Zaccai neutron resilience and site-specific hydration dynamics in a globular protein

Abstract

A discussion is presented of contributions of the Zaccai group to the understanding of flexibility in biological macromolecules using dynamic neutron scattering. The concept of resilience as introduced by Zaccai is discussed and investigated using molecular dynamics simulation on camphor-bound cytochrome P450. The resilience of hydrophilic residues is found to be more strongly affected by hydration than that of hydrophobic counterparts. The hydration-induced softening of protein propagates from the surface into the dry core. Moreover, buried hydrophilic residues behave more like those exposed on the protein surface, and are different from their hydrophobic counterparts.

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References

  1. 1.

    J. Randall, H.D. Middendorf, H.L. Crespi, A.D. Taylor, Nature 276, 636 (1978).

    ADS  Article  Google Scholar 

  2. 2.

    B. Jacrot, S. Cusack, A.J. Dianoux, D.M. Engelman, Nature 300, 84 (1982).

    ADS  Article  Google Scholar 

  3. 3.

    A.J.D.D.M. Engelman, S. Cusack, B. Jacrot, Basic Life Sci. 27, 365 (1984).

    Google Scholar 

  4. 4.

    J.C. Smith, S. Cusack, P. Poole, J. Finney, J. Biomol. Struct. Dyn. 4, 583 (1987).

    Article  Google Scholar 

  5. 5.

    J.C. Smith, S. Cusack, U. Pezzeca, B. Brooks, M. Karplus, J. Chem. Phys. 85, 3636 (1986).

    ADS  Article  Google Scholar 

  6. 6.

    J.C. Smith, S. Cusack, B. Tidor, M. Karplus, J. Chem. Phys. 93, 2974 (1990).

    ADS  Article  Google Scholar 

  7. 7.

    S. Cusack, J.C. Smith, J. Finney, B. Tidor, M. Karplus, J. Mol. Biol. 202, 903 (1988).

    Article  Google Scholar 

  8. 8.

    W. Doster, S. Cusack, W. Petry, Nature 337, 754 (1989).

    ADS  Article  Google Scholar 

  9. 9.

    F. Parak, E.N. Frolov, R.L. Mossbauer, V.I. Goldanskii, J. Mol. Biol. 145, 825 (1981).

    Article  Google Scholar 

  10. 10.

    J.C. Smith, K. Kuczera, M. Karplus, Proc. Natl. Acad. Sci. U.S.A. 87, 1601 (1990).

    ADS  Article  Google Scholar 

  11. 11.

    M. Ferrand, A.J. Dianoux, W. Petry, G. Zaccai, Proc. Natl. Acad. Sci. U.S.A. 90, 9668 (1993).

    ADS  Article  Google Scholar 

  12. 12.

    V. Reat, H. Patzelt, M. Ferrand, C. Pfister, D. Oesterhelt, G. Zaccai, Proc. Natl. Acad. Sci. U.S.A. 95, 4970 (1998).

    ADS  Article  Google Scholar 

  13. 13.

    K. Wood, U. Lehnert, B. Kessler, G. Zaccai, D. Oesterhelt, Biophys. J. 95, 194 (2008).

    Article  Google Scholar 

  14. 14.

    L. Cordone, M. Ferrand, E. Vitrano, G. Zaccai, Biophys. J. 76, 1043 (1999).

    Article  Google Scholar 

  15. 15.

    G. Zaccai, Science 288, 1604 (2000).

    ADS  Article  Google Scholar 

  16. 16.

    Y.T. Lee, R.F. Wilson, I. Rupniewski, D.B. Goodin, Biochemistry-Us 49, 3412 (2010).

    Article  Google Scholar 

  17. 17.

    J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kale, K. Schulten, J. Comput. Chem. 26, 1781 (2005).

    Article  Google Scholar 

  18. 18.

    Y. Miao, J. Baudry, Biophys. J. 101, 1493 (2011).

    ADS  Article  Google Scholar 

  19. 19.

    Z. Yi, Y.L. Miao, J. Baudry, N. Jain, J.C. Smith, J. Phys. Chem. B 116, 5028 (2012).

    Article  Google Scholar 

  20. 20.

    Y. Miao, Z. Yi, C. Cantrell, D. Glass, J. Baudry, N. Jain, J.C. Smith, Biophys. J. 103, 2167 (2012).

    ADS  Article  Google Scholar 

  21. 21.

    Y. Miao, Z. Yi, D.C. Glass, L. Hong, M. Tyagi, J. Baudry, N. Jain, J.C. Smith, J. Am. Chem. Soc. 134, 19576 (2012).

    Article  Google Scholar 

  22. 22.

    U. Essmann, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, L.G. Pedersen, J. Chem. Phys. 103, 8577 (1995).

    ADS  Article  Google Scholar 

  23. 23.

    J.-P. Ryckaert, G. Ciccotti, H.J.C. Berendsen, J. Comput. Phys. 23, 327 (1977).

    ADS  Article  Google Scholar 

  24. 24.

    E. Lindahl, B. Hess, D. van der Spoel, J. Mol. Model 7, 306 (2001).

    Google Scholar 

  25. 25.

    T. Becker, J.C. Smith, Phys. Rev. E 67, 021904 (2003).

    ADS  Article  Google Scholar 

  26. 26.

    L. Hong, X. Cheng, D.C. Glass, J.C. Smith, Phys. Rev. Lett. 108, 238102 (2012).

    ADS  Article  Google Scholar 

  27. 27.

    K. Wood, F.-X. Gallat, R. Otten, A.J. van Heel, M. Lethier, L. van Eijck, M. Moulin, M. Haertlein, M. Weik, F.A.A. Mulder, Angew. Chem. Int. Ed. 52, 665 (2013).

    Article  Google Scholar 

  28. 28.

    A.L. Tournier, J.C. Smith, Phys. Rev. Lett. 91, 20 (2003).

    Article  Google Scholar 

  29. 29.

    D.J. Bicout, G. Zaccai, Biophys. J. 80, 1115 (2001).

    ADS  Article  Google Scholar 

  30. 30.

    L. Hong, D.C. Glass, J.D. Nickels, S. Perticaroli, Z. Yi, M. Tyagi, H. O’Neill, Z. Qiu, A.P. Sokolov, J.C. Smith, Phys. Rev. Lett. 110, 028104 (2013).

    ADS  Article  Google Scholar 

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Correspondence to Jeremy C. Smith.

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Contribution to the Topical Issue “Neutron Biological Physics”, edited by Giovanna Fragneto and Frank Gabel.

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Miao, Y., Hong, L., Yi, Z. et al. Zaccai neutron resilience and site-specific hydration dynamics in a globular protein. Eur. Phys. J. E 36, 72 (2013). https://doi.org/10.1140/epje/i2013-13072-5

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Keywords

  • Topical issue: Neutron Biological Physics