Advertisement

The European Physical Journal Special Topics

, Volume 223, Issue 5, pp 915–926 | Cite as

The role of continuous and discrete water structures in protein function

  • Benjamin H. McMahon
  • Hans Frauenfelder
  • Paul W. Fenimore
Review
Part of the following topical collections:
  1. Discussion and Debate: Water Complexity — More than a Myth?

Abstract

Proteins have evolved to perform numerous roles as specific catalysts and nano-machines. Some of the mechanisms exploited by evolution are clear. Hydrophobicity drives the stabilization energy of folding, charges mediate long-range interactions and facilitate catalysis, and specific geometries and hydrogen bonding patterns facilitate molecular recognition and catalysis. In this work, we examine the energy landscape of protein dynamics in terms of the continuous and discrete water structures that control protein dynamics. We observe that the internal structures at the active site of proteins are constantly shaped by strong interactions with hydration shell and bulk water motions. By describing the energy landscape of proteins in terms of its three component motions; conformational, hydration and protonation, and electronic structure, it is possible to systematically understand protein function.

Keywords

European Physical Journal Special Topic Hydration Shell Energy Landscape Activation Enthalpy Heme Group 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    P.W. Fenimore, H. Frauenfelder, B.H. McMahon, F.G. Parak, PNAS USA 99, 16047 (2002)ADSCrossRefGoogle Scholar
  2. 2.
    V. Lubchenko, P.G. Wolynes, H. Frauenfelder, J. Phys. Chem. B 109, 7488 (2005)CrossRefGoogle Scholar
  3. 3.
    P.W. Fenimore, H. Frauenfelder, B.H. McMahon, R.D. Young, PNAS USA 101, 14408 (2004)ADSCrossRefGoogle Scholar
  4. 4.
    B.H. McMahon, B.P. Stojkovic, P.J. Hay, R.L. Martin, A.E. Garcia, J. Chem. Phys. 113, 6831 (2000)ADSCrossRefGoogle Scholar
  5. 5.
    T. Kleinert, W. Doster, H. Leyser, W. Petry, V. Schwarz, M. Settles, Biochemistry 37, 717 (1998)CrossRefGoogle Scholar
  6. 6.
    H.B. Callen, T.A. Welton, Phys. Rev. 83, 34 (1951)ADSCrossRefzbMATHMathSciNetGoogle Scholar
  7. 7.
    H. Frauenfelder, P.W. Fenimore, G. Chen, B.H. McMahon, PNAS USA 103, 15469 (2006)ADSCrossRefGoogle Scholar
  8. 8.
    N. Agmon, J.J. Hopfield, J. Chem. Phys. 78, 6947 (1983)ADSCrossRefGoogle Scholar
  9. 9.
    N. Agmon, J.J. Hopfield, J. Chem. Phys. 79, 2042 (1983)ADSCrossRefGoogle Scholar
  10. 10.
    J.N. Onuchic, P.G. Wolynes, Z. Luthey-Schulten, N.D. Socci, PNAS USA 92, 3626 (1995)ADSCrossRefGoogle Scholar
  11. 11.
    C.L. Brooks, J.N. Onuchic, D.J. Wales, Science 293, 5530 (2001)CrossRefGoogle Scholar
  12. 12.
    R.B. Best, G. Hummer, W.A. Eaton, Proc Nat. Acad. Sci. USA 110, 17874 (2013)CrossRefGoogle Scholar
  13. 13.
    M.S. Cheung, A.E. Garcia, J.N. Onuchic, PNAS USA 99, 685 (2002)ADSCrossRefGoogle Scholar
  14. 14.
    S. Tripathi, J.J. Portman, PNAS USA 106, 2104 (2009)ADSCrossRefGoogle Scholar
  15. 15.
    S. Tripathi, J.J. Portman, J. Chem. Phys. 135, 075104 (2011)CrossRefGoogle Scholar
  16. 16.
    W. Zheng, N.P. Schafer, P.G. Wolynes, PNAS USA 110, 20515 (2013)ADSCrossRefGoogle Scholar
  17. 17.
    P.C. Whitford, K.Y. Sanbonmatsu, J.N. Onuchic, Rep. Prog. Phys. 75, 076601 (2011)ADSCrossRefGoogle Scholar
  18. 18.
    C. Tanford, J.G. Kirkwood, J. Am. Chem. Soc. 79, 5333 (1957)CrossRefGoogle Scholar
  19. 19.
    A. Warshel, P.K. Sharma, M. Kato, W.W. Parson, BBA 1764, 1647 (2006)Google Scholar
  20. 20.
    B. Honig, A. Nicholls, Science 268, 1144 (1995)ADSCrossRefGoogle Scholar
  21. 21.
    P. Jungwirth, B. Winter, Ann. Rev. Phys. Chem. 59, 343 (2008)ADSCrossRefGoogle Scholar
  22. 22.
    A.G. Cherstvy, Phys. Chem. Chem. Phys. 13, 9942 (2011)CrossRefGoogle Scholar
  23. 23.
    F. Despa, A. Fernandez, R.S. Berry, Phys. Rev. Lett. 93, 228104 (2004)ADSCrossRefGoogle Scholar
  24. 24.
    A. Fernandez, Phys. Rev. Lett. 108, 188102 (2012)ADSCrossRefGoogle Scholar
  25. 25.
    A. Kannt, R.D. Lancaster, H. Michel, Biophys. J. 74, 708 (1998)ADSCrossRefGoogle Scholar
  26. 26.
    V.R.I. Kaila, M.I. Verkhovsky, M. Wikstrom, Chem. Rev. 110, 7062 (2010)CrossRefGoogle Scholar
  27. 27.
    M.R. Gunner, B. Honig, PNAS USA 88, 9151 (1991)ADSCrossRefGoogle Scholar
  28. 28.
    M.H.V. Huynh, T.J. Meyer, Chem. Rev. 107, 5004 (2007)CrossRefGoogle Scholar
  29. 29.
    P. Dimroth, H. Wang, M. Grabe, G. Oster, PNAS USA 96, 4924 (1999)ADSCrossRefGoogle Scholar
  30. 30.
    B.E. Cohen, T.B. McAnaney, E.S. Park, Y.N. Jan, S.G. Boxer, L.Y. Jan, Science 296, 1700 (2002)ADSCrossRefGoogle Scholar
  31. 31.
    T.A. Jackson, M. Lim, P.A. Anfinrud, Chem. Phys. 180, 131 (1994)ADSCrossRefGoogle Scholar
  32. 32.
    K. Nienhaus, D.C. Lamb, P. Deng, G.U. Nienhaus, BioPhys. J. 82, 1059 (2002)CrossRefGoogle Scholar
  33. 33.
    B.H. McMahon, J.D. Muller, C.A. Wraight, G.U. Nienhaus, Biophys. J. 74, 2567 (1998)ADSCrossRefGoogle Scholar
  34. 34.
    M. Malferrari, F. Francia, G. Venturoli, Biochim. Biophys. Acta 1827, 328 (2013)CrossRefGoogle Scholar
  35. 35.
    J.R. Huck, G.A. Noyel, L.J. Jorat, IEEE Trans. Elect. Insul. 23, 627 (1988)CrossRefGoogle Scholar
  36. 36.
    F. Kremer, A. Schönhals, Broadband Dielectric Spectroscopy (Springer-Verlag, Berlin, 2003)Google Scholar
  37. 37.
    Y. Feldman, I. Ermolina, Y. Hayashi, IEEE Trans. Dielec. Elec. Insul. 10, 728 (2003)CrossRefGoogle Scholar
  38. 38.
    H. Frauenfelder, G. Chen, J. Berendzen, P.W. Fenimore, H. Jansson, B.H. McMahon, I.R. Stroe, J. Swenson, R.D. Young, PNAS USA 106, 5129 (2009)ADSCrossRefGoogle Scholar
  39. 39.
    A. Kent, A.K. Jha, J.E. Fitzgerald, K.F. Freed, J. Phys. Chem. 112, 6175 (2008)CrossRefGoogle Scholar
  40. 40.
    A.A. Konstantinov, S. Siletsky, D. Mitchell, A. Kaulen, R.B. Gennis, PNAS USA 94, 9085 (1997)ADSCrossRefGoogle Scholar
  41. 41.
    M. Vidakovic, S.G. Sligar, H. Li, T.L. Poulos, Biochemistry 37, 9211 (1998)CrossRefGoogle Scholar
  42. 42.
    P.M. Petrone, A.E. Garcia, J. Mol. Biol. 336, 419 (2004)CrossRefGoogle Scholar
  43. 43.
    Z. Li, T. Lazaridis, Phys. Chem. Chem. Phys. 9, 573 (2007)CrossRefGoogle Scholar
  44. 44.
    M.S. Cheung, A.E. Garcia, J.N. Onuchic, PNAS USA 99, 685 (2002)ADSCrossRefGoogle Scholar
  45. 45.
    A.J. Patel, P. Varilly, S.N. Jamadagni, M.F. Hagen, D. Chandler, S. Garde, J. Phys. Chem. B 116, 2498 (2012)CrossRefGoogle Scholar
  46. 46.
    K. Lum, D. Chandler, J.D. Weeks, J. Phys. Chem. B 103, 4570 (1999)CrossRefGoogle Scholar
  47. 47.
    Y. Miyazaki, T. Matsuo, H. Suga, Chem. Phys. Lett. 213, 303 (1993)ADSCrossRefGoogle Scholar
  48. 48.
    J. Gomez, V.J. Hilser, D. Xie, E. Freire, Proteins: Struct. Funct. Gen. 22, 404 (1995)CrossRefGoogle Scholar
  49. 49.
    J.D. Muller, B.H. McMahon, E.Y.T. Chien, S.G. Sligar, G.U. Nienhaus, Biophys. J. 77, 1036 (1999)CrossRefGoogle Scholar
  50. 50.
    H. Ishikawa, K. Kwak, J.K. Chung, S. Kim, M.D. Fayer, PNAS USA 105, 8619 (2008)ADSCrossRefGoogle Scholar
  51. 51.
    J. Vojtechovsky, K. Chu, J. Berendzen, R.M. Sweet, I. Schlichting, Biophys. J. 77, 2153 (1999)CrossRefGoogle Scholar
  52. 52.
    R.H. Austin, K.W. Beeson, L. Eisenstein, H. Frauenfelder, I.C. Gunsalus, Biochem. 14, 5355 (1974)CrossRefGoogle Scholar
  53. 53.
    K. Chu, J. Vojtechovsky, B.H. McMahon, R.M. Sweet, J. Berendzen, I. Schlichting, Nature 403, 921 (2000)ADSCrossRefGoogle Scholar
  54. 54.
    F. Schotte, M. Lim, T.A. Jackson, A.V. Smirnov, J. Soman, J.S. Olson, G.N. Phillips Jr., M. Wulff, P.A. Anfinrud, Science 300, 1944 (2003)ADSCrossRefGoogle Scholar
  55. 55.
    F. Schotte, H.S. Cho, J. Soman, M. Wulff, J.S. Olson, P.A. Anfinrud, Chem. Phys. 422, 98 (2013)ADSCrossRefGoogle Scholar
  56. 56.
    W.S. Caughey, H. Shimada, M.G. Choc, M.P. Tucker, PNAS USA 78, 2903 (1981)ADSCrossRefGoogle Scholar
  57. 57.
    D.V. Yang, J. Appl. Phys. 45, 3023 (1974)ADSCrossRefGoogle Scholar
  58. 58.
    J. Berendzen, D. Braunstein, PNAS USA 87, 1 (1990)ADSCrossRefGoogle Scholar
  59. 59.
    H. Frauenfelder, S.G. Sligar, P.G. Wolynes, Science 254, 1598 (1991)ADSCrossRefGoogle Scholar
  60. 60.
    Y. Abadan, E.Y.T. Chien, K. Chu, C.D. Eng, G.U. Nienhaus, S.G. Sligar, Biophys. J. 68, 2497 (1995)ADSCrossRefGoogle Scholar
  61. 61.
    F. Yang, G.N. Phillips Jr., J. Mol. Biol. 256, 762 (1996)CrossRefGoogle Scholar
  62. 62.
    G. Henkelman, M.X. LaBute, C.S. Tung, P.W. Fenimore, B.H. McMahon, PNAS USA 102, 15347 (2005)ADSCrossRefGoogle Scholar
  63. 63.
    P.W. Fenimore, H. Frauenfelder, S. Magaz, B.H. McMahon, F. Mezei, F. Migliardo, R.D. Young, I. Stroe, Chem. Phys. 424, 2 (2013)ADSCrossRefGoogle Scholar
  64. 64.
    H. Frauenfelder, B.H. McMahon, R.H. Austin, K. Chu, J.T. Groves, PNAS USA 98, 2370 (2001)ADSCrossRefGoogle Scholar
  65. 65.
    A. Ansari, J. Berendzen, S.F. Bowne, H. Frauenfelder, M.K. Hong, I.E. Iben, T.B. Sauke, P.J. Steinbach, R.D. Young, PNAS USA 82, 5000 (1985)ADSCrossRefGoogle Scholar
  66. 66.
    J. Monod, J. Wyman, J.P. Changeux, J. Mol. Biol. 12, 88 (1965)CrossRefGoogle Scholar

Copyright information

© EDP Sciences and Springer 2014

Authors and Affiliations

  • Benjamin H. McMahon
    • 1
  • Hans Frauenfelder
    • 1
  • Paul W. Fenimore
    • 1
  1. 1.Theoretical Biology and Biophysics Group MS K710, Theoretical Division, Los Alamos National LaboratoryLos AlamosUSA

Personalised recommendations