The mechanoelectrical response of the cytoplasmic membrane of Vibrio cholerae

Journal of General Physiology

Volumn 142, Issue 1, 2013, Pages 75-85

  Rowe, Ian ^a   Elahi, Merina ^a   Huq, Anwar ^a   Sukharev, Sergei ^a,b  

^a Bldg 142   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI PROTEIN; ION CHANNEL; MSCL PROTEIN, E COLI; MSCS PROTEIN, E COLI;

ACTION POTENTIAL; CELL MEMBRANE; ESCHERICHIA COLI; MECHANOTRANSDUCTION; METABOLISM; OSMOTIC PRESSURE; PHYSIOLOGY; PRESSURE; SPHEROPLAST; VIBRIO CHOLERAE;

ACTION POTENTIALS; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ION CHANNELS; MECHANOTRANSDUCTION, CELLULAR; OSMOTIC PRESSURE; PRESSURE; SPHEROPLASTS; VIBRIO CHOLERAE;

EID: 84880009597     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201310985     Document Type: Article

References (51)

1. Akitake, B., A. Anishkin, and S. Sukharev. 2005. The "dashpot" mechanism of stretch-dependent gating in MscS. J. Gen. Physiol. 125:143-154. http://dx.doi.org/10.1085/jgp.200409198
2. 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. http:// dx.doi.org/10.1038/nsmb1341
3. Anishkin, A., V. Gendel, N.A. Sharifi, C.S. Chiang, L. Shirinian, H.R. Guy, and S. Sukharev. 2003. On the conformation of the COOH-terminal domain of the large mechanosensitive channel MscL. J. Gen. Physiol. 121:227-244. http://dx.doi.org/10.1085/jgp .20028768
4. Anishkin, A., K. Kamaraju, and S. Sukharev. 2008. Mechanosensitive channel MscS in the open state: Modeling of the transition, explicit simulations, and experimental measurements of conductance. J. Gen. Physiol. 132:67-83. http://dx.doi.org/10.1085/jgp .200810000
5. Barcina, I. 1995. Survival strategies of enteric bacteria in aquatic systems. Microbiologia. 11:389-392.
6. Berrier, C., M. Besnard, B. Ajouz, A. Coulombe, and A. Ghazi. 1996. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J. Membr. Biol. 151:175-187. http://dx.doi.org/10.1007/s002329900068
7. Bialecka-Fornal, M., H.J. Lee, H.A. DeBerg, C.S. Gandhi, and R. Phillips. 2012. Single-cell census of mechanosensitive channels in living bacteria. PLoS ONE. 7:e33077. http://dx.doi.org/10.1371/ journal.pone.0033077
8. Boer, M., A. Anishkin, and S. Sukharev. 2011. Adaptive MscS gating in the osmotic permeability response in E. coli: the question of time. Biochemistry. 50:4087-4096. http://dx.doi.org/10.1021/ bi1019435
9. Boucher, P.A., C.E. Morris, and B. Joós. 2009. Mechanosensitive closed-closed transitions in large membrane proteins: osmoprotection and tension damping. Biophys. J. 97:2761-2770. http:// dx.doi.org/10.1016/j.bpj.2009.08.054
10. Britten, R.J., and F.T. McClure. 1062. The amino acid pool in Escherichia coli. Bacteriol. Rev. 26:292-335.
11. Chaiyanan, S., S. Chaiyanan, A. Huq, T. Maugel, and R.R. Colwell. 2001. Viability of the nonculturable Vibrio cholerae O1 and O139. Syst. Appl. Microbiol. 24:331-341. http://dx.doi.org/10.1078/ 0723-2020-00032
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. http://dx.doi.org/10.1126/science.282.5397 .2220
13. 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. http://dx.doi.org/10.1016/S0006-3495 (04)74337-4
14. Csonka, L.N., and A.D. Hanson. 1991. Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 45:569-606. http://dx.doi.org/10.1146/annurev.mi.45.100191.003033
15. Duret, G., and A.H. Delcour. 2006. Deoxycholic acid blocks vibrio cholerae OmpT but not OmpU porin. J. Biol. Chem. 281:19899- 19905. http://dx.doi.org/10.1074/jbc.M602426200
16. Duret, G., V. Simonet, and A.H. Delcour. 2007. Modulation of Vibrio cholerae porin function by acidic pH. Channels (Austin). 1: 70-79.
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. http:// dx.doi.org/10.1529/biophysj.104.053546
18. Grim, C.J., N.A. Hasan, E. Taviani, B. Haley, J. Chun, T.S. Brettin, D.C. Bruce, J.C. Detter, C.S. Han, O. Chertkov, et al. 2010. Genome sequence of hybrid Vibrio cholerae O1 MJ-1236, B-33, and CIRS101 and comparative genomics with V. cholerae. J. Bacteriol. 192:3524-3533. http://dx.doi.org/10.1128/JB.00040-10
19. Gullingsrud, J., and K. Schulten. 2003. Gating of MscL studied by steered molecular dynamics. Biophys. J. 85:2087-2099. http:// dx.doi.org/10.1016/S0006-3495(03)74637-2
20. Hall, J.E. 1975. Access resistance of a small circular pore. J. Gen. Physiol. 66:531-532. http://dx.doi.org/10.1085/jgp.66.4.531
21. Heidelberg, J.F., J.A. Eisen, W.C. Nelson, R.A. Clayton, M.L. Gwinn, R.J. Dodson, D.H. Haft, E.K. Hickey, J.D. Peterson, L. Umayam, et al. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature. 406:477-483. http://dx.doi.org/ 10.1038/35020000
22. Hille, B. 2001. Ionic Channels of Excitable Membranes. Third edition. Sinauer Asssociates, Inc., Sunderland, MA. 814 pp.
23. Huq, A., and C.J. Grim. 2011. Aquatic realm and cholera. In Epidemiological and Molecular Aspects on Cholera (Infectious Disease). T. Ramamurthy and S.K. Bhattachrya, editors. Springer, New York. 311-340.
24. Kamaraju, K., V. Belyy, I. Rowe, A. Anishkin, and S. Sukharev. 2011. The pathway and spatial scale for MscS inactivation. J. Gen. Physiol. 138:49-57. http://dx.doi.org/10.1085/jgp.201110606
25. Keymer, D.P., M.C. Miller, G.K. Schoolnik, and A.B. Boehm. 2007. Genomic and phenotypic diversity of coastal Vibrio cholerae strains is linked to environmental factors. Appl. Environ. Microbiol. 73:3705-3714. http://dx.doi.org/10.1128/AEM.02736-06
26. Koch, A.L., and S. Woeste. 1992. Elasticity of the sacculus of Escherichia coli. J. Bacteriol. 174:4811-4819.
27. 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. http://dx.doi.org/10.1093/emboj/18 .7.1730
28. 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. http://dx.doi.org/ 10.1093/emboj/cdf537
29. Luzardo, M.C., F. Amalfa, A.M. Nuñez, S. Díaz, A.C. Biondi De Lopez, and E.A. Disalvo. 2000. Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys. J. 78:2452- 2458. http://dx.doi.org/10.1016/S0006-3495(00)76789-0
30. Martinac, B., M. Buechner, A.H. Delcour, J. Adler, and C. Kung. 1987. Pressure-sensitive ion channel in Escherichia coli. Proc. Natl. Acad. Sci. USA. 84:2297-2301. http://dx.doi.org/10.1073/ pnas.84.8.2297
31. 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. http://dx.doi .org/10.1021/bi0509649
32. 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. http://dx.doi.org/10.1046/j.1365-2958.1998.00821.x
33. Naismith, J.H., and I.R. Booth. 2012. Bacterial mechanosensitive channels-MscS: evolution's solution to creating sensitivity in function. Annu Rev Biophys. 41:157-177. http://dx.doi.org/10 .1146/annurev-biophys-101211-113227
34. 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. http://dx.doi.org/10.1016/S0014-5793 (99)00054-X
35. Naughton, L.M., S.L. Blumerman, M. Carlberg, and E.F. Boyd. 2009. Osmoadaptation among Vibrio species and unique genomic features and physiological responses of Vibrio parahaemolyticus. Appl. Environ. Microbiol. 75:2802-2810. http://dx.doi.org/10.1128/ AEM.01698-08
36. Pagel, M., and A.H. Delcour. 2011. Effects of conjugated and unconjugated bile acids on the activity of the Vibrio cholerae porin OmpT. Mol. Membr. Biol. 28:69-78. http://dx.doi.org/10.3109/09 687688.2010.519727
37. Perozo, E. 2006. Gating prokaryotic mechanosensitive channels. Nat. Rev. Mol. Cell Biol. 7:109-119. http://dx.doi.org/10.1038/ nrm1833
38. Pflughoeft, K.J., K. Kierek, and P.I. Watnick. 2003. Role of ectoine in Vibrio cholerae osmoadaptation. Appl. Environ. Microbiol. 69:5919- 5927. http://dx.doi.org/10.1128/AEM.69.10.5919-5927.2003
39. Pruzzo, C., A. Huq, R.R. Colwell, and G. Donelli. 2005. Pathogenic Vibrio species in the marine and estuarine environment. In Oceans and Health: Pathogens in the Marine Environment. R.C. Belkin and R. Colwell, editors. Springer, New York. 217-252.
40. Romantsov, T., A.R. Battle, J.L. Hendel, B. Martinac, and J.M. Wood. 2010. Protein localization in Escherichia coli cells: comparison of the cytoplasmic membrane proteins ProP, LacY, ProW, AqpZ, MscS, and MscL. J. Bacteriol. 192:912-924. http://dx.doi.org/ 10.1128/JB.00967-09
41. Rudolph, A.S., J.H. Crowe, and L.M. Crowe. 1986. Effects of three stabilizing agents-proline, betaine, and trehalose-on membrane phospholipids. Arch. Biochem. Biophys. 245:134-143. http:// dx.doi.org/10.1016/0003-9861(86)90197-9
42. Ruthe, H.J., and J. Adler. 1985. Fusion of bacterial spheroplasts by electric fields. Biochim. Biophys. Acta. 819:105-113. http://dx.doi .org/10.1016/0005-2736(85)90200-7
43. Schleyer, M., R. Schmid, and E.P. Bakker. 1993. Transient, specific and extremely rapid release of osmolytes from growing cells of Escherichia coli K-12 exposed to hypoosmotic shock. Arch. Microbiol. 160:424-431. http://dx.doi.org/10.1007/BF00245302
44. Schumann, U., M.D. Edwards, T. Rasmussen, W. Bartlett, P. van West, and I.R. Booth. 2010. YbdG in Escherichia coli is a threshold-setting mechanosensitive channel with MscM activity. Proc. Natl. Acad. Sci. USA. 107:12664-12669. http://dx.doi.org/ 10.1073/pnas.1001405107
45. Steinbacher, S., R. Bass, P. Strop, and D.C. Rees. 2007. Structures of the prokaryotic mechanosensitive channels MscL and MscS. Curr. Top. Membr. 58:1-24. http://dx.doi.org/10.1016/S1063-5823 (06)58001-9
46. Stokes, N.R., H.D. Murray, C. Subramaniam, R.L. Gourse, P. Louis, W. Bartlett, S. Miller, and I.R. Booth. 2003. A role for mechanosensitive channels in survival of stationary phase: regulation of channel expression by RpoS. Proc. Natl. Acad. Sci. USA. 100:15959- 15964. http://dx.doi.org/10.1073/pnas.2536607100
47. 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. http://dx.doi.org/10.1016/S0006-3495(02)75169-2
48. 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. http://dx.doi.org/10.1016/S0006-3495(93)81044-0
49. 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. http://dx.doi.org/10.1085/jgp.113.4.525
50. Villarreal, M.A., S.B. Díaz, E.A. Disalvo, and G.G. Montich. 2004. Molecular dynamics simulation study of the interaction of trehalose with lipid membranes. Langmuir. 20:7844-7851. http:// dx.doi.org/10.1021/la049485l
51. Wood, J.M., E. Bremer, L.N. Csonka, R. Kraemer, B. Poolman, T. van der Heide, and L.T. Smith. 2001. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130:437-460. http://dx.doi .org/10.1016/S1095-6433(01)00442-1