The European Physical Journal E

, Volume 12, Issue 1, pp 153–158 | Cite as

Low-temperature behavior of water confined by biological macromolecules and its relation to protein dynamics

Article

Abstract.

Confined water is an essential component of biological entities and processes and its properties differ from the ones of bulk water. Since protein and water dynamics are thought to be strongly coupled, and since macromolecular dynamics is crucial for biological function, the study of water confined by biological macromolecules is not only interesting on its own right but often provides useful information for understanding biological activity at the molecular level. Studies are reviewed that focus on the low-temperature behavior of water confined in protein crystals and in stacks of native biological membranes. Diffraction methods allowed the determination of characteristic changes that relate to the glass transition and crystallization of water. Protein crystallography and energy-resolved neutron scattering are employed to gain further insight into the coupling of solvent and protein dynamics.

Keywords

Crystallization Biological Activity Glass Transition Macromolecule Biological Function 

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References

  1. 1.
    C. Bon, M.S. Lehmann, C. Wilkinson, Acta Crystallogr., Sect. D 55, 978 (1999).CrossRefGoogle Scholar
  2. 2.
    C. Bon, A.J. Dianoux, M. Ferrand, M.S. Lehmann, Biophys. J. 83, 1578 (2002).Google Scholar
  3. 3.
    M.-C. Bellissent-Funel, J. Phys. Condens. Matter 13, 9165 (2001).CrossRefGoogle Scholar
  4. 4.
    H.J. Sass, I.W. Schachowa, G. Rapp, M.H.J. Koch, D. Oesterhelt, N.A. Dencher, G. Büldt, EMBO J. 16, 1484 (1997).CrossRefGoogle Scholar
  5. 5.
    M. Weik, G. Zaccai, N.A. Dencher, D. Oesterhelt, T. Hauss, J. Mol. Biol. 275, 625 (1998).CrossRefGoogle Scholar
  6. 6.
    J.A. Rupley, G. Careri, Protein Hydration and Function, in Advances in Protein Chemistry, edited by C. Anfinsen, J.T. Edsall, F.M. Richards, D.S. Eisenberg, Vol. 41 (Academic Press, New York, 1991) pp. 37-172.Google Scholar
  7. 7.
    U. Lehnert, V. Reat, M. Weik, G. Zaccai, C. Pfister, Biophys. J. 75, 1945 (1998).Google Scholar
  8. 8.
    F. Parak, Methods Enzymol. 127, 196 (1986).Google Scholar
  9. 9.
    H. Kanno, R.J. Speedy, C.A. Angell, Science 189, 880 (1975).Google Scholar
  10. 10.
    C.A. Angell, Science 267, 1924 (1995).Google Scholar
  11. 11.
    P.G. Debenedetti, F.H. Stillinger, Nature 410, 259 (2001).CrossRefGoogle Scholar
  12. 12.
    G.P. Johari, A. Hallbrucker, E. Mayer, Nature 330, 552 (1987).CrossRefGoogle Scholar
  13. 13.
    M. Fisher, J.P. Devlin, J. Phys. Chem. 99, 11584 (1995).Google Scholar
  14. 14.
    J.A. McMillan, S.C. Los, Nature 206, 806 (1965).Google Scholar
  15. 15.
    R.S. Smith, B.D. Kay, Nature 398, 788 (1999).CrossRefGoogle Scholar
  16. 16.
    A. Mishima, H.E. Stanley, Nature 396, 329 (1998).CrossRefGoogle Scholar
  17. 17.
    V. Velikov, S. Borick, C.A. Angell, Science 294, 2335 (2001).CrossRefGoogle Scholar
  18. 18.
    G. Sartor, A. Hallbrucker, E. Mayer, Biophys. J. 69, 2679 (1995).Google Scholar
  19. 19.
    W. Doster, A. Bachleitner, R. Dunau, M. Hiebl, E. Lüscher, Biophys. J. 50, 213 (1986).Google Scholar
  20. 20.
    D. Beece, L. Eisenstein, H. Frauenfelder, D. Good, M.C. Marden, L. Reinisch, A.H. Reynolds, L.B. Sorensen, K.T. Yue, Biochemistry 19, 5147 (1980).Google Scholar
  21. 21.
    D. Vitkup, D. Ringe, G.A. Petsko, M. Karplus, Nat. Struct. Biol. 7, 34 (2000).CrossRefGoogle Scholar
  22. 22.
    R. Walser, W.F. van Gunsteren, Proteins 42, 414 (2001).CrossRefGoogle Scholar
  23. 23.
    F. Parak, E.W. Knapp, D. Kucheida, J. Mol. Biol. 161, 177 (1982).Google Scholar
  24. 24.
    W. Doster, S. Cusack, W. Petry, Nature 337, 754 (1989).PubMedGoogle Scholar
  25. 25.
    M. Ferrand, A.J. Dianoux, W. Petry, G. Zaccai, Proc. Natl. Acad. Sci. USA 90, 9668 (1993).Google Scholar
  26. 26.
    J. Fitter, Biophys. J. 76, 1034 (1999).Google Scholar
  27. 27.
    A.M. Tsai, D.A. Neumann, L.N. Bell, Biophys. J. 79, 2728 (2000).Google Scholar
  28. 28.
    G. Zaccai, Science 288, 1604 (2000).CrossRefGoogle Scholar
  29. 29.
    F. Gabel, D. Bicout, U. Lehnert, M. Tehei, M. Weik, G. Zaccai, Q. Rev. Biophys. 35, 327 (2002).CrossRefGoogle Scholar
  30. 30.
    H. Frauenfelder, S.G. Sligar, P.G. Wolynes, Science 254, 1598 (1991).PubMedGoogle Scholar
  31. 31.
    B.F. Rasmussen, A.M. Stock, D. Ringe, G.A. Petsko, Nature 357, 423 (1992).PubMedGoogle Scholar
  32. 32.
    R.M. Daniel, J.C. Smith, M. Ferrand, S. Hery, R. Dunn, J.L. Finney, Biophys. J. 75, 2504 (1998).Google Scholar
  33. 33.
    J.M. Bragger, R.V. Dunn, R.M. Daniel, Biochim. Biophys. Acta 1480, 278 (2000).CrossRefGoogle Scholar
  34. 34.
    D.J. Heyes, A.V. Ruban, H.M. Wilks, C.N. Hunter, Proc. Natl. Acad. Sci. USA 99, 11145 (2002).CrossRefGoogle Scholar
  35. 35.
    I.E. Iben, D. Braunstein, W. Doster, H. Frauenfelder, M.K. Hong, J.B. Johnson, S. Luck, P. Ormos, A. Schulte, P.J. Steinbach, A.H. Xie, R.D. Young, Phys. Rev. Lett. 62, 1916 (1989).CrossRefGoogle Scholar
  36. 36.
    P.W. Fenimore, H. Frauenfelder, B.H. McMahon, F.G. Parak, Proc. Natl. Acad. Sci. USA 99, 16047 (2002).CrossRefGoogle Scholar
  37. 37.
    V. Réat, G. Zaccai, M. Ferrand, C. Pfister, Functional dynamics in purple membrane, in Biological Macromolecular Dynamics (Adenine, Guilderland, NY, 1997) pp. 117-122.Google Scholar
  38. 38.
    J.A. Hayward, J.C. Smith, Biophys. J. 82, 1216 (2002).Google Scholar
  39. 39.
    H. Lichtenegger, W. Doster, T. Kleinert, A. Birk, B. Sepiol, G. Vogl, Biophys. J. 76, 414 (1999).Google Scholar
  40. 40.
    W. Doster, M. Settles, The Dynamical Transition in Proteins: The Role of Hydrogen Bonds, in Hydration Processes in Biology, edited by M.-C. Bellissent-Funel, Vol. 305 (IOS, Amsterdam, 1998).Google Scholar
  41. 41.
    V. Réat, R. Dunn, M. Ferrand, J.L. Finney, R.M. Daniel, J.C. Smith, Proc. Natl. Acad. Sci. USA 97, 9961 (2000).CrossRefGoogle Scholar
  42. 42.
    M. Tarek, D.J. Tobias, Phys. Rev. Lett. 88, 138101 (2002).CrossRefGoogle Scholar
  43. 43.
    A.B. Fulton, Cell 30, 345 (1982).Google Scholar
  44. 44.
    E.F. Garman, T.R. Schneider, J. Appl. Crystallogr. 30, 211 (1997).CrossRefGoogle Scholar
  45. 45.
    T.-Y. Teng, K. Moffat, J. Appl. Crystallogr. 31, 252 (1998).CrossRefGoogle Scholar
  46. 46.
    E.H. Snell, R.A. Judge, M. Larson, M.J. van der Woerd, J. Synchrotron Rad. 9, 361 (2002).CrossRefGoogle Scholar
  47. 47.
    J.L. Sussman, M. Harel, F. Frolow, C. Oefner, A. Goldman, L. Toker, I. Silman, Science 253, 872 (1991).PubMedGoogle Scholar
  48. 48.
    M. Weik, G. Kryger, A.M. Schreurs, B. Bouma, I. Silman, J.L. Sussman, P. Gros, J. Kroon, Acta Crystallogr., Sect. D 57, 566 (2001).CrossRefGoogle Scholar
  49. 49.
    W.P. Burmeister, Acta Crystallogr., Sect. D 56, 328 (2000).CrossRefGoogle Scholar
  50. 50.
    R.B. Ravelli, S.M. McSweeney, Structure Fold Des. 8, 315 (2000).CrossRefGoogle Scholar
  51. 51.
    M. Weik, R.B. Ravelli, G. Kryger, S. McSweeney, M.L. Raves, M. Harel, P. Gros, I. Silman, J. Kroon, J.L. Sussman, Proc. Natl. Acad. Sci. USA 97, 623 (2000).CrossRefGoogle Scholar
  52. 52.
    M. Weik, R.B. Ravelli, I. Silman, J.L. Sussman, P. Gros, J. Kroon, Protein Sci. 10, 1953 (2001).CrossRefGoogle Scholar
  53. 53.
    A.E. Blaurock, W. Stoeckenius, Nature New Biol. 233, 152 (1971).Google Scholar
  54. 54.
    U. Haupts, J. Tittor, D. Oesterhelt, Annu. Rev. Biophys. Biomol. Struct. 28, 367 (1999).CrossRefGoogle Scholar
  55. 55.
    D. Oesterhelt, W. Stoeckenius, Methods Enzymol. 31, 667 (1974).Google Scholar
  56. 56.
    G. Zaccai, D.J. Gilmore, J. Mol. Biol. 132, 181 (1979).Google Scholar
  57. 57.
    P.K. Rogan, G. Zaccai, J. Mol. Biol. 145, 281 (1981).Google Scholar
  58. 58.
    G. Zaccai, J. Mol. Biol. 194, 569 (1987).Google Scholar
  59. 59.
    N.A. Dencher, D. Dresselhaus, G. Zaccai, G. Büldt, Proc. Natl. Acad. Sci. USA 86, 7876 (1989).Google Scholar
  60. 60.
    G. Papadopoulos, N.A. Dencher, G. Zaccai, G. Büldt, J. Mol. Biol. 214, 15 (1990).Google Scholar
  61. 61.
    R.E. Lechner, J. Fitter, N.A. Dencher, T. Hauss, J. Mol. Biol. 277, 593 (1998).CrossRefGoogle Scholar
  62. 62.
    R. Bergman, J. Swenson, Nature 403, 283 (2000).CrossRefGoogle Scholar
  63. 63.
    V. Réat, H. Patzelt, M. Ferrand, C. Pfister, D. Oesterhelt, G. Zaccai, Proc. Natl. Acad. Sci. USA 95, 4970 (1998).CrossRefGoogle Scholar
  64. 64.
    J. Fitter, R.E. Lechner, N.A. Dencher, J. Phys. Chem. B 103, 8036 (1999).CrossRefGoogle Scholar
  65. 65.
    R.E. Lechner, N.A. Dencher, J. Fitter, Th. Dippel, Solid State Ionics 70/71, 296 (1994).Google Scholar
  66. 66.
    R. Korenstein, B. Hess, Nature 270, 184 (1977).Google Scholar
  67. 67.
    G. Váró, J.K. Lanyi, Biophys. J. 59, 313 (1991).Google Scholar

Copyright information

© Springer-Verlag Berlin/Heidelberg 2003

Authors and Affiliations

  1. 1.Laboratoire de Biophysique MoléculaireInstitut de Biologie StructuraleGrenoble Cedex 1France

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