The cytoplasmic cage domain of the mechanosensitive channel MscS is a sensor of macromolecular crowding

Journal of General Physiology

Volumn 143, Issue 5, 2014, Pages 543-557

  Rowe, Ian ^a   Anishkin, Andriy ^c   Kamaraju, Kishore ^a   Yoshimura, Kenjiro ^a,d   Sukharev, Sergei ^a,b  

^a Bldg 142   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d SHIBAURA INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

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

AMINO ACID SEQUENCE; CHANNEL GATING; CHEMISTRY; CYTOPLASM; DRUG EFFECTS; ESCHERICHIA COLI; GENETICS; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; CYTOPLASM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FICOLL; ION CHANNEL GATING; ION CHANNELS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84899548584     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201311114     Document Type: Article

References (57)

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., B. Akitake, and S. Sukharev. 2008a. Characterization of the resting MscS: modeling and analysis of the closed bacterial mechanosensitive channel of small conductance. Biophys. J. 94:1252-1266. http://dx.doi.org/10.1529/biophysj.107.110171
4. Anishkin, A., K. Kamaraju, and S. Sukharev. 2008b. 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. Anishkin, A., A.L. Milac, and H.R. Guy. 2010. Symmetry-restrained molecular dynamics simulations improve homology models of potassium channels. Proteins. 78:932-949. http://dx.doi.org/10.1002/prot.22618
6. Balleza, D., and F. Gómez-Lagunas. 2009. Conserved motifs in mechanosensitive channels MscL and MscS. Eur. Biophys. J. 38:1013-1027. http://dx.doi.org/10.1007/s00249-009-0460-y
7. 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. http://dx.doi.org/10.1126/science.1077945
8. Belyy, V., A. Anishkin, K. Kamaraju, N. Liu, and S. Sukharev. 2010a. The tension-transmitting 'clutch' in the mechanosensitive channel MscS. Nat. Struct. Mol. Biol. 17:451-458. http://dx.doi.org/10.1038/nsmb.1775
9. Belyy, V., K. Kamaraju, B. Akitake, A. Anishkin, and S. Sukharev. 2010b. Adaptive behavior of bacterial mechanosensitive channels is coupled to membrane mechanics. J. Gen. Physiol. 135:641-652. http://dx.doi.org/10.1085/jgp.200910371
10. 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
11. Cayley, S., and M.T. Record Jr. 2003. Roles of cytoplasmic osmolytes, water, and crowding in the response of Escherichia coli to osmotic stress: biophysical basis of osmoprotection by glycine betaine. Biochemistry. 42:12596-12609. http://dx.doi.org/10.1021/bi0347297
12. Cayley, S., B.A. Lewis, H.J. Guttman, and M.T. Record Jr. 1991. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity: Implications for protein-DNA interactions in vivo. J. Mol. Biol. 222:281-300. http://dx.doi.org/10.1016/0022-2836(91)90212-O
13. Cayley, D.S., H.J. Guttman, and M.T. Record Jr. 2000. Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys. J. 78:1748-1764. http://dx.doi.org/10.1016/S0006-3495(00)76726-9
14. Cox, C.D., T. Nomura, C.S. Ziegler, A.K. Campbell, K.T. Wann, and B. Martinac. 2013. Selectivity mechanism of the mechanosensitive channel MscS revealed by probing channel subconducting states. Nat. Commun. 4:2137. http://dx.doi.org/10.1038/ncomms3137
15. 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
16. Edwards, M.D., S. Black, T. Rasmussen, A. Rasmussen, N.R. Stokes, T.L. Stephen, S. Miller, and I.R. Booth. 2012. Characterization of three novel mechanosensitive channel activities in Escherichia coli. Channels (Austin). 6:272-281. http://dx.doi.org/10.4161/chan.20998
17. Ellis, R.J. 2001. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol. 11:114-119. http://dx.doi.org/10.1016/S0959-440X(00)00172-X
18. 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
19. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38. http://dx.doi.org/10.1016/0263-7855(96)00018-5
20. 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
21. Koch, A.L., and S. Woeste. 1992. Elasticity of the sacculus of Escherichia coli. J. Bacteriol. 174:4811-4819.
22. Koprowski, P., W. Grajkowski, and A. Kubalski. 2007. The MscS cytoplasmic domain and its conformational changes on the channel gating. In Mechanosensitive Ion Channels, Part 1. Current Topics in Membranes, Vol. 58. O.P. Hamill, editor. Academic Press, San Diego. 295-309.
23. Koprowski, P., W. Grajkowski, E.Y. Isacoff, and A. Kubalski. 2011. Genetic screen for potassium leaky small mechanosensitive channels (MscS) in Escherichia coli: recognition of cytoplasmic β domain as a new gating element. J. Biol. Chem. 286:877-888. http://dx.doi.org/10.1074/jbc.M110.176131
24. Lai, J.Y., Y.S. Poon, J.T. Kaiser, and D.C. Rees. 2013. Open and shut: crystal structures of the dodecylmaltoside solubilized mechanosensitive channel of small conductance from Escherichia coli and Helicobacter pylori at 4.4 Å and 4.1 Å resolutions. Protein Sci. 22:502-509. http://dx.doi.org/10.1002/pro.2222
25. 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
26. 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
27. Liedtke, W. 2005. TRPV4 as osmosensor: a transgenic approach. Pflugers Arch. 451:176-180. http://dx.doi.org/10.1007/s00424-005-1449-8
28. Machiyama, H., H. Tatsumi, and M. Sokabe. 2009. Structural changes in the cytoplasmic domain of the mechanosensitive channel MscS during opening. Biophys. J. 97:1048-1057. http://dx.doi.org/10.1016/j.bpj.2009.05.021
29. 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
30. Minton, A.P. 1998. Molecular crowding: analysis of effects of high concentrations of inert cosolutes on biochemical equilibria and rates in terms of volume exclusion. Methods Enzymol. 295:127-149. http://dx.doi.org/10.1016/S0076-6879(98)95038-8
31. 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
32. Nakayama, Y., K. Yoshimura, and H. Iida. 2013. Electrophysiological characterization of the mechanosensitive channel MscCG in Corynebacterium glutamicum. Biophys. J. 105:1366-1375. http://dx.doi.org/10.1016/j.bpj.2013.06.054
33. Nomura, T., M. Sokabe, and K. Yoshimura. 2008. Interaction between the cytoplasmic and transmembrane domains of the mechanosensitive channel MscS. Biophys. J. 94:1638-1645. http://dx.doi.org/10.1529/biophysj.107.114785
34. Petrov, E., D. Palanivelu, M. Constantine, P.R. Rohde, C.D. Cox, T. Nomura, D.L. Minor Jr., and B. Martinac. 2013. Patch-clamp characterization of the MscS-like mechanosensitive channel from Silicibacter pomeroyi. Biophys. J. 104:1426-1434. http://dx.doi.org/10.1016/j.bpj.2013.01.055
35. Pivetti, C.D., M.R. Yen, S. Miller, W. Busch, Y.H. Tseng, I.R. Booth, and M.H. Saier Jr. 2003. Two families of mechanosensitive channel proteins. Microbiol. Mol. Biol. Rev. 67:66-85. http://dx.doi.org/10.1128/MMBR.67.1.66-85.2003
36. Record, M.T. Jr., E.S. Courtenay, S. Cayley, and H.J. Guttman. 1998. Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments. Trends Biochem. Sci. 23:190-194. http://dx.doi.org/10.1016/S0968-0004(98)01207-9
37. Reiser, V., D.C. Raitt, and H. Saito. 2003. Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J. Cell Biol. 161:1035-1040. http://dx.doi.org/10.1083/jcb.200301099
38. Schumann, U., M.D. Edwards, T. Rasmussen, W. Bartlett, P. van West, and I.R. Booth. 2010. YbdG in Escherichia coli is a thresholdsetting mechanosensitive channel with MscM activity. Proc. Natl. Acad. Sci. USA. 107:12664-12669. http://dx.doi.org/10.1073/pnas.1001405107
39. Sotomayor, M., and K. Schulten. 2004. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys. J. 87:3050-3065. http://dx.doi.org/10.1529/biophysj.104.046045
40. Steinbacher, S., R. Bass, P. Strop, and D.C. Rees. 2007. Structures of the prokaryotic mechanosensitive channels MscL and MscS. In Mechanosensitive Ion Channels, Part 1. Current Topics in Membranes, Vol. 58. O.P. Hamill, editor. Academic Press, San Diego. 1-24.
41. Sukharev, S.I., P. Blount, B. Martinac, F.R. Blattner, and C. Kung. 1994. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature. 368:265-268. http://dx.doi.org/10.1038/368265a0
42. 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
43. Sukharev, S., B. Akitake, and A. Anishkin. 2007. The bacterial mechanosensitive channel MscS: Emerging principles of gating and modulation. In Mechanosensitive Ion Channels, Part 1. Current Topics in Membranes, Vol. 58. O.P. Hamill, editor. Academic Press, San Diego. 235-267.
44. van den Berg, B., R.J. Ellis, and C.M. Dobson. 1999. Effects of macromolecular crowding on protein folding and aggregation. EMBO J. 18:6927-6933. http://dx.doi.org/10.1093/emboj/18.24.6927
45. Vasquez, V., and E. Perozo. 2004. Voltage dependent gating in MscS. Biophys. J. 86:545A.
46. Vásquez, V., M. Sotomayor, D.M. Cortes, B. Roux, K. Schulten, and E. Perozo. 2008. Three-dimensional architecture of membraneembedded MscS in the closed conformation. J. Mol. Biol. 378: 55-70. http://dx.doi.org/10.1016/j.jmb.2007.10.086
47. Vollmer, W., and J.V. Höltje. 2001. Morphogenesis of Escherichia coli. Curr. Opin. Microbiol. 4:625-633. http://dx.doi.org/10.1016/S1369-5274(01)00261-2
48. Wang, L.C., L.K. Morgan, P. Godakumbura, L.J. Kenney, and G.S. Anand. 2012. The inner membrane histidine kinase EnvZ senses osmolality via helix-coil transitions in the cytoplasm. EMBO J. 31:2648-2659. http://dx.doi.org/10.1038/emboj.2012.99
49. Wang, W., S.S. Black, M.D. Edwards, S. Miller, E.L. Morrison, W. Bartlett, C. Dong, J.H. Naismith, and I.R. Booth. 2008. The structure of an open form of an E. coli mechanosensitive channel at 3.45 Å resolution. Science. 321:1179-1183. http://dx.doi.org/10.1126/science.1159262
50. Wood, J.M. 1999. Osmosensing by bacteria: signals and membranebased sensors. Microbiol. Mol. Biol. Rev. 63:230-262.
51. Wood, J.M. 2007. Bacterial osmosensing transporters. Methods Enzymol. 428:77-107. http://dx.doi.org/10.1016/S0076-6879(07)28005-X
52. 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
53. Yao, X., M. Jericho, D. Pink, and T. Beveridge. 1999. Thickness and elasticity of gram-negative murein sacculi measured by atomic force microscopy. J. Bacteriol. 181:6865-6875.
54. Yoshimura, K., A. Batiza, and C. Kung. 2001. Chemically charging the pore constriction opens the mechanosensitive channel MscL. Biophys. J. 80:2198-2206. http://dx.doi.org/10.1016/S0006-3495(01)76192-9
55. Zhang, X., J. Wang, Y. Feng, J. Ge, W. Li, W. Sun, I. Iscla, J. Yu, P. Blount, Y. Li, and M. Yang. 2012. Structure and molecular mechanism of an anion-selective mechanosensitive channel of small conductance. Proc. Natl. Acad. Sci. USA. 109:18180-18185. http://dx.doi.org/10.1073/pnas.1207977109
56. Zhou, H.X., G. Rivas, and A.P. Minton. 2008. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu. Rev. Biophys. 37:375-397. http://dx.doi.org/10.1146/annurev.biophys.37.032807.125817
57. Zimmerman, S.B., and S.O. Trach. 1991. Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J. Mol. Biol. 222:599-620. http://dx.doi.org/10.1016/0022-2836(91)90499-V