Investigating lipid composition effects on the mechanosensitive channel of large conductance (MscL) using molecular dynamics simulations

Biophysical Journal

Volumn 85, Issue 3, 2003, Pages 1512-1524

  Elmore, Donald E ^a   Dougherty, Dennis A ^a,b  

^a California Institute of Technology   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; HYDROGEN BOND; LIPID COMPOSITION; LIPID MEMBRANE; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN LIPID INTERACTION;

MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 0041320859     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74584-6     Document Type: Article

References (67)

1. 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.
2. Ajouz, B., C. Berrier, A. Garrigues, M. Besnard, and A. Ghazi. 1998. Release of thioredoxin via the mechanosensitive channel MscL during osmotic downshock of Escherichia coli cells. J. Biol. Chem. 273:26670-26674.
3. Arbuzova, A., L. Wang, J. Wang, G. Hangyás-Mihályné, D. Murray, B. Honig, and S. McLaughlin. 2000. Membrane binding of peptides containing both basic and aromatic residues. Experimental studies with peptides corresponding to the scaffolding region of caveolin and the effector region of MARCKS. Biochemistry. 39:10330-10339.
4. Batiza, A. F., I. Rayment, and C. Kung. 1999. Channel gate! Tension, leak, and disclosure. Structure. 7:R99-R103.
5. 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.
6. Berendsen, H. J. C., D. van der Spoel, and R. van Drunen. 1995. GROMACS: a message-passing parallel molecular dynamics implementation. Comp. Phys. Comm. 91:43-56.
7. Berger, O., O. Edholm, and F. Jähnig. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72:2002-2013.
8. Berrier, C., A. Garrigues, G. Richarme, and A. Ghazi. 2000. Elongation factor Tu and DnaK are transferred from the cytoplasm to the periplasm of Escherichia coli during osmotic downshock presumably via the mechanosensitive channel MscL. J. Bacteriol. 182:248-251.
9. Bilston, L. E., and K. Mylvaganam. 2002. Molecular simulations of the large conductance mechanosensitive (MscL) channel under mechanical loading. FEBS Lett. 512:185-190.
10. 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.
11. Capener, C. E., and M. S. P. Sansom. 2002. Molecular dynamics simulations of a K channel model: sensitivity to changes in ions, waters, and membrane environment. J. Phys. Chem. B. 106:4545-4551.
12. 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.
13. Cruickshank, C. C., R. F. Minchin, A. C. LeDain, and B. Martinac. 1997. Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. Biophys. J. 73:1925-1931.
14. Daffé, M., and P. Draper. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39:131-203.
15. Darden, T. D., 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.
16. 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.
17. Faraldo-Gómez, J. D., G. R. Smith, and M. S. P. Sansom. 2002. Setting up and optimization of membrane protein simulations. Eur. Biophys. J. 31:217-227.
18. Feller, S. E., R. W. Pastor, A. Rojnuckarin, S. Bogusz, and B. R. Brooks. 1996. Effect of electrostatic force truncation on interfacial and transport properties of water. J. Phys. Chem. 100:17011-17020.
19. Forrest, L. R., and M. S. P. Sansom. 2000. Membrane simulations: bigger and better? Curr. Opin. Struct. Biol. 10:174-181.
20. Gullingsrud, J., D. Kosztin, and K. Schulten. 2001. Structural determinants of MscL gating studied by molecular dynamics simulations. Biophys. J. 80:2074-2081.
21. Hamill, O. P., and B. Martinac. 2001. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81:685-740.
22. Häse, C. C., A. C. 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.
23. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comp. Chem. 18:1463-1472.
24. Khuller, G. K., R. Taneja, S. Kaur, and J. N. Verma. 1982. Lipid composition and virulence of Mycobacterium tuberculosis H37rv. Aust. J. Exp. Biol. Med. Sci. 60:541-547.
25. Kloda, A., and B. Martinac. 2001. Mechanosensitive channel of Thermoplasma, the cell wall-less archaea: cloning and molecular characterization. Cell Biochem. Biophys. 34:321-347.
26. Kochendoerfer, G. G., J. M. Tack, and S. Cressman. 2002. Total chemical synthesis of a 27 kDa TASP protein derived from the MscL ion channel of M. tuberculosis by ketoxime-forming ligation. Bioconjugate Chem. 13:474-480.
27. Lanéelle, M. A., D. Promé, G. Lanéelle, and J. C. Promé. 1990. Ornithine lipid of Mycobacterium tuberculosis: its distribution in some slow-growing and fast-growing mycobacteria. J. Gen. Microbiol. 136:773-778.
28. Lee, R. E., P. J. Brennan, and G. S. Besra. 1996. Mycobacterium tuberculosis cell envelope. Curr. Top. Microbiol. Immunol. 215:1-27.
29. Levina, N., S. Tötemeyer, 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.
30. Lewis, B. A., and D. M. Engelman. 1983. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211-217.
31. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Mod. 7:306-317.
32. Maurer, J. A., and D. A. Dougherty. 2001. A high-throughput screen for MscL channel activity and mutational phenotyping. Biochim. Biophys. Acta. 1514:165-169.
33. Maurer, J. A., and D. A. Dougherty. 2003. Generation and evaluation of a large mutational library from the E. coli mechanosensitive channel of large conductance, MscL. Implications for channel gating and evolutionary design. J. Biol. Chem. 278:21076-21082
34. Maurer, J. A., D. E. Elmore, H. A. Lester, and D. A. Dougherty. 2000. Comparing and contrasting Escherichia coli and Mycobacterium tuberculosis mechanosensitive channels (MscL): new gain of function mutations in the loop region. J. Biol. Chem. 275:22238-22244.
35. Mihailescu, D., and J. C. Smith. 2000. Atomic detail peptide-membrane interactions: molecular dynamics simulation of gramicidin S in a DMPC bilayer. Biophys. J. 79:1718-1730.
36. Miyamoto, S., and P. A. Kollman. 1992. SETTLE: an analytical version of the SHAKE and RATTLE algorithms for rigid water models. J. Comp. Chem. 13:952-962.
37. Moe, P. C., P. Blount, and C. Kung. 1998. Functional and structural conservation in the mechanosensitive channel MscL implicates elements crucial for mechanosensation. Mol. Microbiol. 28:583-592.
38. 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.
39. Murray, D., L. Hermida-Matsumoto, C. A. Buser, J. Tsang, C. T. Sigal, N. Ben-Tal, B. Honig, M. D. Resh, and S. McLaughlin. 1998. Electrostatics and the membrane association of Src: theory and experiment. Biochemistry. 37:2145-2159.
40. Murray, D., and B. Honig. 2002. Electrostatic control of the membrane targeting of C2 domains. Mol. Cell. 9:145-154.
41. Nakamaru, Y., Y. Takahashi, T. Unemoto, and T. Nakamura. 1999. Mechanosensitive channel functions to alleviate the cell lysis of marine bacterium, Vibrio alginolyticus, by osmotic downshock. FEBS Lett. 444:170-172.
42. Perozo, E., D. M. Cortes, P. Sompompisut, A. Kloda, and B. Martinac. 2002a. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature. 418:942-948.
43. Perozo, E., A. Kloda, D. M. Cortes, and B. Martinac. 2001. Site-directed spin-labeling analysis of reconstituted MscL in the closed state. J. Gen. Physiol. 118:193-205.
44. Perozo, E., A. Kloda, D. M. Cortes, and B. Martinac. 2002b. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9:696-703.
45. Petrache, H. I., S. W. Dodd, and M. F. Brown. 2000a. Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by H-2 NMR spectroscopy. Biophys. J. 79:3172-3192.
46. Petrache, H. I., A. Grossfield, K. R. MacKenzie, D. M. Engelman, and T. B. Woolf. 2000b. Modulation of glycophorin A transmembrane helix interactions by lipid bilayers: molecular dynamics calculations. J. Mol. Biol. 302:727-746.
47. Petrache, H. I., D. M. Zuckerman, J. N. Sachs, J. A. Killian, R. E. I. Koeppe, and T. B. Woolf. 2002. Hydrophobic matching mechanism investigated by molecular dynamics simulations. Langmuir. 18:1340-1351.
48. Raetz, C. R. 1978. Enzymology, genetics, and regulation of membrane phospholipid synthesis in Escherichia coli. Microbiol. Rev. 42:614-659.
49. Rand, R. P., and V. A. Parsegian. 1989. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta. 988:351-376.
50. Roux, B. 2002. Theoretical and computational models of ion channels. Curr. Opin. Struct. Biol. 12:182-189.
51. Shrivastava, I. H., and M. S. P. Sansom. 2000. Simulations of ion permeation through a potassium channel: molecular dynamics of KcsA in a phospholipid bilayer. Biophys. J. 78:557-570.
52. + ions in a K channel selectivity filter: a simulation study. Biophys. J. 83:633-645.
53. Smart, O. S., J. Breed, G. R. Smith, and M. S. P. Samson. 1997. A novel method for structure-based predictions of ion channel conductance properties. Biophys. J. 72:1109-1126.
54. Spencer, R. H., G. Chang, and D. C. Rees. 1999. "Feeling the pressure": structural insights into a gated mechanosensitive channel. Curr. Opin. Struct. Biol. 9:448-454.
55. 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.
56. Sukharev, S., S. R. Durell, and H. R. Guy. 2001b. Structural models of the MscL gating mechanism. Biophys. J. 81:917-936.
57. 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.
58. 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. 113:525-539.
59. 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.
60. Tieleman, D. P., L. R. Forrest, M. S. P. Sansom, and H. J. C. Berendsen. 1998. Lipid properties and the orientation of aromatic residues in OmpF, influenza M2, and alamethicin systems: molecular dynamics simulations. Biochemistry. 37:17554-17561.
61. Tieleman, D. P., I. H. Shrivastava, M. R. Ulmschneider, and M. S. P. Sansom. 2001. Proline-induced hinges in transmembrane helices: possible roles in ion channel gating. Prot. Struct. Funct. Gen. 44:63-72.
62. van Dalen, A., S. Hegger, J. A. Killian, and B. de Kruijff. 2002. Influence of lipids on membrane assembly and stability of the potassium channel KcsA. FEBS Lett. 525:33-38.
63. Vasquez-Laslop, N., H. Lee, R. Hu, and A. A. Neyfakh. 2001. Molecular sieve mechanism of selective release of cytoplasmic proteins by osmotically shocked Escherichia coli. J. Bacteriol. 183:2399-2404.
64. Wilkinson, S. G. 1972. Composition and structure of omithine-containing lipid from Pseudomonas rubescens. Biochim. Biophys. Acta. 270:1-17.
65. Wood, J. M. 1999. Osmosensing by bacteria: signals and membrane-based sensors. Microbiol. Mol. Biol. Rev. 63:230-262.
66. Woolf, T. B. 1998. Molecular dynamics simulations of individual α-helices of bacteriorhodopsin in dimyristoylphosphatidylcholine. II. Interaction energy analysis. Biophys. J. 74:115-131.
67. Zhu, F., E. Tajkhorshid, and K. Schulten. 2001. Molecular dynamics study of aquaporin-1 water channel in a lipid bilayer. FEBS Lett. 504:212-218.