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Computational Studies of the Bacterial Mechanosensitive Channels

  • Ben Corry
  • Boris Martinac
Part of the Mechanosensitivity in Cells and Tissues book series (MECT, volume 1)

abstract

Bacterial mechanosensitive (MS) channels were first documented in giant spheroplasts of Escherichia coli during a survey of the bacterial cell membrane by the patch clamp some twenty years ago. Two major events that greatly advanced and kept the research on bacterial MS channels at the forefront of the MS channel research field include: (i) cloning of MscL and MscS, the MS channels of Large and Small conductance, and (ii) solving their 3D crystal structure. In addition to advancing further experimental studies of the bacterial MS channels by enabling the use of new techniques, such as EPR and FRET spectroscopy, these events also enabled theoretical approaches to be employed. In this chapter we will review recent computational approaches used to elucidate the molecular dynamics of MscL and MscS, which has significantly contributed to our understanding of basic physical principles of the mechanosensory transduction in living organisms.

Keywords

MS channels Patch clamp Bilayer model Mechanosensory transduction EPR spectroscopy FRET Molecular dynamics Brownian dynamics 

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References

  1. Ajouz, B., Berrier, C., Besnard, M., Martinac, B. and Ghazi, A. (2000) Contributions of the different extramembraneous domains of the mechanosensitive ion channel MscL to its response to membrane tension. J. Biol. Chem. 275: 1015–1022.PubMedCrossRefGoogle Scholar
  2. Aksimentiev, A., Schulten, K. (2005) Imaging alpha-hemolysin with molecular dynamics: Ionic conductance, osmotic permeability and the electrostatic potential map. Biophys. J. 88: 3745–3761.PubMedCrossRefGoogle Scholar
  3. Anishkin, A., V. Gendel, N. A. Sharifi, C. S. Chiang, L. Shirinian, H. R. Guy and S. I. Sukharev (2003) On the conformation of the COOH-terminal domain of the large mechanosensitive channel MscL. J. Gen. Physiol. 121: 227–244.PubMedCrossRefGoogle Scholar
  4. Anishkin, A., Sukharev, S. (2004) Water dynamics and dewetting transitions in the small mechanosensitive channel MscS, Biophys. J. 86: 2883–2895.Google Scholar
  5. Bass, R.B., Strop, P., Barclay, M., Rees, D. (2002) Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science 298: 1582–1587.PubMedCrossRefGoogle Scholar
  6. Beckstein, O., Biggin, P.C., Sansom, M.S.P. (2001) A hydrophobic gating mechanism for nanopores, J. Phys. Chem. B. 105: 12902–12905.CrossRefGoogle Scholar
  7. Beckstein, O., Sansom, M.S.P. (2003) Liquid-vapor oscillations of water in hydrophobic nanopores, Proc. Natl. Acad. Sci. USA 100: 7063–7068.CrossRefGoogle Scholar
  8. Beckstein, O., Sansom, M.S.P. (2004) The influence of geometry, surface character, and flexibility on the permeation of ions and water through biological pores, Phys. Biol. 1: 42–52.Google Scholar
  9. Beckstein, O., Sansom, M.S.P. (2006) A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor, Phys. Biol. 3: 147–159.Google Scholar
  10. Berrier, C., Besnard, M., Ajouz, B., Coulombe, A., Ghazi, A. (1996) Multiple mechano-sensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J. Memb. Biol. 151: 175–187.CrossRefGoogle Scholar
  11. Betanzos, M., Chiang, C.-S., Guy, H.R., Sukharev, S. (2002) A large iris-like expansion of a mechanosensitive channel protein induced by membrane tension. Nature Struct. Biol. 9: 704–710.PubMedCrossRefGoogle Scholar
  12. Bilston, L.E., Mylvaganam, K. (2002) Molecular simulations of the large mechanosensitive channel (MscL) under mechanical loading, FEBS Lett., 512: 185–190.PubMedCrossRefGoogle Scholar
  13. Blount, P., Li, Y., Moe, P. C., and Iscla, I. (2007) Mechanosensitive channels gated by membrane tension: Bacteria and beyond. In: Mechanosensitive ion channels (a volume in the Mechanosensitivity in Cells and Tissues, Moscow Academia series), A. Kamkin, and I. Kiseleva, eds. (New York, Springer Press). (in press)Google Scholar
  14. Chang, G., Spencer, R., Lee, A., Barclay, M., Rees, D. (1998) Structure of the MscL homologue from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282: 2220–2226.PubMedCrossRefGoogle Scholar
  15. Colombo, G., Marrink, S.J., Mark, A.E. (2003) Simulation of MscL gating in a bilayer under stress, Biophys. J. 84: 2331–2337.PubMedGoogle Scholar
  16. Corry, B., Rigby, P., Liu, Z.-W., Martinac, B. (2005) Conformational changes involved in MscL channel gating measured using FRET spectroscopy. Biophys. J. 89: L49-L51.PubMedCrossRefGoogle Scholar
  17. Corry, B. (2006) An energy-efficient gating mechanism in the acetylcholine receptor suggested by molecular and Brownian dynamics, Biophys. J. 90: 799–810.PubMedCrossRefGoogle Scholar
  18. Cruickshank, C.C., Minchin, R., Le Dain, A., Martinac, B. (1997) Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. Biophys J 73: 1925–1931.PubMedGoogle Scholar
  19. Dzubiella, J., Allen, R.J., Hansen, J.-P. (2004). Electric field-controlled water permeation coupled to ion transport through a nanopore. J. Chem. Phys. 120: 5001–5004.PubMedCrossRefGoogle Scholar
  20. Edwards, M.D., Booth, I.R., Miller, S. (2004) Gating the bacterial mechanosensitive channel: MscS a new paradigm? Curr., Opin. Microbiol. 7: 163–167.Google Scholar
  21. Elmore, D.E., Dougherty, D.A. (2001) Molecular dynamics simulations of wild-type and mutant forms of the Mycobacterium tuberculosis MscL channel, Biophys. J. 81: 1345–1359.PubMedGoogle Scholar
  22. Elmore, D.E., Dougherty, D.A. (2003) Investigating lipid composition effects on the mechanosensitive channel of large conductance (MscL) using molecular dynamics simulations, Biophys. J. 85: 1512–11524.PubMedGoogle Scholar
  23. Gullingsrud, J., Kosztin, D., Schulten, K. (2001) Structural determinants of MscL gating studied by molecular dynamics simulations. Biophys. J. 80: 2074–2081.PubMedGoogle Scholar
  24. Gullingsrud, J., Schulten, K. (2003) Gating of MscL studied by steered molecular dynamics, Biophys. J. 85: 2087–2099.PubMedCrossRefGoogle Scholar
  25. Gullingsrud, J., Schulten, K. (2004) Lipid bilayer pressure profiles and mechanosensitive channel gating, Biophys. J. 86: 3496–3509.PubMedCrossRefGoogle Scholar
  26. Hamill, O.P., Marty, A., Neher, E., Sackmann, B., Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. Eur. J. Physiol. 391: 85–100.CrossRefGoogle Scholar
  27. Hummer, G., Rasaiah, J.C., Noworyta, J.P. (2001) Water conduction through the hydrophobic channel of a carbon nanotube, Nature 414: 188–190.PubMedCrossRefGoogle Scholar
  28. Kong, Y.F., Shen, Y.F., Warth, T.E., Ma, J.P. (2002) Conformational pathways in the gating of Escherichia coli mechanosensitive channel, Proc. Natl. Acad. Sci. USA 99: 5999–6004.CrossRefGoogle Scholar
  29. Koprowski, P., Kubalski, A. (2003) C-termini of the Escherichia coli mechanosensitive ion channel (MscS) move apart upon the channel opening, J. Biol. Chem. 278: 11237–11245.PubMedCrossRefGoogle Scholar
  30. Levina, N., Totemeyer, S., Stokes, N.R., Louis, P., Jones, M.A., Booth, I.R. (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.PubMedCrossRefGoogle Scholar
  31. Martinac, B.: Mechanosensitive channels in prokaryotes. Cellular Physiol. Biochem. 11(2): 61–76, 2001.CrossRefGoogle Scholar
  32. Martinac, B. (2005) Structural plasticity in MS channels. Nat. Struct. Mol. Biol. 12: 104–105.PubMedCrossRefGoogle Scholar
  33. Martinac, B. (2006) Mechanosensitive channels. In: Biological Membrane Ion Channels: Dynamics, Structure, and Applications (eds. S. H. Chung, O. S. Andersen and V. Krishnamurthy. Springer, New York. Chapter 10, pp. 369–398.Google Scholar
  34. Martinac, B., Buechner, M., Delcour, A.H., Adler, J., Kung, C. (1987) Pressure-sensitive ion channel in Escherichia coli. Proc. Natl. Acad. Sci. USA, 84: 2297–2301.PubMedCrossRefGoogle Scholar
  35. Martinac, B., Kloda, A. (2003) Evolutionary origins of mechanosensitive ion channels. Progress Biophys. Mol. Biol. 82: 11–24.CrossRefGoogle Scholar
  36. Meyer, G.R., Gullingsrud, J., Schulten, K., Martinac, B. (2006) Molecular dynamics study of MscL interactions with a curved lipid bilayer, Biophys. J. 91: 1630–1637.PubMedCrossRefGoogle Scholar
  37. Miller, S., Bartlett, W., Chandrasekaran, S., Simpson, S., Edwards, M., Booth, I.R. (2003) Domain organisation of the MscS mechanosensitive channel of Escherichia coli, EMBO J. 22: 36–46.PubMedCrossRefGoogle Scholar
  38. Oakley, A.J., Martinac, B., Wilce, M.C.J. (1999) Structure and function of the bacterial mechanosensitive channel of large conductance. Protein Sci. 8: 1915–1921.PubMedGoogle Scholar
  39. Park, K.H., Berrier, C., Martinac, B., Ghazi, A. (2004) Purification and Functional Reconstitution of N-and C-Halves of the MscL Channel Biophys. J. 86: 2129–2136.PubMedCrossRefGoogle Scholar
  40. Perozo, E., Kloda, A. Cortes, D.M. and Martinac, B. (2001) Site-directed spin-labeling analysis of reconstituted MscL in the closed state. J. Gen. Physiol. 118: 193–206.PubMedCrossRefGoogle Scholar
  41. Perozo, E., Kloda, A., Cortes, D.M., Martinac, B. (2002a) Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nature Struct. Biol. 9: 696–703.CrossRefGoogle Scholar
  42. Perozo, E., Cortes, D.M., Sompornpisut, P., Kloda, A., Martinac, B. (2002b) Structure of MscL in the open state and the molecular mechanism of gating in mechanosensitive channels. Nature 418: 942–948.CrossRefGoogle Scholar
  43. Pivetti, C. D., Yen, M. R., Miller, S., Busch, W., Tseng, Y., Booth, I.R., & Saier M.H.J. (2003) Two families of mechanosensitive channel proteins. Microbiol. Mol. Biol. Rev., 67, 66–85.PubMedCrossRefGoogle Scholar
  44. Ruthe, H.J., Adler, J. (1985) Fusion of bacterial spheroplasts by electric fields. Biochim Biophys Acta. 819: 105–113.PubMedCrossRefGoogle Scholar
  45. Saint, N., Lacapere, J.J., Gu, L-Q., Ghazi, A., Martinac, B. and Rigaud, J.L. (1998) A hexameric transmembrane pore revealed by two-dimensional crystallization of the large mechanosensitive ion channel (MscL) of Escherichia coli. J. Biol. Chem., 273: 14667–14670.PubMedCrossRefGoogle Scholar
  46. Schumann, U., Edwards, M.D., Li, C., Booth, I.R. (2004) The conserved carboxy-terminus of the MscS mechanosensitive channel is not essential but increases stability and activity, FEBS Lett. 572: 233–237.PubMedCrossRefGoogle Scholar
  47. Sotomayor, M., Schulten, K., (2004) Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS, Biophys. J. 87: 3050–3065.PubMedCrossRefGoogle Scholar
  48. Sotomayor, M., van der Straaten, T.A., Ravaioli, U., Schulten, K. (2006) Electrostatic properties of the mechanosensitive channel of small conductance MscS, Biophys. J. 90: 3496–3510.PubMedCrossRefGoogle Scholar
  49. Sotomayor, M. Vásquez, V., Perozo, E., Schulten, K. (2007) Ion conduction though MscS as determined by electrophysiology and simulation. Biophys. J. 92: 886–902.PubMedCrossRefGoogle Scholar
  50. Spronk, S.A., Elmore, D.E., Dougherty, D.A. (2006) Voltage-dependent hydration and conduction properties of the hydrophobic pore of the mechanosensitive channel of small conductance, Biophys. J. 90: 3555–3569.PubMedCrossRefGoogle Scholar
  51. Sukharev, S.I., Blount, P., Martinac, B., Blattner, F.R., Kung, C. (1994) A large mechanosensitive channel in E. coli encoded by mscL alone. Nature 368: 265–268.PubMedCrossRefGoogle Scholar
  52. Sukharev, S.I., Martinac, B., Arshavsky, V.Y., and Kung, C. (1993) Two types of mechanosensitive channels in the E. coli cell envelope: solubilization and functional reconstitution. Biophys. J. 65: 177–183.PubMedGoogle Scholar
  53. Tang, Y.Y., Cao, G.X., Chen, X., Yoo, J., Yethiraj, A., Cui, A. (2006) A finite element framework for studying the mechanical response of macromolecules: Application to the gating of the mechanosensitive channel MscL, Biophys. J. 91: 1248–1263.PubMedCrossRefGoogle Scholar
  54. Tsai, I-J., Zhen-Wei Liu, Z-W., Rayment, J, Norman, C., McKinley, A. and Martinac, B. (2005) The role of the periplasmic loop residue glutamine 65 for MscL mechanosensitivity. Eur. Biophys. J. 34: 403–413.PubMedCrossRefGoogle Scholar
  55. Vora, T., Corry, B., Chung, S.H. (2006) Brownian dynamics investigations into the conductance state of the MscS channel crystal structure, Biochim. Biophys. Acta 1758: 730–737.PubMedCrossRefGoogle Scholar
  56. Valadie, H., Lacapcre, J.J., Sanejouand, Y.H., Etchebest, C. (2003) Dynamical properties of the MscL of Escherichia coli: A normal mode analysis, J. Mol. Biol. 332: 657–674.PubMedCrossRefGoogle Scholar
  57. Wan, R., Li, J., Lu, H., Fang, H. (2005) Controllable water channel gating of nanometer dimensions, J. Am. Chem. Soc. 127: 7166–7170.PubMedCrossRefGoogle Scholar
  58. Wiggins, P., Phillips, R. (2004) Analytic models for mechanotransduction: Gating a mechanosensitive channel, Proc. Natl. Acad. Sci. USA, 101: 4071–4076.CrossRefGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Ben Corry
  • Boris Martinac

There are no affiliations available

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