Molecular dynamics study of MscL interactions with a curved lipid bilayer

Biophysical Journal

Volumn 91, Issue 5, 2006, Pages 1630-1637

  Meyer, Grischa R ^a,b,c   Gullingsrud, Justin ^b,d   Schulten, Klaus ^b   Martinac, Boris ^a,c  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; PROTEIN MSCL; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; CONTROLLED STUDY; ESCHERICHIA COLI; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE CHANNEL; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN INTERACTION; PROTEIN STRUCTURE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33748451900     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.080721     Document Type: Article

References (53)

1. Martinac, B. 2004. Mechanosensitive ion channels: molecules of mechanotransduction. J. Cell Sci. 117:2449-2460.
2. Hamill, O., and B. Martinac. 2001. Molecular basis of mechano-transduction in living cells. Physiol. Rev. 81:685-740.
3. Sukharev, S., W. 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.
4. Häse, C., A. Le Dain, and B. Martinac. 1995. Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli. J. Biol. Chem. 270:18329-18334.
5. Maurer, J., and D. Dougherty. 2003. Generation and evaluation of a large mutational library from the Escherichia coli mechanosensitive channel of large conductance, MscL: implications for channel gating and evolutionary design. J. Biol. Chem. 278:21076-21082.
6. Yoshimura, K., A. Batiza, and C. Kung. 2001. Chemically charging the pore constriction opens the mechanosensitive channel MscL. Biophys. J. 80:2198-2206.
7. Ou, X., P. Blount, R. Hoffman, and C. Kung. 1998. One face of a transmembrane helix is crucial in mechanosensitive channel gating. Proc. Natl. Acad. Sci. USA. 95:11471-11475.
8. Blount, P., S. I. Sukharev, M. J. Schroeder, S. K. Nagle, and C. Kung. 1996. Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli. Proc. Natl. Acad. Sci. USA. 93:11652-11657.
9. Chang, G., R. Spencer, A. Lee, M. Barclay, and D. Rees. 1998. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science. 282:2220-2226.
10. Gullingsrud, J., and K. Schulten. 2003. Gating of MscL studied by steered molecular dynamics. Biophys. J. 85:2087-2099.
11. Elmore, D., and D. Dougherty. 2003. Investigating lipid composition effects on the mechanosensitive channel of large conductance (MscL) using molecular dynamics simulations. Biophys. J. 85:1512-1524.
12. Colombo, G., S. Marrink, and A. Mark. 2003. Simulation of MscL gating in a bilayer under stress. Biophys. J. 84:2331-2337.
13. Perozo, E., D. 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.
14. Perozo, E., A. Kloda, D. Cortes, and B. Martinac. 2002. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9:696-703.
15. Kong, Y., Y. Shen, T. Warth, and J. Ma. 2002. Conformational pathways in the gating of Escherichia coli mechanosensitive channel. Proc. Natl. Acad. Sci. USA. 99:5999-6004.
16. Gullingsrud, J., D. Kosztin, and K. Schulten. 2001. Structural determinants of MscL gating studied by molecular dynamics simulations. Biophys. J. 80:2074-2081.
17. Martinac, B., J. Adler, and C. Kung. 1990. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature. 348:261-263.
18. Corry, B., P. Rigby, Z. W. Liu, and B. Martinac. 2005. Conformational Changes involved in MscL channel gating measured using FRET spectroscopy. Biophys. J. 89:L49-L51.
19. Sheetz, M., and S. Singer. 1974. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA. 71:4457-4461.
20. + channel. EMBO J. 17:4283-4290.
21. Bilston, L., and K. Mylvaganam. 2002. Molecular simulations of the large conductance mechanosensitive (MscL) channel under mechanical loading. FEBS Lett. 512:185-190.
22. Frenkel, D., and B. Smit. 1996. Understanding Molecular Simulation: From Algorithms to Applications. Academic Press, San Diego, CA.
23. Sukharev, S., M. Betanzos, C. Chiang, and H. Guy. 2001. The gating mechanism of the large mechanosensitive channel MscL. Nature. 409:720-724.
24. Sukharev, S., S. Durell, and H. Guy. 2001. Structural models of the MscL gating mechanism. Biophys. J. 81:917-936.
25. Häse, C., A. Le Dain, and B. Martinac. 1997. Molecular dissection of the large mechanosensitive ion channel (MscL) of E. coli: mutants with altered channel gating and pressure sensitivity. J. Membr. Biol. 157:17-25.
26. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD-visual molecular dynamics. J. Mol. Graph. 14:33-38.
27. 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.
28. Feller, S., D. Yin, R. Pastor, and A. MacKerell Jr. 1997. Molecular dynamics simulation of unsaturated lipid bilayers at low hydration: parameterization and comparison with diffraction studies. Biophys. J. 73:2269-2279.
29. Schlenkrich, M., J. Brickmann, A. D. MacKerell Jr., and M. Karplus. 1996. Empirical potential energy function for phospholipids: Criteria for parameter optimization and applications. In Biological Membranes: A Molecular Perspective from Computation and Experiment. K. M. Merz and B. Roux, editors. Birkhauser, Boston. 31-81.
30. MacKerell, A. D. Jr., D. Bashford, M. Bellott, R. L. Dunbrack, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, D. T. Nguyen, T. Ngo, B. Prodhom, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. Straub, J. Wiorkiewiczkuczera, and M. Karplus. 1992. Self-consistent parameterization of biomolecules for molecular modeling and condensed phase simulations. FASEB J. 6:A143.
31. MacKerell, A. D. Jr., D. Bashford, M. Bellott, R. L. Dunbrack, J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher, B. Roux, M. Schlenkrich, J. C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
32. Ryckaert, J., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
33. 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.
34. Pastor, R. W., B. R. Brooks, and A. Szabo. 1988. An analysis of the accuracy of Langevin and molecular dynamics algorithms. Mol. Phys. 65:1409-1419.
35. Smart, O., J. Goodfellow, and B. Wallace. 1993. The pore dimensions of gramicidin A. Biophys. J. 65:2455-2460.
36. Feller, S. E., and R. W. Pastor. 1999. Constant surface tension simulations of lipid bilayers: The sensitivity of surface areas and compressibilities. J. Chem. Phys. 111:1281-1287.
37. Seelig, J. 1977. Deuterium magnetic resonance: theory and application to lipid membranes. Q. Rev. Biophys. 10:353-418.
38. Gullingsrud, J., and K. Schulten. 2004. Lipid bilayer pressure profiles and mechanosensitive channel gating. Biophys. J. 86:3496-3509.
39. Petrache, H. I., S. W. Dodd, and M. F. Brown. 2000. Area per Lipid and Acyl Length Distributions in Fluid Phosphatidylcholines Determined by 2H NMR Spectroscopy. Biophys. J. 79:3172-3192.
40. 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.
41. Park, K. H., C. Berrier, B. Martinac, and A. Ghazi. 2004. Purification and Functional Reconstitution of N- and C-halves of the MscL channel. Biophys. J. 86:2129-2136.
42. Tsai, I. J., Z. W. Liu, J. Rayment, C. Norman, A. McKinley, and B. Martinac. 2005. The role of the periplasmic loop residue glutamine 65 for MscL mechanosensitivity. Eur. Biophys. J. 34:403-412.
43. Sansom, M., and H. Weinstein. 2000. Hinges, swivels and switches: the role of prolines in signalling via transmembrane alpha-helices. Trends Pharmacol. Sci. 21:445-451.
44. Doyle, D. A. 2004. Structural changes during ion channel gating. Trends Neurosci. 27:298-302.
45. Valadie, H., J. Lacapcre, Y. Sanejouand, and C. Etchebest. 2003. Dynamical properties of the MscL of Escherichia coli: a normal mode analysis. J. Mol. Biol. 332:657-674.
46. Sotomayor, M., and K. Schulten. 2004. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys. J. 87:3050-3065.
47. Tieleman, D. P., L. R. Forrest, M. S. Sansom, and H. J. Berendsen. 1998. Lipid properties and the orientation of aromatic residues in OmpF, influenza M2, and alamethicin systems: molecular dynamics simulations. Biochemistry. 37:17554-17561.
48. Dumas, F., M. C. Lebrun, and J. F. Tocanne. 1999. Is the protein/lipid hydrophobic matching principle relevant to membrane organization and functions? FEBS Lett. 458:271-277.
49. Mouritsen, O. G., and M. Bloom. 1984. Mattress model of lipid-protein interactions in membranes. Biophys. J. 46:141-153.
50. Mouritsen, O. G., and M. Bloom. 1993. Models of lipid-protein interactions in membranes. Annu. Rev. Biophys. Biomol. Struct. 22:145-171.
51. Mouritsen, O. G., and M. M. Sperotto. 1993. Thermodynamics of lipid-protein interactions in lipid membranes. In The Hydrophobic Matching Condition. M. Jackson, editor. CRC Press, Boca Raton, FL.
52. Mouritsen, O. G., B. Dammann, H. C. Fogedby, J. H. Ipsen, C. Jeppesen, K. Jorgensen, J. Risbo, M. C. Sabra, M. M. Sperotto, and M. J. Zuckermann. 1995. The computer as a laboratory for the physical-chemistry of membranes. Biophys. Chem. 55:55-68.
53. Gullingsrud, J., A. Babakhani, and J. A. McCammon. 2006. Computational investigation of pressure profiles in lipid bilayers with embedded proteins. Mol. Simul. In press.