The Bacterial Mechanosensitive Channel MscS: Emerging Principles of Gating and Modulation

Current Topics in Membranes

Volumn 58, Issue , 2007, Pages 235-267

  Sukharev, Sergei ^a   Akitake, Bradley ^a   Anishkin, Andriy ^a  

^a University of Maryland   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 34047095894     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1063-5823(06)58009-3     Document Type: Review

References (76)

1. Akitake B., Anishkin A., and Sukharev S. The "dashpot" mechanism of stretch-dependent gating in MscS. J. Gen. Physiol. 125 (2005) 143-154
2. Akitake B., Spelbrink R.E., Anishkin A., Killian J.A., de Kruijff B., and Sukharev S. 2,2,2-Trifluoroethanol changes the transition kinetics and subunit interactions in the small bacterial mechanosensitive channel MscS. Biophys. J. (2005) (in press)
3. Anishkin A., and Sukharev S. Water dynamics and dewetting transitions in the small mechanosensitive channel MscS. Biophysics 86 (2004) 2883-2895
4. Barry J.A., and Gawrisch K. Direct NMR evidence for ethanol binding to the lipid-water interface of phospholipid bilayers. Biochemistry 33 (1994) 8082-8088
5. Bass R.B., Strop P., Barclay M., and Rees D.C. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298 (2002) 1582-1587
6. Beckstein O., and Sansom M.S. Liquid-vapor oscillations of water in hydrophobic nanopores. Proc. Natl. Acad. Sci. USA 100 (2003) 7063-7068
7. Beckstein O., Biggin P.C., and Sansom M.S.P. A hydrophobic gating mechanism for nanopores. J. Phys. Chem. B 105 (2001) 12902-12905
8. Berrier C., Besnard M., Ajouz B., Coulombe A., and Ghazi A. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J. Membr. Biol. 151 (1996) 175-187
9. Blount P., Sukharev S.I., Moe P.C., Martinac B., and Kung C. Mechanosensitive channels of bacteria. Methods Enzymol. 294 (1999) 458-482
10. Booth I.R., and Louis P. Managing hypoosmotic stress: Aquaporins and mechanosensitive channels in Escherichia coli. Curr. Opin. Microbiol. 2 (1999) 166-169
11. Booth I.R., Edwards M.D., and Miller S. Bacterial ion channels. Biochemistry 42 (2003) 10045-10053
12. Britten R.J., and McClure F.T. The amino acid pool in Escherichia coli. Bacteriol. Rev. 26 (1962) 292-335
13. Chang G., Spencer R.H., Lee A.T., Barclay M.T., and Rees D.C. Structure of the MscL homolog from Mycobacterium tuberculosis: A gated mechanosensitive ion channel. Science 282 (1998) 2220-2226
14. Chernomordik L.V., Sukharev S.I., Popov S.V., Pastushenko V.F., Sokirko A.V., Abidor I.G., and Chizmadzhev Y.A. The electrical breakdown of cell and lipid-membranes-the similarity of phenomenologies. Biochim. Biophys. Acta 902 (1987) 360-373
15. Chiang C.S., Anishkin A., and Sukharev S. Gating of the large mechanosensitive channel in situ: Estimation of the spatial scale of the transition from channel population responses. Biophysics 86 (2004) 2846-2861
16. Csonka L.N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53 (1989) 121-147
17. Csonka L.N., and Hanson A.D. Prokaryotic osmoregulation: Genetics and physiology. Annu. Rev. Microbiol. 45 (1991) 569-606
18. Cui C., and Adler J. Effect of mutation of potassium-efflux system, KefA, on mechanosensitive channels in the cytoplasmic membrane of Escherichia coli. J. Membr. Biol. 150 (1996) 143-152
19. Cui C., Smith D.O., and Adler J. Characterization of mechanosensitive channels in Escherichia coli cytoplasmic membrane by whole-cell patch clamp recording. J. Membr. Biol. 144 (1995) 31-42
20. de Planque M.R., Bonev B.B., Demmers J.A., Greathouse D.V., Koeppe R.E., Separovic F., Watts A., and Killian J.A. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 42 (2003) 5341-5348
21. Dzubiella J., Allen R.J., and Hansen J.P. Electric field-controlled water permeation coupled to ion transport through a nanopore. J. Chem. Phys. 120 (2004) 5001-5004
22. Edwards M.D., Booth I.R., and Miller S. Gating the bacterial mechanosensitive channels: MscS a new paradigm?. Curr. Opin. Microbiol. 7 (2004) 163-167
23. Edwards M.D., Li Y., Kim S., Miller S., Bartlett W., Black S., Dennison S., Iscla I., Blount P., Bowie J.U., and Booth I.R. Pivotal role of the glycine-rich TM3 helix in gating the MscS mechanosensitive channel. Nat. Struct. Mol. Biol. 12 (2005) 113-119
24. Epstein W. The roles and regulation of potassium in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 75 (2003) 293-320
25. Ferguson G.P., Battista J.R., Lee A.T., and Booth I.R. Protection of the DNA during the exposure of Escherichia coli cells to a toxic metabolite: The role of the KefB and KefC potassium channels. Mol. Microbiol. 35 (2000) 113-122
26. Fraczkiewicz R., and Braun W. Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comput. Chem. 19 (1998) 319-333
27. Grajkowski W., Kubalski A., and Koprowski P. Surface changes of the mechanosensitive channel MscS upon its activation, inactivation, and closing. Biophysics 88 (2005) 3050-3059
28. Hall J.E. Access resistance of a small circular pore. J. Gen. Physiol. 66 (1975) 531-532
29. Hamill O.P., Marty A., Neher E., Sakmann B., and Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391 (1981) 85-100
30. Haswell E.S., and Meyerowitz E.M. MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr. Biol. 16 (2006) 1-11
31. Hille B. "Ionic Channels of Excitable Membranes." (1992), Sinauer Asssociates Inc., Sunderland, MA
32. Hummer G., Rasaiah J.C., and Noworyta J.P. Water conduction through the hydrophobic channel of a carbon nanotube. Nature 414 (2001) 188-190
33. Koch A.L., and Woeste S. Elasticity of the sacculus of Escherichia coli. J. Bacteriol. 174 (1992) 4811-4819
34. Koenig B.W., and Gawrisch K. Lipid-ethanol interaction studied by NMR on bicelles. J. Phys. Chem. B 109 (2005) 7540-7547
35. Koprowski P., and Kubalski A. Voltage-independent adaptation of mechanosensitive channels in Escherichia coli protoplasts. J. Membr. Biol. 164 (1998) 253-262
36. Koprowski P., and Kubalski A. C termini of the Escherichia coli mechanosensitive ion channel (MscS) move apart upon the channel opening. J. Biol. Chem. 278 (2003) 11237-11245
37. Levina N., Totemeyer S., Stokes N.R., Louis P., Jones M.A., and Booth I.R. 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 (1999) 1730-1737
38. Li Y., Moe P.C., Chandrasekaran S., Booth I.R., and Blount P. Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J. 21 (2002) 5323-5330
39. Markin V.S., and Martinac B. Mechanosensitive ion channels as reporters of bilayer expansion. A theoretical model. Biophysics 60 (1991) 1120-1127
40. Martinac B. Mechanosensitive channels in prokaryotes. Cell Physiol. Biochem. 11 (2001) 61-76
41. Martinac B., Buechner M., Delcour A.H., Adler J., and Kung C. Pressure-sensitive ion channel in Escherichia coli. Proc. Natl. Acad. Sci. USA 84 (1987) 2297-2301
42. Martinac B., Adler J., and Kung C. Mechanosensitive ion channels of, E. coli activated by amphipaths. Nature 348 (1990) 261-263
43. McLaggan D., Naprstek J., Buurman E.T., and Epstein W. Interdependence of K + and glutamate accumulation during osmotic adaptation of Escherichia coli. J. Biol. Chem. 269 (1994) 1911-1917
44. McLaggan D., Jones M.A., Gouesbet G., Levina N., Lindey S., Epstein W., and Booth I.R. Analysis of the kefA2 mutation suggests that KefA is a cation-specific channel involved in osmotic adaptation in Escherichia coli. Mol. Microbiol. 43 (2002) 521-536
45. Miller S., Bartlett W., Chandrasekaran S., Simpson S., Edwards M., and Booth I.R. Domain organization of the MscS mechanosensitive channel of Escherichia coli. EMBO J. 22 (2003) 36-46
46. Miller S., Edwards M.D., Ozdemir C., and Booth I.R. The closed structure of the MscS mechanosensitive channel. Cross-linking of single cysteine mutants. J. Biol. Chem. 278 (2003) 32246-32250
47. Nomura T., Yoshimura K., and Sokabe M. Exploring the lipid-protein interface essential to the mechanosensitivity of MscS, a mechanosensitive channel from, E. coli. Biophys. J. 88 (2005) 290A
48. Nomura T., Yoshimura K., and Sokabe M. Voltage dependence of the adaptation in mscS occurs independent of the charged residues in the transmembrane domain. Biophys. J. 90 (2006) XXA
49. Okada K., Moe P.C., and Blount P. Functional design of bacterial mechanosensitive channels. Comparisons and contrasts illuminated by random mutagenesis. J. Biol. Chem. 277 (2002) 27682-27688
50. Perozo E., Kloda A., Cortes D.M., and Martinac B. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9 (2002) 696-703
51. Pivetti C.D., Yen M.R., Miller S., Busch W., Tseng Y.H., Booth I.R., and Saier Jr. M.H. Two families of mechanosensitive channel proteins. Microbiol. Mol. Biol. Rev. 67 (2003) 66-85 table
52. Ruthe H.J., and Adler J. Fusion of bacterial spheroplasts by electric fields. Biochim. Biophys. Acta 819 (1985) 105-113
53. Sachs F., and Morris C.E. Mechanosensitive ion channels in nonspecialized cells. Rev. Physiol. Biochem. Pharmacol. 132 (1998) 1-77
54. Schleyer M., Schmid R., and Bakker E.P. Transient, specific and extremely rapid release of osmolytes from growing cells of Escherichia coli K-12 exposed to hypoosmotic shock. Arch. Microbiol. 160 (1993) 424-431
55. Schumann U., Edwards M.D., Li C., and Booth I.R. The conserved carboxy-terminus of the MscS mechanosensitive channel is not essential but increases stability and activity. FEBS Lett. 572 (2004) 233-237
56. Shapovalov G., and Lester H.A. Gating transitions in bacterial ion channels measured at 3 micros resolution. J. Gen. Physiol. 124 (2004) 151-161
57. Sheetz M.P., and Singer S.J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA 71 (1974) 4457-4461
58. Smart O.S., Neduvelil J.G., Wang X., Wallace B.A., and Sansom M.S. HOLE: A program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14 (1996) 354-360 376
59. Sotomayor M., and Schulten K. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophysics 87 (2004) 3050-3065
60. Sotomayor M., van der Straaten T.A., Ravaioli U., and Schulten K. Electrostatic properties of the mechanosensitive channel of small conductance MscS. Biophysics 90 (2006) 3496-3510
61. Spelbrink R.E., Kolkman A., Slijper M., Killian J.A., and de K.B. Detection and identification of stable oligomeric protein complexes in Escherichi coli inner membranes: A proteomics approach. J. Biol. Chem. 280 (2005) 28742-28748
62. Spronk S.A., Elmore D.E., and Dougherty D.A. Voltage-dependent hydration and conduction properties of the hydrophobic pore of the mechanosensitive channel of small conductance. Biophysics 90 (2006) 3555-3569
63. Stewart G.R., Patel J., Robertson B.D., Rae A., and Young D.B. Mycobacterial mutants with defective control of phagosomal acidification. PLoS Pathog. 1 (2005) 269-278
64. Strandberg E., Ozdirekcan S., Rijkers D.T., van der Wel P.C., Koeppe R.E., Liskamp R.M., and Killian J.A. Tilt angles of transmembrane model peptides in oriented and non-oriented lipid bilayers as determined by 2H solid-state NMR. Biophysics 86 (2004) 3709-3721
65. Strop P., Bass R., and Rees D.C. Prokaryotic mechanosensitive channels. Adv. Protein Chem. 63 (2003) 177-209
66. Sukharev S. Purification of the small mechanosensitive channel of Escherichia coli (MscS): The subunit structure, conduction, and gating characteristics in liposomes. Biophysics 83 (2002) 290-298
67. Sukharev S.I., Martinac B., Arshavsky V.Y., and Kung C. Two types of mechanosensitive channels in the Escherichia coli cell envelope: Solubilization and functional reconstitution. Biophysics 65 (1993) 177-183
68. Sukharev S.I., Blount P., Martinac B., Blattner F.R., and Kung C. A large-conductance mechanosensitive channel in, E. coli encoded by mscL alone. Nature 368 (1994) 265-268
69. Tieleman D.P., Leontiadou H., Mark A.E., and Marrink S.J. Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. J. Am. Chem. Soc. 125 (2003) 6382-6383
70. Tsapis A., and Kepes A. Transient breakdown of the permeability barrier of the membrane of Escherichia coli upon hypoosmotic shock. Biochim. Biophys. Acta 469 (1977) 1-12
71. van der Straaten T.A., Kathawala G., Trellakis A., Eisenberg R.S., and Ravaioli U. BioMOCA-a Boltzmann transport Monte Carlo model for ion channel simulation. Mol. Simul. 31 (2005) 151-171
72. Vasquez V., and Perozo E. Voltage dependent gating in MscS. Biophys. J. 86 (2004) 545A
73. Vora T., Corry B., and Chung S.H. Brownian dynamics investigation into the conductance state of the MscS channel crystal structure. Biochim. Biophys. Acta. 1758 (2006) 730-737
74. Wesson L., and Eisenberg D. Atomic solvation parameters applied to molecular dynamics of proteins in solution. Protein Sci. 1 (1992) 227-235
75. Wood J.M. Osmosensing by bacteria: Signals and membrane-based sensors. Microbiol. Mol. Biol. Rev. 63 (1999) 230-262
76. Wood J.M., Bremer E., Csonka L.N., Kraemer R., Poolman B., van der H.T., and Smith L.T. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem. Physiol. A Mol. Integr. Physiol. 130 (2001) 437-460