Mechanosensitive channel MscS in the open state: Modeling of the transition, explicit simulations, and experimental measurements of conductance

Journal of General Physiology

Volumn 132, Issue 1, 2008, Pages 67-83

  Anishkin, Andriy ^a   Kamaraju, Kishore ^a   Sukharev, Sergei ^a  

^a University of Maryland   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ARTICLE; CHANNEL GATING; CHLORIDE CURRENT; CONDUCTANCE; ELECTRIC FIELD; ELECTROOSMOSIS; ION TRANSPORT; MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; SIMULATION;

CHLORINE; COMPUTER SIMULATION; DIFFUSION; ELECTRIC CONDUCTIVITY; ELECTROPHYSIOLOGY; ELECTROSTATICS; ESCHERICHIA COLI PROTEINS; ION CHANNEL GATING; ION CHANNELS; IONS; LIPID BILAYERS; MEMBRANE POTENTIALS; MODELS, MOLECULAR; PHOSPHATIDYLCHOLINES; POTASSIUM; PROTEIN CONFORMATION; WATER;

EID: 48749122220     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200810000     Document Type: Article

References (62)

1. Akitake, B., A. Anishkin, N. Liu, and S. Sukharev. 2007. Straightening and sequential buckling of the pore-lining helices define the gating cycle of MscS. Nat. Struct. Mol. Biol. 14:1141-1149.
2. Akitake, B., A. Anishkin, and S. Sukharev. 2005. The " dashpot" mechanism of stretch-dependent gating in MscS. J. Gen. Physiol. 125:143-154.
3. Aksimentiev, A., and K. Schulten. 2005. Imaging α-hemolysin with molecular dynamics: ionic conductance, osmotic permeability, and the electrostatic potential map. Biophys. J. 88:3745-3761.
4. Anishkin, A., B. Akitake, and S. Sukharev. 2008. Characterization of the resting MscS: modeling and analysis of the closed bacterial mechanosensitive channel of small conductance. Biophys. J. 94:1252-1266.
5. Anishkin, A., and S. Sukharev. 2004. Water dynamics and dewetting transitions in the small mechanosensitive channel MscS. Biophys. J. 86:2883-2895.
6. Bass, R.B., P. Strop, M. Barclay, and D.C. Rees. 2002. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science. 298:1582-1587.
7. 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.
8. Blount, P., I. Iscla, P.C. Moe, and Y.Z. Li. 2007. MscL: the bacterial mechanosensitive channel of large conductance. Mechanosensitive Ion Channels. Part A. 58:201-233.
9. 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.
10. Chiang, C.S., A. Anishkin, and S. Sukharev. 2004. Gating of the large mechanosensitive channel in situ: estimation of the spatial scale of the transition from channel population responses. Biophys. J. 86:2846-2861.
11. Chivian, D., D.E. Kim, L. Malmstrom, J. Schonbrun, C.A. Rohl, and D. Baker. 2005. Prediction of CASP6 structures using automated Robetta protocols. Proteins. 61(Suppl. 7):157-166.
12. Corey, D.P., and A.J. Hudspeth. 1983. Kinetics of the receptor current in bullfrog saccular hair cells. J. Neurosci. 3:962-976.
13. 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.
14. Edwards, M.D., W. Bartlett, and I.R. Booth. 2007. Pore mutations of the Escherichia coli MscS channel affect desensitisation but not ionic preference. Biophys. J.
15. Edwards, M.D., I.R. Booth, and S. Miller. 2004. Gating the bacterial mechanosensitive channels: MscS a new paradigm? Curr. Opin. Microbiol. 7:163-167.
16. Edwards, M.D., Y. Li, S. Kim, S. Miller, W. Bartlett, S. Black, S. Dennison, I. Iscla, P. Blount, J.U. Bowie, and I.R. Booth. 2005. Pivotal role of the glycine-rich TM3 helix in gating the MscS mechanosensitive channel. Nat. Struct. Mol. Biol. 12:113-119.
17. Grajkowski, W., A. Kubalski, and P. Koprowski. 2005. Surface changes of the mechanosensitive channel MscS upon its activation, inactivation, and closing. Biophys. J. 88:3050-3059.
18. Gullingsrud, J., D. Kosztin, and K. Schulten. 2001. Structural determinants of MscL gating studied by molecular dynamics simulations. Biophys. J. 80:2074-2081.
19. Gullingsrud, J., and K. Schulten. 2004. Lipid bilayer pressure profiles and mechanosensitive channel gating. Biophys. J. 86:3496-3509.
20. Hall, J.E. 1975. Access resistance of a small circular pore. J. Gen. Physiol. 66:531-532.
21. Haswell, E.S., and E.M. Meyerowitz. 2006. MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr. Biol. 16:1-11.
22. Hille, B. 1992. Ionic Channels of Excitable Membranes. Second ed. Sinauer Asssociates Inc. Sunderland, MA. 607 pp.
23. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.
24. Jorgensen, W.L., J. Chandrasekhar, and J.D. Madura. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926.
25. Klauda, J.B., N. Kucerka, B.R. Brooks, R.W. Pastor, and J.F. Nagle. 2006. Simulation-based methods for interpreting x-ray data from lipid bilayers. Biophys. J. 90:2796-2807.
26. Koprowski, P., and A. Kubalski. 2003. C termini of the Escherichia coli mechanosensitive ion channel (MscS) move apart upon the channel opening. J. Biol. Chem. 278:11237-11245.
27. Kucerka, N., S. Tristram-Nagle, and J.F. Nagle. 2006. Closer look at structure of fully hydrated fluid phase DPPC bilayers. Biophys. J. 90:L83-L85.
28. Levina, N., S. Totemeyer, N.R. Stokes, P. Louis, M.A. Jones, and I.R. Booth. 1999. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J. 18:1730-1737.
29. Li, Y., P.C. Moe, S. Chandrasekaran, I.R. Booth, and P. Blount. 2002. Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J. 21:5323-5330.
30. Lide, D.R. 2007. CRC Handbook of Chemistry and Physics. 88 ed. CRC Press, Boca Raton, FL. 2,608 pp.
31. MacKerell, A.D., D. Bashford, M. Bellott, R.L. Dunbrack, J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
32. Markin, V.S., and F. Sachs. 2004. Thermodynamics of mechanosensitivity. Phys. Biol. 1:110-124.
33. McLaggan, D., M.A. Jones, G. Gouesbet, N. Levina, S. Lindey, W. Epstein, and I.R. Booth. 2002. Analysis of the kefA2 mutation suggests that KefA is a cation-specific channel involved in osmotic adaptation in Escherichia coli. Mol. Microbiol. 43:521-536.
34. Miller, S., M.D. Edwards, C. Ozdemir, and I.R. Booth. 2003. The closed structure of the MscS mechanosensitive channel. Cross-linking of single cysteine mutants. J. Biol. Chem. 278:32246-32250.
35. Nakayama, Y., K. Fujiu, M. Sokabe, and K. Yoshimura. 2007. Molecular and electrophysiological characterization of a mechanosensitive channel expressed in the chloroplasts of Chlamydomonas. Proc. Natl. Acad. Sci. USA. 104:5883-5888.
36. Okada, K., P.C. Moe, and P. Blount. 2002. Functional design of bacterial mechanosensitive channels. Comparisons and contrasts illuminated by random mutagenesis. J. Biol. Chem. 277:27682-27688.
37. + channels. Trends Neurosci. 24:339-346.
38. Perozo, E. 2006. Gating prokaryotic mechanosensitive channels. Nat. Rev. Mol. Cell Biol. 7:109-119.
39. 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.
40. Phillips, J.C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kale, and K. Schulten. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
41. Sachs, F., and C.E. Morris. 1998. Mechanosensitive ion channels in nonspecialized cells. Rev. Physiol. Biochem. Pharmacol. 132:1-77.
42. Schumann, U., M.D. Edwards, C. Li, and I.R. Booth. 2004. The conserved carboxy-terminus of the MscS mechanosensitive channel is not essential but increases stability and activity. FEBS Lett. 572:233-237.
43. Shapovalov, G., and H.A. Lester. 2004. Gating transitions in bacterial ion channels measured at 3 μ resolution. J. Gen. Physiol. 124:151-161.
44. Smart, O.S., J.G. Neduvelil, X. Wang, B.A. Wallace, and M.S. Sansom. 1996. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14:354-360, 376.
45. Sotomayor, M., and K. Schulten. 2004. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys. J. 87:3050-3065.
46. Sotomayor, M., T.A. van der Straaten, U. Ravaioli, and K. Schulten. 2006. Electrostatic properties of the mechanosensitive channel of small conductance MscS. Biophys. J. 90:3496-3510.
47. 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.
48. Spronk, S.A., D.E. Elmore, and D.A. Dougherty. 2006. Voltage-dependent hydration and conduction properties of the hydrophobic pore of the mechanosensitive channel of small conductance. Biophys. J. 90:3555-3569.
49. Steinbacher, S., R. Bass, P. Strop, and D.C. Rees. 2007. Structures of the prokaryotic mechanosensitive channels MscL and MscS. Mechanosensitive Ion Channels. Part A. 58:1-24.
50. Sukharev, S. 2002. Purification of the small mechanosensitive channel of Escherichia coli (MscS): the subunit structure, conduction, and gating characteristics in liposomes. Biophys. J. 83:290-298.
51. Sukharev, S., B. Akitake, and A. Anishkin. 2007. The bacterial mechanosensitive channel MscS: Emerging principles of gating and modulation. Mechanosensitive Ion Channels. Part A. 58:235-267.
52. Sukharev, S., A. Anishkin, C.-S. Chiang, M. Betanzos, and H.R. Guy. 2005. MscL, a bacterial mechanosensitive channel. In Bacterial Ion Channels and their Eukaryotic Homologs. B. Martinac and A. Kubalski, editors. ASM Press, Washington, DC. 259-290.
53. Sukharev, S., M. Betanzos, C.S. Chiang, and H.R. Guy. 2001a. The gating mechanism of the large mechanosensitive channel MscL. Nature. 409:720-724.
54. Sukharev, S., S.R. Durell, and H.R. Guy. 2001b. Structural models of the mscl gating mechanism. Biophys. J. 81:917-936.
55. 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.
56. Sukharev, S.I., W.J. Sigurdson, C. Kung, and F. Sachs. 1999. Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J. Gen. Physiol. 113:525-540.
57. van der Straaten, T.A., G. Kathawala, A. Trellakis, R.S. Eisenberg, and U. Ravaioli. 2005. BioMOCA - a Boltzmann transport Monte Carlo model for ion channel simulation. Mol. Simul. 31:151-171.
58. Vasquez, V., and E. Perozo. 2004. Voltage dependent gating in MscS. Biophys. J. 86:545A.
59. Vasquez, V., M. Sotomayor, D.M. Cortes, B.S.K. Roux, and E. Perozo. 2008. Three dimensional architecture of membrane-embedded MscS in the closed conformation. J. Mol. Biol. 378:55-70.
60. Vora, T., B. Corry, and S.H. Chung. 2006. Brownian dynamics investigation into the conductance state of the MscS channel crystal structure. Biochim. Biophys. Acta. 1758:730-737.
61. Wiggins, P., and R. Phillips. 2005. Membrane-protein interactions in mechanosensitive channels. Biophys. J. 88:880-902.
62. Zhou, X.L., S.H. Loukin, R. Coria, C. Kung, and Y. Saimi. 2005. Heterologously expressed fungal transient receptor potential channels retain mechanosensitivity in vitro and osmotic response in vivo. Eur. Biophys. J. 34:413-422.