The dynamics of protein hydration water: A quantitative comparison of molecular dynamics simulations and neutron-scattering experiments

Biophysical Journal

Volumn 79, Issue 6, 2000, Pages 3244-3257

  Tarek, Mounir ^a,b   Tobias, Douglas J ^c  

^a NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE A; WATER;

ARTICLE; CHEMICAL STRUCTURE; DIFFUSION; HYDRATION; HYDROGEN BOND; MOLECULAR DYNAMICS; NEUTRON SCATTERING; PROTEIN BINDING; ROTATION; SIMULATION;

EID: 0033637521     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76557-X     Document Type: Article

References (67)

1. Allen, M. P., and D. J. Tildesley. 1989. Computer Simulation of Liquids. Clarendon Press, Oxford.
2. Andersen, H. C. 1983. Rattle: a Velocity Version of the Shake Algorithm for Molecular Dynamics Calculations. J. Comp. Phys. 52:24-34.
3. Angell, C. A. 1995. Formation of Glasses from Liquids and Biopolymers. Science. 267:1924-1935.
4. Badger, J., and D. L. D. Caspar. 1991. Water Structure in Cubic Insulin Crystals. Proc. Natl. Acad. Sci. U. S. A. 88:622-626.
5. Barron, L. D., L. Hecht, and G. Wilson. 1997. The Lubricant of Life: A Proposal That Solvent Water Promotes Extremely Fast Conformational Fluctuations in Mobile Heteropolypeptide Structure. Biochemistry. 36: 13143-13147.
6. Beé, M. 1988. Quasielastic Neutron Scattering: Principles and Applications in Solid State Chemistry, Biology, and Materials Science. Adam Hilger, Bristol.
7. Bellissent-Funel, M. C. 2000. Hydration in Protein Dynamics and Function. J. Molec. Liq. 94:39-52.
8. Bellissent-Funel, M. C., K. F. Bradley, S. H. Chen, J. Lal, and J. Teixeira. 1993. Slow Dynamics of Water Molecules in Confined Space. Physica A. 201:277-285.
9. Bellissent-Funel, M. C., J. M. Zanotti, and S. H. Chen. 1996. Slow Dynamics of Water Molecules on the Surface of a Globular Protein. Faraday Discuss. 103:281-294.
10. Berendsen, H. J. C., J. R. Grigera, and T. P. Straatsma. 1987. The Missing Term in Effective Pair Potentials. J. Phys. Chem. 91:6269-6271.
11. Bizzarri, A. R., and S. Cannistraro. 1996. Molecular Dynamics Simulation Evidence of Anomalous Diffusion of Protein Hydration Water. Phys. Rev. E. 53:3040-3043.
12. Bizzarri, A. R., and S. Cannistraro. 1997. Anomalous and Anisotropic Diffusion of Plastocyanin Hydration Water. Europhys. Lett. 37:201-206.
13. Bizzarri, A. R., C. Rocchi, and S. Cannistraro. 1996. Origin of the Anomalous Diffusion Observed by MD Simulation at the Protein-Water Interface. Chem. Phys. Lett. 263:559-566.
14. Boon, J. P., and S. Yip. 1991. Molecular Hydrodynamics. Dover, New York.
15. Bryant, R. G. 1996. The Dynamics of Water-Protein Interactions. Annu. Rev. Biophys. Biomol. Struct. 25:29-53.
16. Burling, F. T., W. I. Weis, K. M. Flaherty, and A. T. Brünger. 1996. Direct Observation of Protein Solvation and Discrete Disorder with Experimental Crystallographic Phase. Science. 217:72-77.
17. Chen, S. H., P. Gallo, F. Sciortino, and P. Tartaglia. 1997. Molecular-Dynamics Study of Incoherent Quasielastic Neutron-Scattering Spectra of Supercooled Water. Phys. Rev. E. 56:4231-4243.
18. Cheng, X., and B. P. Schoenborn. 1990. Hydration in Protein Crystals. A Neutron Diffraction Analysis of Carbonmonoxymyoglobin. Acta Cryst. B46:195-208.
19. Denisov, V. P., and B. Halle. 1995:Protein Hydration Dynamics in Aqueous Solution. A Comparison of Bovine Pancreatic Trypsin Inhibitor and Ubiquitin by Oxygen-17. Spin Relaxation Dispersion. J. Mol. Biol. 245:682-697.
20. Denisov, V. P., and B. Halle. 1996. Protein Hydration Dynamics in Aqueous Solution. Faraday Disc. 103:227-244.
21. 2H Magnetic Relaxation Dispersion. Biochemistry. 37:9595-9604.
22. Doster, W., S. Cusack, and W. Petry. 1990. Dynamical Instability of Liquidlike Motions in a Globular Protein Observed by Inelastic Neutron Scattering. Phys. Rev. Lett. 65:1080-1083.
23. Doster, W., and M. Settles. 1999. The Dynamical Transition in Proteins: The Role of Hydrogen Bonds. In Hydration Processes in Biology: Experimental and Theoretical Approaches. M.-C. Bellissent-Funel, editor. IOS Press, Amsterdam. 177-191.
24. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, and L. G. Pedersen. 1995. A Smooth Particle Mesh Ewald Method. J. Chem. Phys. 103: 8577-8593.
25. Ferrand, M., A. J. Dianoux, W. Petry, and G. G. Zaccai. 1993. Thermal Motions and Function of Bacteriorhodopsin in Purple Membranes: Effects of Temperature and Hydration Studied by Neutron Scattering. Proc. Natl. Acad. Sci. U. S. A. 90:9668-9672.
26. Fitter, J. 1999. The Temperature Dependence of Internal Molecular Motions in Hydrated and Dry α-Amylase: The Role of Hydration Water in the Dynamical Transition of Proteins. Biophys. J. 76:1034-1042.
27. Fitter, J., R. E. Lechner, and N. A. Dencher. 1997. Picosecond Molecular Motions in Bacteriorhodopsin from Neutron Scattering. Biophys. J. 73:2126-2137.
28. Frick, B., and D. Richter. 1995. The Microscopic Basis of the Glass Transition in Polymers from Neutron Scattering Studies. Science. 267: 1939-1945.
29. Gallo, P., F. Sciortino, P. Tartaglia, and S. H. Chen. 1996. Slow Dynamics of Water Molecules in Supercooled States. Phys. Rev. Lett. 76: 2730-2733.
30. Goldanskii, V. I., and Y. F. Krupyanskii. 1989. Protein and Protein-Bound Water Dynamics Studied by Raleigh Scattering of Mössbauer Radiation (RSMR). Quart. Rev. Biophys. 22:39-92.
31. Halle, B. 1999a. Magnetic Relaxation Dispersion: Principles and Applications. In Hydration Processes in Biology: Theoretical and Experimental Approaches. M.-C. Bellissent-Funel, editor. IOS Press, Amsterdam. 221-232.
32. Halle, B. 1999b. Water in Biological Systems: The NMR Picture. In Hydration Processes in Biology: Theoretical and Experimental Approaches. M.-C. Bellissent-Funel, editor. IOS Press, Amsterdam. 233-249.
33. Jiang, J. S., and A. T. Brünger. 1994. Protein Hydration Observed by X-Ray Diffraction. Solvation Properties of Penicillopepsin and Neuraminidase Crystal Structures. J. Mol. Biol. 243:100-115.
34. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of Simple Potential Functions for Simulating Liquid Water. J. Chem. Phys. 79:926-935.
35. Lehnen, U., V. Réat, M. Weik, G. Zaccaï, and C. Pfister. 1998. Thermal Motion in Bacteriorhodopsin at Different Hydration Levels Studied by Neutron Scattering: Correlation with Kinetics and Light-Induced Conformational Changes. Biophys. J. 75:1945-1952.
36. Leyser, H., W. Doster, and M. Diehl. 1999. Far-Infrared Emission by Boson Peak Vibrations in a Globular Protein. Phys. Rev. Lett. 82: 2987-2990.
37. Lichtenegger, H., W. Doster, T. Kleinen, A. Birk, B. Sepiol, and G. Vogl. 1999. Heme-Solvent Coupling: A Mössbauer Study of Myoglobin in Sucrose. Biophys. J. 76:414-422.
38. MacKerell, Jr., A. D., D. Bashford, M. Bellott, R. L. Dunbrack, Jr., J. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher, I. I. I., B. Roux, M. Schlenkrich, J. C. Smith, R. Stole, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. 1998. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins. J. Phys. Chem. B. 102:3586-3616.
39. Martyna, G. J., D. J. Tobias, and M. L. Klein. 1994. Constant Pressure Molecular Dynamics Simulations. J. Chem. Phys. 101:4177-4189.
40. Martyna, G. J., M. E. Tuckerman, and M. L. Klein. 1992. Nosé-Hoover Chains: the Canonical Ensemble via Continuous Dynamics. J. Chem. Phys. 97:2635-2643.
41. Martyna, G. J., M. E. Tuckerman, D. J. Tobias, and M. L. Klein. 1996. Explicit Reversible Integrators for Extended Systems Dynamics. Molec. Phys. 87:1117-1157.
42. Meyer, E. 1992. Internal Water Molecules and H-Bonding in Biological Macromolecules: A Review of Structural Features with Functional Implications. Protein Sci. 1:1543-1562.
43. Middendorf, H. D. 1984. Biophysical Applications of Quasi-elastic and Inelastic Neutron Scattering. Ann. Rev. Biophys. Bioeng. 13:425-451.
44. Middendorf, H. D. 1996. Neutron Studies of the Dynamics of Biological Water. Physica B. 226:113-127.
45. Otting, G. 1997. NMR Studies of Water Bound to Biological Molecules. Prog. NMR Spect. 31:259-285.
46. Otting, G., E. Liepinsh, and K. Wüthrich. 1991. Protein Hydration in Aqueous Solution. Science. 254:974-980.
47. Otting, G., and K. Wüthrich. 1989. Studies of Protein Hydration in Aqueous Solution by Direct NMR Observation of Individual Protein-Bound Water Molecules. J. Am. Chem. Soc. 111:1871-1875.
48. Paciaroni, A., A. R. Bizzarri, and S. Cannistraro. 1998. Molecular-Dynamics Simulation Evidences of a Boson Peak in Protein Hydration Water. Phys. Rev. E. 57:6277-6280.
49. Paciaroni, A., A. R. Bizzarri, and S. Cannistraro. 1999. Neutron Scattering Evidence of a Boson Peak in Protein Hydration Water. Phys. Rev. E. 60:2476-2479.
50. Phillips, G. N., and B. M. Pettitt. 1995. Structure and Dynamics of the Water Around Myoglobin. Protein Sci. 4:149-158.
51. Polnaszek, C. F., and R. G. Bryant. 1984. Nitroxide Radical Induced Solvent Proton Relaxation: Measurements of Localized Translational Diffusion. J. Chem. Phys. 81:4038-4045.
52. Randall, J., H. D. Middendorf, H. L. Crespi, and A. D. Taylor. 1978. Dynamics of Protein Hydration by Quasi-elastic Neutron Scattering. Nature. 276:636-638.
53. Rasmussen, B. F., A. M. Stock, D. Ringe, and G. A. Petsko. 1992. Crystalline Ribonuclease A Loses Function Below the Dynamical Transition at 220 K. Nature. 357:423-424.
54. Rocchi, C., A. R. Bizzarri, and S. Cannistraro. 1998. Water Dynamical Anomalies Evidenced by Molecular-Dynamics Simulations at the Solvent-Protein Interface. Phys. Rev. E. 57:3315-3325.
55. Rupley, J. A., and G. Careri. 1991. Protein Hydration and Function. Adv. Protein Chem. 41:37-172.
56. Ryckaert, J.-P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of n-Alkanes. J. Comp. Phys. 23: 327-341.
57. Settles, M., and W. Doster. 1996. Anomalous Diffusion of Adsorbed Water: A Neutron Scattering Study of Hydrated Myoglobin. Faraday Discuss. 103:269-279.
58. Steinhoff, H. J., B. Kramm, G. Hess, C. Owerdieck, and A. Redhardt. 1993. Rotational and Translational Water Diffusion in the Hemoglobin Hydration Shell. Biophys. J. 65:1486-1495.
59. Tarek, M., and D. J. Tobias. 1999. Environmental Dependence of the Dynamics of Protein Hydration Water. J. Am. Chem. Soc. 121: 9740-9741.
60. Teeter, M. M. 1991. Water-Protein Interactions: Theory and Experiment. Ann. Rev. Biophys. Chem. 20:577-600.
61. Tilton, Jr., R. F., J. C. Dewan, and G. A. Petsko. 1992. Effect of Temperature on Protein Structure and Dynamics: X-ray Crystallographic Studies of the Protein Ribonuclease-A at Nine Different Temperatures from 98 to 320 K. Biochemistry. 31:2469-2481.
62. Vitkup, D., D. Ringe, G. A. Petsko, and M. Karplus. 2000. Solvent Mobility and the Protein 'Glass' Transition. Nature Struct. Biol. 7:34-38.
63. Weast, R. C. 1971. Handbook of Chemistry and Physics. CRC Press, Boca Raton.
64. Williams, M. A., J. M. Goodfellow, and J. M. Thornton. 1994. Buried Waters and Internal Cavities in Monomeric Proteins. Protein Sci. 3:1224-1235.
65. Wlodawer, A. 1982. Neutron Protein Crystallography. Prog. Biophys. Mol. Biol. 40:115-157.
66. Wlodawer, A., L. A. Svensson, L. Sjolin, and G. Gilliland. 1988. Structure of Phosphate Free Ribonuclease A Refined at 1.26 Å Resolution. Biochemistry. 27:2705-2717.
67. Zanotti, J. M., M. C. Bellissent-Funel, and S. H. Chen. 1999. Relaxational Dynamics of Supercooled Water in Porous Glass. Phys. Rev. E. 59: 3084-3093.