Water mediation in protein folding and molecular recognition

Annual Review of Biophysics and Biomolecular Structure

Volumn 35, Issue , 2006, Pages 389-415

  Levy, Yaakov ^a   Onuchic, José N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Energy landscape; Folding funnel; Protein association; Protein DNA interactions; Solvent effect

Indexed keywords

NUCLEIC ACID; PROTEIN; WATER;

ENTHALPY; ENTROPY; MACROMOLECULE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW;

BINDING SITES; COMPUTER SIMULATION; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS; SOLVENTS; WATER;

EID: 33745032291     PISSN: 10568700     EISSN: None     Source Type: Book Series    
DOI: 10.1614/WT-05-118R.1     Document Type: Review

References (150)

1. Agmon N. 1995. The Grotthuss mechanism. Chem. Phys. Lett. 244:456-62
2. Ansari A, Jones CM, Henry ER, Hofrichter J, Eaton WA. 1992. The role of solvent viscosity in the dynamics of protein conformational changes. Science 256:1796-98
3. Athawale MV, Dordick JS, Garde S. 2005. Osmolyte trimethylamine-N-oxide does not affect the strength of hydrophobic interactions: origin of osmolyte compatibility. Biophys. J. 89:858-66
4. Autenrieth F, Tajkhorshid E, Schulten K, Luthey-Schulten Z. 2004. Role of water in transient cytochrome c(2) docking. J. Phys. Chem. B 108:20376-87
5. Baker NA. 2005. Improving implicit solvent simulations: a Poisson-centric view. Curr. Opin. Struct. Biol. 15:137-43
6. 2O: A Biography of Water. London: Weidenfeld & Nicolson
7. Ball P. 2005. Water and life: seeking the solution. Nature 436:1084-85
8. Barron LD, Hecht L, Wilson G. 1997. The lubricant of life: a proposal that solvent water promotes extremely fast conformational fluctuations in mobile heteropolypeptide structure. Biochemistry 36:13143-47
9. Benner SA, Ricardo A, Carrigan MA. 2004. Is there a common chemical model for life in the universe? Curr. Opin. Chem. Biol. 8:672-89
10. Bennion BJ, Daggett V. 2003. The molecular basis for the chemical denaturation of proteins by urea. Proc. Natl. Acad. Sci. USA 100:5142-47
11. Bennion BJ, Daggett V. 2004. Counteraction of urea-induced protein denaturation by trimethylamine N-oxide: a chemical chaperone at atomic resolution. Proc. Natl. Acad. Sci. USA 101:6433-38
12. Bhat TN, Bentley GA, Boulot G, Greene MI, Tello D, et al. 1994. Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proc. Natl. Acad. Sci. USA 91:1089-93
13. Bizzarri AR, Cannistraro S. 2002. Molecular dynamics of water at the protein-solvent interface. J. Phys. Chem. B 106:6617-33
14. Blokzijl W, Engberts JBFN. 1993. Hydrophobic effects: opinions and facts. Angew. Chem. Int. Ed. 32:1545-79
15. Bogan AA, Thorn KS. 1998. Anatomy of hot spots in protein interfaces. J. Mol. Biol. 280:1-9
16. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG. 1995. Funnels, pathways, and the energy landscape of protein-folding: a synthesis. Proteins Struct. Fund. Genet. 21:167-95
17. Bryngelson JD, Wolynes PG. 1987. Spin glasses and the statistical mechanics of protein folding. Proc. Natl. Acad. Sci. USA 84:7524-28
18. Caflisch A, Karplus M. 1999. Structural details of urea binding to barnase: a molecular dynamics analysis. Struct. Fold. Des. 7:477-88
19. Calladine CR, Drew HR, Luisi BF, Travers AA. 2004. Understanding DNA: The Molecule and How It Works. Amsterdam: Elsevier
20. Chan HS, Shimizu S, Kaya H. 2004. Cooperativity principles in protein folding. Methods Enzymol. 380:350-79
21. Chandler D. 2005. Interfaces and the driving force of hydrophobic assembly. Nature 473:640-47
22. Chavez LL, Onuchic JN, Clementi C. 2004. Quantifying the roughness on the free energy landscape: entropic bottlenecks and protein folding rates. J. Am. Chem. Soc. 126:8426-32
23. Cheng YK, Rossky PJ. 1998. Surface topography dependence of biomolecular hydrophobic hydration. Nature 392:696-99
24. Cheung MS, Garcia AE, Onuchic JN. 2002. Protein folding mediated by solvation: Water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc. Natl. Acad. Sci. USA 99:685-90
25. Chiu TK, Kubelka J, Herbst-Irmer R, Eaton WA, Hofrichter J, Davies DR. 2005. High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein. Proc. Natl. Acad. Sci. USA 102:7517-22
26. Chong LT, Snow CD, Rhee YM, Pande VS. 2005. Dimerization of the p53 oligomerization domain: identification of a folding nucleus by molecular dynamics simulations. J. Mol. Biol. 345:869-78
27. Clementi C, Jennings PA, Onuchic JN. 2000. How native-state topology affects the folding of dihydrofolate reductase and interleukin-lbeta. Proc. Natl. Acad. Sci. USA 97:5871-76
28. Clementi C, Nymeyer H, Onuchic JN. 2000. Toplogical and energetical factors: What determines the structural details of the transition state ensemble and "en-route" intermediate for protein folding? An investigation of small globular proteins. J. Mol. Biol. 298:937-53
29. Covalt JC, Roy M, Jennings PA. 2001. Core and surface mutations affect folding kinetics, stability and cooperativity in IL-1 beta: Does alteration in buried water play a role? J. Mol. Biol. 307:657-69
30. Crowe JH, Hoekstra FA, Crowe LM. 1992. Anhydrobiosis. Annu. Rev. Physiol. 54:579-99
31. Damjanovic A, Garcia-Moreno B, Lattman EE, Garcia AE. 2005. Molecular dynamics study of hydration of the protein interior. Comput. Phys. Commun. 169:126-29
32. Davenas E, Beauvais F, Amara J, Oberbaum M, Robinzon B, et al. 1988. Human basophil de-granulation triggered by very dilute antiserum against Ige. Nature 333:816-18
33. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ. 2002. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Angstrom resolution. J. Mol. Biol. 319:1097-113
34. De Simone A, Dodson GG, Verma CS, Zagari A, Fraternali F. 2005. Prion and water: Tight and dynamical hydration sites have a key role in structural stability. Proc. Natl. Acad. Sci. USA 102:7535-40
35. Denisov VP, Halle B. 1995. Protein hydration dynamics on aqueous solution: a comparison of bovine pancreatic trypsin inhibitor and ubiquitin by oxygen-17 spin relaxation dispersion. J. Mol. Biol. 245:682-97
36. Denisov VP, Jonsson BH, Halle B. 1999. Hydration of denatured and molten globule proteins. Nat. Struct. Biol. 6:253-60
37. Dill KA. 1990. Dominant forces in protein folding. Biochemistry 29:7133-41
38. Dill KA, Truskett TM, Vlachy V, Hribar-Lee B. 2005. Modeling water, the hydrophobic effect, and ion solvation. Annu. Rev. Biophys. Biomol. Struct. 34:173-99
39. Dunn RV, Daniel RM. 2004. The use of gas-phase substrates to study enzyme catalysis at low hydration. Philos. Trans. R. Soc. London Ser. B Biol. Sci. 359:1309-20
40. Egli M, Portmann S, Usman N. 1996. RNA hydration: a detailed look. Biochemistry 35:8489-94
41. Eisenberg D, McLachlan AD. 1986. Solvation energy in protein folding and binding. Nature 319:199-203
42. Eisenstein M, Shakked Z. 1995. Hydration patterns and intermolecular interactions in A-DNA crystal structures. Implications for DNA recognition. J. Mol. Biol. 248:662-78
43. Ejtehadi MR, Avall SP, Plotkin SS. 2004. Three-body interactions improve the prediction of rate and mechanism in protein folding models. Proc. Natl. Acad. Sci. USA 101:15088-93
44. Elcock AH, McCammon JA. 1995. Sequence-dependent hydration of DNA: theoretical results. J. Am. Chem. Soc. 117:10161-62
45. Ernst JA, Clubb RT, Zhou H-X, Gronenborn AM, Clore GM. 1995. Demonstration of positionally disordered water within a protein hydrophobic cavity by NMR. Science 267:1813-17
46. Falconi M, Brunelli M, Pesce A, Ferrario M, Bolognesi M, Desideri A. 2003. Static and dynamic water molecules in Cu,Zn superoxide dismutase. Proteins Struct. Funct. Genet. 51:607-15
47. Feig M, Brooks CL. 2004. Recent advances in the development and application of implicit solvent models in biomolecule simulations. Curr. Opin. Struct. Biol. 14:217-24
48. Fenimore PW, Frauenfelder H, McMahon BH, Parak FG. 2002. Slaving: Solvent fluctuations dominate protein dynamics and functions. Proc. Natl. Acad. Sci. USA 99:16047-51
49. Fernandez A, Scheraga HA. 2003. Insufficiently dehydrated hydrogen bonds as determinants of protein interactions. Proc. Natl. Acad. Sci. USA 100:113-18
50. Fernandez-Escamilla AM, Cheung MS, Vega MC, Wilmanns M, Onuchic JN, Serrano L. 2004. Solvation in protein folding analysis, combination of theoretical and experimental approches. Proc. Natl. Acad. Sci. USA 101:2834-39
51. Ferreiro DU, Cho SS, Komives EA, Wolynes PG. 2005. The energy landscape of modular repeat proteins: Topology determines folding mechanism in the ankyrin family. J. Mol. Biol. 354:679-92
52. Ferreiro DU, de Prat-Gay G. 2003. A protein-DNA binding mechanism proceeds through multi-state or two-state parallel pathways. J. Mol. Biol. 331:89-99
53. Ferreiro DU, Dellarole M, Nadra AD, de Prat-Gay G. 2005. Free energy contributions to direct readout of a DNA sequence. J. Biol. Chem. 280:32480-84
54. Finney JL. 1996. Hydration processes in biological and macromolecular systems. Faraday Discuss. (103):1-18
55. Frank H, Franks F. 1968. Structural approach to solvent power of water for hydrocarbons: urea as a structure breaker. J. Chem. Phys. 48:4746-57
56. Garcia AE, Hummer G. 2000. Water penetration and escape in proteins. Proteins Struct. Funct. Genet. 38:261-72
57. Garcia AE, Onuchic JN. 2003. Folding a protein in a computer: anatomic description of the folding/unfolding of protein A. Proc. Natl. Acad. Sci. USA 24:13898-903
58. Goldstein RA, Luthey-Schulten ZA, Wolynes PG. 1992. Protein tertiary structure recognition using optimized Hamiltonians with local interactions. Proc. Natl. Acad. Sci. USA 89:9029-33
59. Guo WH, Lampoudi S, Shea JE. 2003. Posttransition state desolvation of the hydrophobic core of the src-SH3 protein domain. Biophys. J. 85:61-69
60. Halle B. 2004. Biomolecular cryocrystallography: structural changes during flash-cooling. Proc. Natl. Acad. Sci. USA 101:4793-98
61. Hamada D, Dobson CM. 2002. A kinetic study of beta-lactoglobulin amyloid fibril formation promoted by urea. Protein Sci. 11:2417-26
62. Harano Y, Kinoshita M. 2004. Large gain in translational entropy of water is a major driving force in protein folding. Chem. Phys. Lett. 399:342-48
63. Henchman RH, McCammon JA. 2002. Structural and dynamic properties of water around acetylcholinesterase. Protein Sci. 11:2080-90
64. Hillson N, Onuchic JN, Garcia AE. 1999. Pressure-induced protein-folding/unfolding kinetics. Proc. Natl. Acad. Sci. USA 96:14848-53
65. Hirst S, Phillips DI, Vines SK, Clark PM, Hales CN. 1993. Reproducibility of the short insulin tolerance test. Diabet. Med. 10:839-42
66. Huang Q, Ding SW, Hua CY, Yang HC, Chen CL. 2004. A computer simulation study of water drying at the interface of protein chains. J. Chem. Phys. 121:1969-77
67. Huang X, Margulis CJ, Berne BJ. 2003. Dewetting-induced collapse of hydrophobic particles. Proc. Natl. Acad. Sci. USA 100:11953-58
68. Hummer G, Garde S, Garcia AE, Pratt LR. 2000. New perspectives on hydrophobic effects. Chem. Phys. 258:349-70
69. Janin J. 1999. Wet and dry interfaces: the role of solvent in protein-protein and protein-DNA recognition. Structure 7:R277-79
70. Jayaram B, Jain T. 2004. The role of water in protein-DNA recognition. Annu. Rev. Biophys. Biomol. Struct. 33:343-61
71. Jen-Jacobson L, Engler LE, Jacobson LA. 2000. Structural and thermodynamic strategies for site-specific DNA binding proteins. Structure 8:1015-23
72. Jones S, Thornton JM. 1996. Principles of protein-protein interactions. Proc. Natl. Acad. Sci. USA 93:13-20
73. Karanicolas J, Brooks CL. 2003. The structural basis for biphasic kinetics in the folding of the WW domain from a formin-binding protein: lessons for protein design? Proc. Natl. Acad. Sci. USA 100:3954-59
74. Kauzmann W. 1959. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 14:1-59
75. Kaya H, Chan HS. 2003. Solvation effects and driving forces for protein thermodynamics and kinetics cooperativity: How adequate is native-centric topological modeling? J. Mol. Biol. 326:911-31
76. Kaya H, Liu ZR, Chan HS. 2005. Chevron behavior and isostable enthalpic barriers in protein folding: successes and limitations of simple Go-like modeling. Biophys. J. 89:520-35
77. Khmelnitsky YL, Welch SH, Clark DS, Dordick JS. 1994. Salts dramatically enhance activity of enzymes suspended in organic solvents. J. Am. Chem. Soc. 116:2647-48
78. Klibanov AM. 2001. Improving enzymes by using them in organic solvents. Nature 409:241-46
79. Klimov DK, Straub JE, Thirumalai D. 2004. Aqueous urea solution destabilizes A-beta(16-22) oligomers. Proc. Natl. Acad. Sci. USA 101:14760-65
80. Koga N, Takada S. 2001. Roles of native topology and chain-length scaling in protein folding: a simulation study with a Go-like model. J. Mol. Biol. 313:171-80
81. Kovacs IA, Szalay MS, Csermely P. 2005. Water and molecular chaperones act as weak links of protein folding networks: Energy landscape and punctuated equilibrium changes point towards a game theory of proteins. FEBS Lett. 579:2254-60
82. Kuharski RA, Rossky PJ. 1984. Solvation of hydrophobic species in aqueous urea solution: a molecular dynamics study. J. Am. Chem. Soc. 106:5794-800
83. Ladbury JE. 1996. Just add water! The effect of water on the specificity of protein-ligand binding sites and its potential application to drug design. Chem. Biol. 3:973-80
84. Lazaridis T, Karplus M. 1999. Effective energy function for protein in solution. Proteins Struct. Funct. Genet. 35:133-52
85. Lee MY, Dordick JS. 2002. Enzyme activation for nonaqueous media. Curr. Opin. Biotechnol. 13:376-84
86. Leopold PE, Montal M, Onuchic JN. 1992. Protein folding funnels: a kinetic approach to the sequence-structure relationship. Proc. Natl. Acad. Sci. USA 89:8721-25
87. Levitt M, Park BH. 1993. Water: Now you see it, now you don't. Structure 1:223-26
88. Levy Y, Caflisch A, Onuchic JN, Wolynes PG. 2004. The folding and dimerization of HIV-1 protease: evidence for a stable monomer from simulations. J. Mol. Biol. 340:67-79
89. Levy Y, Cho SS, Onuchic JN, Wolynes PG. 2005. A survey of flexible protein binding mechanisms and their transition states using native topology based energy landscapes. J. Mol. Biol. 346:1121-45
90. Levy Y, Jortner J, Becker OM. 2001. Solvent effects on the energy landscapes and folding kinetics of polyalanine. Proc. Natl. Acad. Sci. USA 98:2188-93
91. Levy Y, Onuchic JN. 2004. Water and proteins: a love-hate relationship. Proc. Natl. Acad. Sci. USA 101:3325-26
92. Levy Y, Onuchic JN. 2006. Mechanism of protein assembly: lessons from minimalist models. Acc. Chem. Res. 39:135-42
93. Levy Y, Papoian GA, Onuchic JN, Wolynes PG. 2004. Energy landscape analysis of protein dimers. Isr. J. Chem. 44:281-97
94. Levy Y, Wolynes PG, Onuchic JN. 2004. Protein topology determines binding mechanism. Proc. Natl. Acad. Sci. USA 101:511-16
95. Liu P, Huang X, Zhou R, Berne BJ. 2005. Observation of a dewetting transition in the collapse of the melittin tetramer. Nature 437:159-62
96. Liu ZR, Chan HS. 2005. Desolvation is a likely origin of robust enthalpic barriers to protein folding. J. Mol. Biol. 349:872-89
97. Lum K, Chandler D, Weeks JD. 1999. Hydrophobicity at small and large length scales. J. Chem. Phys. B 103:4570-77
98. Makarov V, Pettitt BM, Feig M. 2002. Solvation and hydration of proteins and nucleic acids: a theoretical view of simulation and experiment. Acc. Chem. Res. 35:376-84
99. Mattos C. 2002. Protein-water interactions in a dynamic world. Trends Biochem. Sci. 27:203-8
100. Meyer E. 1992. Internal water molecules and H-bonding in biological macromolecules: a review of structural features with functional implications. Protein Sci. 1:1543-62
101. Moglich A, Krieger F, Kiefhaber T. 2005. Molecular basis for the effect of urea and guanidinium chloride on the dynamics of unfolded polypeptide chains. J. Mol. Biol. 345:153-62
102. Nymeyer H, Garcia AE. 2003. Simulation of the folding equilibrium of alpha-helical peptides: a comparison of the generalized Born approximation with explicit solvent. Proc. Natl. Acad. Sci. USA 100:13934-39
103. Olano LR, Rick SW. 2004. Hydration free energies and entropies for water in protein interiors. J. Am. Chem. Soc. 126:7991-8000
104. Oleinikova A, Smolin N, Brovchenko I, Geiger A, Winter R. 2005. Formation of spanning water networks on protein surfaces via 2 D percolation transition. J. Phys. Chem. B 109:1988-98
105. Onuchic JN, Luthey-Schulten Z, Wolynes PG. 1997. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48:545-600
106. Onuchic JN, Wolynes PG. 2004. Theory of protein folding. Curr. Opin. Struct. Biol. 14:70-75
107. Otting G, Liepinsh E, Wuthrich K. 1991. Protein hydration in aqueous solution. Science 254:974-80
108. Pace CN. 1986. Determination and analysis of urea and guanidine hydrochloride denatration curves. Methods Enzymol. 131:266-80
109. Pal SK, Peon J, Zewail AH. 2002. Biological water at the protein surface: dynamical solvation probed directly with femtosecond resolution. Proc. Natl. Acad. Sci. USA 99:1763-68
110. Pal SK, Zewail AH. 2004. Dynamics of water in biological recognition. Chem. Rev. 104:2099-123
111. Papoian GA, Ulander J, Eastwood ME, Wolynes PG. 2004. Water in protein structure prediction. Proc. Natl. Acad. Sci. USA 101:3352-57
112. Papoian GA, Ulander J, Wolynes PG. 2003. Role of water mediated interactions in protein-protein recognition landscapes. J. Am. Chem. Soc. 125:9170-78
113. Park S, Saven JG. 2005. Statistical and molecular dynamics studies of buried waters in globular proteins. Proteins Struct. Funct. Bioinform. 60:450-63
114. Pertsemlidis A, Soper AK, Sorenson JM, Head-Gordon T. 1999. Evidence for microscopic, long-range hydration forces for a hydrophobic amino acid. Proc. Natl. Acad. Sci. USA 96:481-86
115. Petrone PM, Garcia AE. 2004. MHC-peptide binding is assisted by bound water molecules. J. Mol. Biol. 338:419-35
116. Pratt LR, Pohorille A. 2002. Hydrophobic effects and modeling of biophysical aqueous solution interfaces. Chem. Rev. 102:2671-91
117. Rank JA, Baker D. 1997. A desolvation barrier to hydrophobic cluster formation may contribute to the rate-limiting step in protein folding. Protein Sci. 6:347-54
118. Rarey M, Kramer B, Lengauer T. 1999. The particle concept: placing discrete water molecules during protein-ligand docking predictions. Proteins Struct. Funct. Genet. 34:17-28
119. Rhee YM, Sorin EJ, Jayachandran G, Lindahl E, Pande VS. 2004. Simulations of the role of water in the protein-folding mechanism. Proc. Natl. Acad. Sci. USA 101:6456-61
120. Robinson CR, Sligar SG. 1993. Molecular recognition mediated by bound water. A mechanism for star activity of the restriction endonuclease EcoRI. J. Mol. Biol. 234:302-6
121. Rodier F, Bahadur RP, Chakrabarti P, Janin J. 2005. Hydration of protein-protein interfaces. Proteins Struct. Funct. Bioinform. 60:36-45
122. Roux B, Simonson T. 1999. Implicit solvent models. Biophys. Chem. 78:1-20
123. Russo D, Hura G, Head-Gordon T. 2004. Hydration dynamics near a model protein surface. Biophys. J. 86:1852-62
124. Sastry GM, Agmon N. 1997. Trehalose prevents myoglobin collapse and preserves its internal mobility. Biochemistry 36:7097-108
125. Savage H, Wlodawer E. 1986. Determination of water-structure around bimolecules using X-ray and neutron-diffraction methods. Methods Enzymol. 127:162-83
126. Schreiber G. 2002. Kinetic studies of protein-protein interactions. Curr. Opin. Struct. Biol. 12:41-47
127. Schwabe JWR. 1997. The role of water in protein DNA interactions. Curr. Opin. Struct. Biol. 7:126-34
128. Sessions RB, Thomas GL, Parker MJ. 2004. Water as a conformational editor in protein folding. J. Mol. Biol. 343:1125-33
129. Shakked Z, Guzikevichguerstein G, Frolow F, Rabinovich D, Joachimiak A, Sigler PB. 1994. Determinants of repressor-operator recognition from the structure of the Trp operator binding site. Nature 368:469-73
130. Sharp KA, Nicholls A, Fine RF, Honig B. 1991. Reconciling the magnitude of the microscopic and macroscopic hydrophobic effects. Science 252:106-9
131. Shea JE, Onuchic JN, Brooks CL. 1999. Exploring the origins of topological frustration: design of a minimally frustrated model of fragment B of protein A. Proc. Natl. Acad. Sci. USA 96:12512-17
132. Shea J-E, Onuchic JN, Brooks CL. 2002. Probing the folding free energy landscape of the src-SH3 protein domain. Proc. Natl. Acad. Sci. USA 25:16064-68
133. Sheinerman FB, Brooks CL 3rd. 1998. Calculations on folding of segment B1 of Streptococcal protein G. J. Mol. Biol. 278:439-56
134. Shoemaker BA, Portman JJ, Wolynes PG. 2000. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. USA 97:8868-73
135. Shortle D. 1999. Protein folding as seen from water's perspective. Nat. Struct. Biol. 6:203-5
136. Sleigh SH, Seavers PR, Wilkinson AJ, Ladbury JE, Tame JRH. 1999. Crystallographic and calorimetric analysis of peptide binding to OppA protein. J. Mol. Biol. 291:393-415
137. Sorenson JM, Head-Gordon T. 1998. The importance of hydration for the kinetics and thermodynamics of protein folding: simplified lattice models. Fold Des. 3:523-34
138. Sorenson JM, Hura G, Soper AK, Pertsemlidis A, Head-Gordon T. 1999. Determining the role of hydration forces in protein folding. J. Phys. Chem. B 103:5413-26
139. Sorin EJ, Nakatani BJ, Rhee YM, Jayachandran G, Vishal V, Pande VS. 2004. Does native state topology determine the RNA folding mechanism? J. Mol. Biol. 337:789-97
140. Sreenivasan U, Axelsen PH. 1992. Buried water in homologous serine proteases. Biochemistry 31:12785-91
141. Tanford C. 1970. Protein denaturation. Part C. Theoretical models for the mechanism of denaturation. Adv. Protein Chem. 24:1-95
142. Tarek M, Tobias DJ. 2002. Role of protein-water hydrogen bond dynamics in the protein dynamical transition. Phys. Rev. Lett. 88:138101
143. Timasheff S. 1998. Control of protein stability and reactions by weakly interacting cosolvents: the simplicity of the complicated. Adv. Protein Chem. 51:355-432
144. Tobi D, Elber R, Thirumalai D. 2003. The dominant interaction between peptide and urea is electrostatic in nature: a molecular dynamics simulation study. Biopolymers 68:359-69
145. Wang AJ, Bolen DW. 1997. A naturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 36:9101-8
146. Woda J, Schneider B, Patel K, MistryK, Berman HM. 1998. An analysis of the relationship between hydration and protein-DNA interactions. Biophys. J. 75:2170-77
147. Xu D, Tsai C-J, Nussinov R. 1997. Hydrogen bonds and salt bridges across protein-protein interfaces. Protein Eng. 10:999-1012
148. Zhou RH, Berne BJ. 2002. Can a continuum solvent model reproduce the free energy landscape of a beta-hairpin folding in water? Proc. Natl. Acad. Sci. USA 99:12777-82
149. Zhou RH, Huang XH, Margulis CJ, Berne BJ. 2004. Hydrophobic collapse in multidomain protein folding. Science 305:1605-9
150. Zou Q, Bennion BJ, Daggett V, Murphy KP. 2002. The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea. J. Am. Chem. Soc. 124:1192-202