Osmolyte trimethylamine-N-oxide does not affect the strength of hydrophobic interactions: Origin of osmolyte compatibility

Biophysical Journal

Volumn 89, Issue 2, 2005, Pages 858-866

  Athawale, Manoj V ^a   Dordick, Jonathan S ^a   Garde, Shekhar ^a  

^a Rensselaer Polytechnic Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYMER; TRIMETHYLAMINE OXIDE; WATER;

AQUEOUS SOLUTION; ARTICLE; HYDRATION; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PROTEIN FOLDING; PROTEIN STRUCTURE; THERMODYNAMICS;

EID: 23244459863     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.056671     Document Type: Article

References (59)

1. Wang, A., and D. W. Bolen. 1997. A naturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry. 36:9101-9108.
2. Yancey, P. H., M. E. Clark, S. C. Hand, R. D. Bowlus, and G. N. Somero. 1982. Living with water stress: evolution of osmolyte systems. Science. 217:1214-1222.
3. Lin, T.-Y., and S. N. Timasheff. 1994. Why do some organisms use a urea-methylamine mixture as osmolyte? Thermodynamic compensation of urea and trimethylamine n-oxide interactions with protein. Biochemistry. 33:12695-12701.
4. Gillett, M. B., J. R. Suko, F. O. Santoso, and P. H. Yancey. 1997. Elevated levels of trimethylamine oxide in muscles of deep-sea gadiform teleosts: A high-pressure adaptation. J. Exp. Tool. 279:386-391.
5. Yancey, P. H. 2001. Water stress, osmolytes and proteins. Am. Zool. 41:669-709.
6. Yancey, P. H., W. R. Blake, and J. Conley, 2002. Unusual organic osmolytes in deep-sea animals: adaptations to hydrostatic pressure and other perturbants. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133:667-676.
7. Timasheff, S. N. 2003. Preferential interactions of urea with lysozyme and their linkage to protein denaturation, Biophys. Chem. 105:421-448.
8. Somero, G. N., C. B. Osmond, and C. L. Bolis. 2001. Water and Life. Springer-Verlag, New York.
9. Liu, Y., and D. W. Bolen. 1995. The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes. Biochemists. 34:12884-12891.
10. Baskakov, I., and D. W. Bolen. 1998. Forcing thermodynamically unfolded proteins to fold. J. Biol. Chem. 273:4831-4834.
11. Bolen, D. W., and I. V. Baskakov. 2001. The osmophobic effect: natural selection of a thermodynamics force in protein folding. J. Mol. Biol. 310:955-963.
12. Zou, Q., B. J. Bennion, V. Daggett, and K. P. Murphy. 2002. The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea. J. Am. Chem. Soc. 124:1192-1202.
13. Bennion, B. J., and V. Daggett. 2004. Counteraction of urea-induced protein denaturation by trimethylamine n-oxide: a chemical chaperone at atomic resolution. Proc. Natl. Acad. Sci. USA. 101:6433-6438.
14. Dill, K. A. 1990. Dominant forces in protein folding. Biochemistry. 29:7133-7135.
15. Tanford, C. 1973. The Hydrophobic Effect: Formation of Micelles and Biological Membranes. John Wiley, New York.
16. Kauzmann, W. 1959. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 14:1-63.
17. Pratt, L. R.. and A. Pohorille. 2002. Hydrophobic effects and modeling of biophysical aqueous solution interfaces. Chem. Rev. 102:2671-2692.
18. Berendsen, H. J. C., D. van der Spoel, and R. van Drunen. 1995. Gromacs: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91:43-56.
19. Lindahl, E., B. Hess, and D. van der Spoel. 2001. Gromacs 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
20. 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.
21. Kast, K. M., J. Brickmann, S. M. Kast, and R. S. Berry. 2003. Binary phases of aliphatic n-oxides and water: Force field development and molecular dynamics simulation. J. Phys. Chem. A. 107:5342-5351.
22. Allen, M. P., and D. J. Tildesley. 1987. Computer Simulation of Liquids. Clarendon Press, Oxford.
23. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald: An n loe(n) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
24. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. DiNola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
25. Miyamoto, S., and P. A. Kollman. 1992. Settle: an analytical version of the shake and rattle algorithm for rigid water models. J. Comput. Chem. 13:952-962.
26. Chau, P. L., and A. J. Hardwick. 1998. A new order parameter for tetrahedral configurations. Mol. Phys. 92:511-518.
27. Truskett, T. M., S. Torquato, and P. G. Debenedetti. 2000. Towards a quantification of disorder in materials: distinguishing equilibrium and glassy sphere packings. Phys. Rev. E. 62:993-1001.
28. Torquato, S., T. M. Truskett, and P. G. Debenedetti. 2000. Is random close packing of spheres well defined? Phys. Rev. Lett. 84:2064-2067.
29. Errington, J. R., and P. G. Debenedetti. 2001. Relationship between structural order and the anomalies of liquid water. Nature. 409:318-321.
30. Widom, B. 1963. Some topics in the theory of fluids. J. Chem. Phys. 39:2808-2812.
31. Widom, B. 1982. Potential distribution theory and statistical mechanics of fluids. J. Phys. Chem. 86:869-872.
32. Verlet, L., and J. J. Weis. 1972. Perturbation-theory for thermodynamic properties of simple liquids. Mol. Phys. 24:1013-1024.
33. Garde, S., A. E. Garcia, L. R. Pratt, and G. Hummer. 1999. Temperature dependence of the solubility of nonpolar gases in water. Biophys. Chem. 78:21-32.
34. ten Wolde, P. R., and D. Chandler. 2002. Drying-induced hydrophobic polymer collapse. Proc. Natl. Acad. Sci. USA. 99:6539-6543.
35. Ghosh, T., A. Kalra, and S. Garde. 2005. On the salt-induced stabilization of pair and many-body hydrophobic interactions. J. Phys. Chem. B. 109:642-651.
36. Beutler, T. C., and W. F. V. Gunsteren. 1994. The computation of a potential of mean force: choice of the biasing potential in the umbrella sampling technique. J. Chem. Phys. 100:1492-1497.
37. Ferrenberg, A. M., and R. H. Swendsen. 1989. Optimized Monte Carlo data analysis. Phys. Rev. Lett. 63:1195-1198.
38. Frenkel, D., and B. Smit. 2001. Understanding Molecular Simulation. Academic Press, New York.
39. Pratt, L. R., and D. Chandler. 1977. Theory of the hydrophobic effect. J. Chem. Phys. 67:3683-3704.
40. Pratt, L. R., and D. Chandler. 1980. Effects of solute-solvent attractive forces on hydrophobic correlations. J. Chem. Phys. 73:3434-3441.
41. Ghosh, T., A. E. Garcia, and S. Garde. 2002. Enthalpy and entropy contributions to the pressure dependence of hydrophobic interactions. J. Chem. Phys. 116:2480-2486.
42. Ghosh, T., A. E. Garcia, and S. Garde. 2001. Molecular dynamics simulations of pressure effects on hydrophobic interactions. J. Am. Chem. Soc. 123:10997-11003.
43. Ghosh, T., A. E. Garcia, and S. Garde. 2003. Water-mediated three-particle hydrophobic interactions between hydrophobic solutes: size, pressure, and salt dependences. J. Phys. Chem. B. 107:612-617.
44. Kalra, A., N. Tugcu, S. M. Cramer, and S. Garde. 2001. Salting-in and salting-out of hydrophobic solutes in aqueous salt solutions. J. Phys. Chem. B. 105:6380-6386.
45. Smith, P. E. 1999. Computer simulation of cosolvent effects on hydrophobic hydration. J. Phys. Chem. B. 103:525-534.
46. Hummer, G., and S. Garde. 1998. Cavity expulsion and weak dewetting of hydrophobic solutes in water. Phys. Rev. Lett. 80:4193-4196.
47. Kita, Y., T. Arakawa, T.-Y. Lin, and S. N. Timasheff. 1994. Contribution of the surface free energy perturbation to protein-solvent interactions. Biochemistry. 33:15178-15189.
48. Arakawa, T., and S. N. Timasheff. 1985. The stabilization of proteins by osmolytes. Biophys. J. 47:411-414.
49. Arakawa, T., and S. N. Timasheff. 1982. Stabilization of protein structure by sugars. Biochemistry. 21:6536-6544.
50. Arakawa, T., and S. N. Timasheff. 1984. Mechanism of protein salting in and salting out by divalent cation salts: balance between hydration and salt binding. Biochemistry. 25:5912-5923.
51. Parsegian, V. A., R. P. Rand, and D. C. Rau. 2000. Osmotic stress, crowding, preferential hydration, and binding: a comparison of perspectives. Proc. Natl. Acad. Sci. USA. 97:3987-3992.
52. Baynes, B. M., and B. L. Trout. 2003. Proteins in mixed solvents: a molecular-level perspective. J. Phys. Chem. B. 107:14058-14067.
53. Shimizu, S. 2004. Estimating hydration changes upon biomolecular reactions from osmotic stress, high pressure, and preferential hydration experiments. Proc. Natl. Acad. Sci. USA. 101:1195-1199.
54. Schellman, J. A. 1978. Solvent denaturation. Biopolymers. 17:1305-1322.
55. Ashbaugh, H. S., D. Asthagiri. L. R. Pratt, and S. B. Rempe. 2003. Hydration of krypton and consideration of clathrate models of hydrophobic effects from the perspective of quasi-chemical theory. Biophys. Chem. 105:323-338.
56. Garde, S., G. Hummer, and M. E. Paulaitis. 1996. Hydrophobic interactions: conformational equilibria and the association of nonpolar molecules in water. Faraday Discuss. 103:125-139.
57. Garde, S., G. Hummer, and M. E. Paulaitis. 1998. Free energy of hydration of a molecular ionic solute: tetramethylammonium ion. J. Chem. Phys. 108:1552-1561.
58. Rajamani, S., T. Ghosh, and S. Garde. 2004. Size dependent ion hydration, its asymmetry, and convergence to macroscopic behavior. J. Chem. Phys. 120:4457-4466.
59. Bennion, B. J., M. L. DeMarco, and V. Daggett. 2004. Preventing misfolding of the prion protein by trimethylamine n-oxide. Biochemistry. 43:12955-12963.