophys. J. 88:11041119.
35. Levin, G., and P. Blount. 2004. Cysteine scanning of MscL transmembrane domains reveals residues critical for mechanosensitive channel gating. Biophys. J. 86:2862-2870.
36. Bartlett, J. L., G. Levin, and P. Blount. 2004. An in vivo assay identifies changes in residue accessibility on mechanosensitive channel gating. Proc. Natl. Acad. Sci. USA. 101:10161-10165.
37. Iscla, I., G. Levin, R. Wray, R. Reynolds, and P. Blount. 2004. Defining the physical gate of a mechanosensitive channel, MscL, by engineering metal-binding sites. Biophys. J. 87:3172-3180.
38. Tieleman, D. P., and H. J. C. Berendsen. 1998. A molecular dynamics study of the pores formed by Escherichia coli OmpF porin in a fully hydrated palmitoyloleoylphosphatidylcholine bilayer. Biophys. J. 74: 2786-2801.
39. Moe, P., and P. Blount. 2005. Assessment of potential stimuli for mechano-dependent gating of MscL: effects of pressure, tension, and lipid headgroups. Biochemistry. 44:12239-12244.
40. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, and J. Hermans. 1981. Interaction models for water in relation to protein hydration. In Intermolecular Forces. B. Pullman, editor. Reidel, Dordrecht. 331-342.
41. Ajouz, B., C. Berrier, M. Besnard, B. Martinac, and A. Ghazi. 2000. Contributions of the different extramembranous domains of the mechanosensitive ion channel MscL to its response to membrane tension. J. Biol. Chem. 275:1015-1022.
42. Berger, O., O. Edholm, and F. Jahnig. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72:2002-2013.
43. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
44. Spoel, D. V. D., E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, and H. J. C. Berendsen. 2005. GROMACS: fast, flexible, and free. J. Comput. Chem. 26:1701-1718.
45. Nosé, S. 1984. A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys. 52:255-268.
46. Hoover, W. G. 1985. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A. 31:1695-1697.
47. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. DiNola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
48. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
49. Smart, O. S., J. G. Neduvelila, X. Wanga, B. A. Wallacea, and M. S. P. Sansom. 1996. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14:354-360.
50. Egberts, E., and H. J. C. Berendsen. 1988. Molecular dynamics simulation of a smectic liquid crystal with atomic detail. J. Chem. Phys. 89:3718-3732.
51. Evans, E., and D. Needham. 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion, and colloidal interactions. J. Phys. Chem. 91:4219-4228.
52. Rawicz, W., K. C. Olbrich, T. Mcintosh, D. Needham, and E. Evans. 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79:328-339.
53. Powl, A. M., J. M. East, and A. G. Lee. 2007. Different effects of lipid chain length on the two sides of a membrane and the lipid annulus of MscL. Biophys. J. 93:113-122.
54. Anishkin, A., C.-S. Chiang, and S. Sukharev. 2005. Gain-of-function mutations reveal expanded intermediate states and a sequential action of two gates in MscL. J. Gen. Physiol. 125:155-170.
55. Anishkin, A., and S. Sukharev. 2004. Water dynamics and dewetting transitions in the small mechanosensitive channel MscS. Biophys. J. 86:2883-2895.
56. Liu, P., X. Huang, R. Zhou, and B. J. Berne. 2005. Observation of a dewetting transition in the collapse of the melittin tetramer. Nature. 437:159-162.
57. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.