Solvation effects and driving forces for protein thermodynamic and kinetic cooperativity: How adequate is native-centric topological modeling?

Journal of Molecular Biology

Volumn 326, Issue 3, 2003, Pages 911-931

  Kaya, Hüseyin ^a   Chan, Hue Sun ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Calorimetric cooperativity; Chevron plot; Desolvation barrier; Single exponential kinetics; Unfolding

Indexed keywords

PROTEIN; WATER;

ARTICLE; CALORIMETRY; KINETICS; PRIORITY JOURNAL; PROTEIN INTERACTION; SOLVATION; THERMODYNAMICS;

EID: 0037459035     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01434-1     Document Type: Article

References (131)

1. Baker D. A surprising simplicity to protein folding. Nature. 405:2000;39-42.
2. Bilsel O., Matthews C.R. Barriers in protein folding reactions. Advan. Protein Chem. 53:2000;153-207.
3. Eaton W.A., Muñoz V., Hagen S.J., Jas G.S., Lapidus L.J., Henry E.R., Hofrichter J. Fast kinetics and mechanisms in protein folding. Annu. Rev. Biophys. Biomol. Struct. 29:2000;321-359.
4. Fersht A.R. Transition-state structure as a unifying basis in protein-folding mechanisms: contact order, chain topology, stability, and the extended nucleus mechanism. Proc. Natl Acad. Sci. USA. 97:2000;1525-1529.
5. Plaxco K.W., Simons K.T., Baker D. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277:1998;985-994.
6. Chan H.S. Matching speed and locality. Nature. 392:1998;761-763.
7. Plaxco K.W., Simons K.T., Ruczinski I., Baker D. Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics. Biochemistry. 39:2000;11177-11183.
8. Duan Y., Kollman P.A. Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. Science. 282:1998;740-744.
9. Daggett V. Molecular dynamics simulations of the protein unfolding/folding reaction. Acc. Chem. Res. 35:2002;422-429.
10. Sanbonmatsu K.Y., García A.E. Structure of Met-enkephalin in explicit aqueous solution using replica exchange molecular dynamics. Proteins: Struct. Funct. Genet. 46:2002;225-234.
11. Levitt M., Warshel A. Computer simulation of protein folding. Nature. 253:1975;694-698.
12. Taketomi H., Ueda Y., Gō N. Studies on protein folding, unfolding and fluctuations by computer simulation. 1. The effect of specific amino acid sequence represented by specific inter-unit interactions. Int. J. Pept. Protein Res. 7:1975;445-459.
13. Hagler A.T., Honig B. On the formation of protein tertiary structure on a computer. Proc. Natl Acad. Sci. USA. 75:1978;554-558.
14. Godzik A., Kolinski A., Skolnick J. Lattice representations of globular proteins: how good are they? J. Comp. Chem. 14:1993;1194-1202.
15. Bryngelson J.D., Onuchic J.N., Socci N.D., Wolynes P.G. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins: Struct. Funct. Genet. 21:1995;167-195.
16. Dill K.A., Bromberg S., Yue K., Fiebig K.M., Yee D.P., Thomas P.D., Chan H.S. Principles of protein folding - a perspective from simple exact models. Protein Sci. 4:1995;561-602.
17. Thirumalai D., Woodson S.A. Kinetics of folding of proteins and RNA. Acc. Chem. Res. 29:1996;433-439.
18. Chan H.S., Kaya H., Shimizu S. Computational methods for protein folding: scaling a hierarchy of complexities. Jiang T., Xu Y., Zhang M.Q. Current Topics in Computational Molecular Biology. 2002;403-447 The MIT Press, Cambridge, MA.
19. Mirny L., Shakhnovich E. Protein folding theory: from lattice to all-atom models. Annu. Rev. Biophys. Biomol. Struct. 30:2001;361-396.
20. Thirumalai D., Klimov D.K. Deciphering the timescales and mechanisms of protein folding using minimal off-lattice models. Curr. Opin. Struct. Biol. 9:1999;197-207.
21. Onuchic J.N., Nymeyer H., García A.E., Chahine J., Socci N.D. The energy landscape theory of protein folding: insights into folding mechanisms and scenarios. Advan. Protein Chem. 53:2000;87-152.
22. Burton R.E., Myers J.K., Oas T.G. Protein folding dynamics: quantitative comparison between theory and experiment. Biochemistry. 37:1998;5337-5343.
23. Alm E., Baker D. Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures. Proc. Natl Acad. Sci. USA. 96:1999;11305-11310.
24. Debe D.A., Goddard W.A. First principles prediction of protein folding rates. J. Mol. Biol. 294:1999;619-625.
25. Muñoz V., Eaton W.A. A simple model for calculating the kinetics of protein folding from three-dimensional structures. Proc. Natl Acad. Sci. USA. 96:1999;11311-11316.
26. Galzitskaya O.V., Finkelstein A.V. A theoretical search for folding/unfolding nuclei in three-dimensional protein structures. Proc. Natl Acad. Sci. USA. 96:1999;11299-11304.
27. Micheletti C., Banavar J.R., Maritan A., Seno F. Protein structures and optimal folding from a geometrical variational principle. Phys. Rev. Letters. 82:1999;3372-3375.
28. Shea J.-E., Onuchic J.N., Brooks C.L. III. Exploring the origins of topological frustration: design of a minimally frustrated model of fragment B of protein A. Proc. Natl Acad. Sci. USA. 96:1999;12512-12517.
29. Takada S. Gō-ing for the prediction of protein folding mechanisms. Proc. Natl Acad. Sci. USA. 96:1999;11698-11700.
30. Zhou Y., Karplus M. Interpreting the folding kinetics of helical proteins. Nature. 401:1999;400-403.
31. Clementi C., Jennings P.A., Onuchic J.N. How native-state topology affects the folding of dihydrofolate reductase and interleukin-1β Proc. Natl Acad. Sci. USA. 97:2000;5871-5876.
32. Clementi C., Nymeyer H., Onuchic J.N. Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol. 298:2000;937-953.
33. Banavar J.R., Maritan A. Computational approach to the protein-folding problem. Proteins: Struct. Funct. Genet. 42:2001;433-435.
34. Cieplak M., Hoang T.X. Kinetic nonoptimality and vibrational stability of proteins. Proteins: Struct. Funct. Genet. 44:2001;20-25.
35. Koga N., Takada S. Roles of native topology and chain-length scaling in protein folding: a simulation study with a Gō-like model. J. Mol. Biol. 313:2001;171-180.
36. Li L., Shakhnovich E.I. Constructing, verifying, and dissecting the folding transition state of chymotrypsin inhibitor 2 with all-atom simulations. Proc. Natl Acad. Sci. USA. 98:2001;13014-13018.
37. Micheletti C., Banavar J.R., Maritan A. Conformations of proteins in equilibrium. Phys. Rev. Letters. 87:2001;. Art. No. 088102.
38. Portman J.J., Takada S., Wolynes P.G. Microscopic theory of protein folding rates. I. Fine structure of the free energy profile and folding routes from a variational approach. J. Chem. Phys. 114:2001;5069-5081.
39. Portman J.J., Takada S., Wolynes P.G. Microscopic theory of protein folding rates. II. Local reaction coordinates and chain dynamics. J. Chem. Phys. 114:2001;5082-5096.
40. Cheung M.S., García A.E., Onuchic J.N. Protein folding mediated by solvation: water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc. Natl Acad. Sci. USA. 99:2002;685-690.
41. Jang H., Hall C.K., Zhou Y. Folding thermodynamics of model four-strand antiparallel β-sheet proteins. Biophys. J. 82:2002;646-659.
42. Klimov D.K., Thirumalai D. Stiffness of the distal loop restricts the structural heterogeneity of the transition state ensemble in SH3 domains. J. Mol. Biol. 317:2002;721-737.
43. Makarov D.E., Keller C.A., Plaxco K.W., Metiu H. How the folding rate constant of simple, single-domain proteins depends on the number of native contacts. Proc. Natl Acad. Sci. USA. 99:2002;3535-3539.
44. Micheletti C., Lattanzi G., Maritan A. Elastic properties of proteins: insight on the folding process and evolutionary selection of native structures. J. Mol. Biol. 321:2002;909-921.
45. Zhou Y., Linhananta A. Thermodynamics of an all-atom off-lattice model of the fragment B of Staphylococcal protein A: implication for the origin of the cooperativity of protein folding. J. Phys. Chem. B. 106:2002;1481-1485.
46. Linhananta A., Zhou Y. The role of sidechain packing and native contact interactions in folding: discontinuous molecular dynamics folding simulations of an all-atom Gō model of fragment B of Staphylococcal protein A. J. Chem. Phys. 117:2002;8983-8995.
47. Kaya H., Chan H.S. Polymer principles of protein calorimetric two-state cooperativity. Proteins: Struct. Funct. Genet. 40:2000;637-661. Erratum: 43, 523 (2001).
48. Kaya H., Chan H.S. Energetic components of cooperative protein folding. Phys. Rev. Letters. 85:2000;4823-4826.
49. Gō N. The consistency principle revisited. Kuwajima K., Arai M. Old and New Views of Protein Folding. 1999;97-105 Elsevier, Amsterdam, The Netherlands.
50. Laughlin R.B., Pines D. The theory of everything. Proc. Natl Acad. Sci. USA. 97:2000;28-31.
51. Isin B., Doruker P., Bahar I. Functional motions of influenza virus hemagglutinin: a structure-based analytical approach. Biophys. J. 82:2002;569-581.
52. Keskin O., Bahar I., Flatow D., Covell D.G., Jernigan R.L. Molecular mechanisms of chaperonin GroEL-GroES function. Biochemistry. 41:2002;491-501.
53. Jacobs D.J., Rader A.J., Kuhn L.A., Thorpe M.F. Protein flexibility prediction using graph theory. Proteins: Struct. Funct. Genet. 44:2001;150-165.
54. Gō N. Theoretical studies of protein folding. Annu. Rev. Biophys. Bioeng. 12:1983;183-210.
55. Bryngelson J.D., Wolynes P.G. Spin glasses and the statistical mechanics of protein folding. Proc. Natl Acad. Sci. USA. 84:1987;7524-7528.
56. Panchenko A.R., Luthey-Schulten Z., Cole R., Wolynes P.G. The foldon universe: a survey of structural similarity and self-recognition of independently folding units. J. Mol. Biol. 272:1997;95-105.
57. Lau K.F., Dill K.A. A lattice statistical mechanics model of the conformational and sequence spaces of proteins. Macromolecules. 22:1989;3986-3997.
58. Chan H.S., Dill K.A. Sequence space soup of proteins and copolymers. J. Chem. Phys. 95:1991;3775-3787.
59. Shakhnovich E., Farztdinov G., Gutin A.M., Karplus M. Protein folding bottlenecks - a lattice Monte-Carlo simulation. Phys. Rev. Letters. 67:1991;1665-1668.
60. Leopold P.E., Montal M., Onuchic J.N. Protein folding funnels - a kinetic approach to the sequence structure relationship. Proc. Natl Acad. Sci. USA. 89:1992;8721-8725.
61. Camacho C.J., Thirumalai D. Kinetics and thermodynamics of folding in model proteins. Proc. Natl Acad. Sci. USA. 90:1993;6369-6372.
62. Shrivastava I., Vishveshwara S., Cieplak M., Maritan A., Banavar J.R. Lattice model for rapidly folding protein-like heteropolymers. Proc. Natl Acad. Sci. USA. 92:1995;9206-9209.
63. Plotkin S.S. Speeding protein folding beyond the Gō model: How a little frustration sometimes helps. Proteins: Struct. Funct. Genet. 45:2001;337-345.
64. Paci E., Vendruscolo M., Karplus M. Native and non-native interactions along protein folding and unfolding pathways. Proteins: Struct. Funct. Genet. 47:2002;379-392.
65. McCallister E.L., Alm E., Baker D. Critical role of β-hairpin formation in protein G folding. Nature Struct. Biol. 7:2000;669-673.
66. Hillson N., Onuchic J.N., García A.E. Pressure-induced protein-folding/unfolding kinetics. Proc. Natl Acad. Sci. USA. 96:1999;14848-14853.
67. Chan H.S. Modeling protein density of states: additive hydrophobic effects are insufficient for calorimetric two-state cooperativity. Proteins: Struct. Funct. Genet. 40:2000;543-571.
68. Kaya H., Chan H.S. Towards a consistent modeling of protein thermodynamic and kinetic cooperativity: how applicable is the transition state picture to folding and unfolding? J. Mol. Biol. 315:2002;899-909.
69. Tiktopulo E.I., Bychkova V.E., Rička J., Ptitsyn O.B. Cooperativity of the coil-globule transition in a homopolymer - microcalorimetric study of poly(N-isopropylacrylamide). Macromolecules. 27:1994;2879-2882.
70. Matthews C.R. Effect of point mutations on the folding of globular proteins. Methods Enzymol. 154:1987;498-511.
71. Gillespie B., Plaxco K.W. Nonglassy kinetics in the folding of a simple single-domain protein. Proc. Natl Acad. Sci. USA. 97:2000;12014-12019.
72. Jackson S.E., Moracci M., elMasry N., Johnson C.M., Fersht A.R. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2. Biochemistry. 32:1993;11259-11269.
73. De Jong D., Riley R., Alonso D.O.V., Daggett V. Probing the energy landscape of protein folding/unfolding transition states. J. Mol. Biol. 319:2002;229-242.
74. Fersht A.R., Daggett V. Protein folding and unfolding at atomic resolution. Cell. 108:2002;573-582.
75. Sobolev V., Sorokine A., Prilusky J., Abola E.E., Edelman M. Automated analysis of interatomic contacts in proteins. Bioinformatics. 15:1999;327-332.
76. Vaiana S.M., Manno M., Emanuele A., Palma-Vittorelli M.B., Palma M.U. The role of solvent in protein folding and in aggregation. J. Biol. Phys. 27:2001;133-145.
77. Pratt L.R., Chandler D. Theory of the hydrophobic effect. J. Chem. Phys. 67:1977;3683-3704.
78. Geiger A., Rahman A., Stillinger F.H. Molecular dynamics study of the hydration of Lennard-Jones solutes. J. Chem. Phys. 70:1979;263-276.
79. Pangali C., Rao M., Berne B.J. A Monte Carlo simulation of the hydrophobic interaction. J. Chem. Phys. 71:1979;2975-2981.
80. Guo C., Cheung M.S., Levine H., Kessler D.A. Mechanisms of cooperativity underlying sequence-independent β-sheet formation. J. Chem. Phys. 116:2002;4353-4365.
81. Karanicolas J., Brooks C.L. The origins of asymmetry in the folding transition states of protein L and protein G. Protein Sci. 11:2002;2351-2361.
82. Roux B., Simonson T. Implicit solvent models. Biophys. Chem. 78:1999;1-20.
83. Shimizu S., Chan H.S. Anti-cooperativity and cooperativity in hydrophobic interactions: three-body free energy landscapes and comparison with implicit-solvent potential functions for proteins. Proteins: Struct. Funct. Genet. 48:2002;15-30. Erratum: 49, 294 (2002).
84. Shimizu S., Chan H.S. Temperature dependence of hydrophobic interactions: a mean force perspective, effects of water density, and non-additivity of thermodynamic signatures. J. Chem. Phys. 113:2000;4683-4700. Erratum: 116, 8636 (2002).
85. Shimizu S., Chan H.S. Configuration-dependent heat capacity of pairwise hydrophobic interactions. J. Am. Chem. Soc. 123:2001;2083-2084.
86. Ghosh T., García A.E., Garde S. Enthalpy and entropy contributions to the pressure dependence of hydrophobic interactions. J. Chem. Phys. 116:2002;2480-2486.
87. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., DiNola A., Haak J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:1984;3684-3690.
88. Guo Z., Thirumalai D. Kinetics of protein folding: nucleation mechanism, time scales, and pathways. Biopolymers. 36:1995;83-102.
89. Veitshans T., Klimov D., Thirumalai D. Protein folding kinetics: timescales, pathways and energy landscapes in terms of sequence-dependent properties. Fold. Des. 2:1997;1-22.
90. Allen M.P., Tildesley D.J. Computer Simulation of Liquids. 1987;Oxford University Press, Oxford, UK.
91. Swope W.C., Andersen H.C., Berens P.H., Wilson K.R. A computer simulation method for the calculation of equilibrium constants for the formation of physical clusters of molecules: application to small water clusters. J. Chem. Phys. 76:1982;637-649.
92. Fersht A.R. Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7:1997;3-9.
93. Chu R.-A., Bai Y. Lack of definable nucleation sites in the rate-limiting transition state of barnase under native conditions. J. Mol. Biol. 315:2002;759-770.
94. Yang D., Mok Y.K., Forman-Kay J.D., Farrow N.A., Kay L.E. Contributions to protein entropy and heat capacity from bond vector motions measured by NMR spin relaxation. J. Mol. Biol. 272:1997;790-804.
95. Jackson S.A., Fersht A.R. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry. 30:1991;10428-10435.
96. Cui Y., Wong W.H., Bornberg-Bauer E., Chan H.S. Recombinatoric exploration of novel folded structures: a heteropolymer-based model of protein evolutionary landscapes. Proc. Natl Acad. Sci. USA. 99:2002;809-814.
97. Chan H.S., Bornberg-Bauer E. Perspectives on protein evolution from simple exact models. Appl. Bioinformatics. 1:2002;121-144.
98. Chan H.S., Dill K.A. Protein folding in the landscape perspective: chevron plots and non-Arrhenius kinetics. Proteins: Struct. Funct. Genet. 30:1998;2-33.
99. Bakk A., Høye J.S., Hansen A., Sneppen K., Jensen M.H. Pathways in two-state protein folding. Biophys. J. 79:2000;2722-2727.
100. Uversky V.N., Fink A.L. The chicken-egg scenario of protein folding revisited. FEBS Letters. 515:2002;79-83.
101. Creamer T.P., Rose G.D. α-Helix-forming propensities in peptides and proteins. Proteins: Struct. Funct. Genet. 19:1994;85-97.
102. Chan H.S. Modelling protein folding by Monte Carlo dynamics: chevron plots, chevron rollover, and non-Arrhenius kinetics. Grassberger P., Barkema G.T., Nadler W. Monte Carlo Approach to Biopolymers and Protein Folding. 1998;29-44 World Scientific, Singapore.
103. Wallqvist A., Covell D.G., Thirumalai D. Hydrophobic interactions in aqueous urea solutions with implications for the mechanism of protein denaturation. J. Am. Chem. Soc. 120:1998;427-428.
104. Crippen G.M. A Gaussian statistical mechanical model for the equilibrium thermodynamics of barnase folding. J. Mol. Biol. 306:2001;565-573.
105. Ikeguchi M., Nakamura S., Shimizu K. Molecular dynamics study on hydrophobic effects in aqueous urea solutions. J. Am. Chem. Soc. 123:2001;677-682.
106. Shimizu S., Chan H.S. Origins of protein denatured states compactness and hydrophobic clustering in aqueous urea: inferences from nonpolar potentials of mean force. Proteins: Struct. Funct. Genet. 49:2002;560-566.
107. Englander S.W., Mayne L., Bai Y., Sosnick T.R. Hydrogen exchange: the modern legacy of Linderstrøm-Lang. Protein Sci. 6:1997;1101-1109.
108. Kim K.S., Woodward C. Protein internal flexibility and global stability: effect of urea on hydrogen-exchange rates of bovine pancreatic trypsin inhibitor. Biochemistry. 32:1993;9609-9613.
109. Bai Y., Sosnick T.R., Mayne L., Englander S.W. Protein folding intermediates: native-state hydrogen exchange. Science. 269:1995;192-197.
110. Llinás M., Gillespie B., Dahlquist F.W., Marqusee S. The energetics of T4 lysozyme reveal a hierarchy of conformations. Nature Struct. Biol. 6:1999;1072-1078.
111. Klimov D.K., Thirumalai D. Is there a unique melting temperature for two-state proteins? J. Comput. Chem. 23:2002;161-165.
112. Kuhlman B., Luisi D.L., Evans P.A., Raleigh D.P. Global analysis of the effects of temperature and denaturant on the folding and unfolding kinetics of the N-terminal domain of the protein L9. J. Mol. Biol. 284:1998;1661-1670.
113. Houry W.A., Rothwarf D.M., Scheraga H.A. The nature of the initial step in the conformational folding of disulphide-intact ribonuclease A. Nature Struct. Biol. 2:1995;495-503.
114. Oliveberg M., Tan Y.J., Fersht A.R. Negative activation enthalpies in the kinetics of protein folding. Proc. Natl Acad. Sci. USA. 92:1995;8926-8929.
115. Abkevich V.I., Gutin A.M., Shakhnovich E.I. Free energy landscape for protein folding kinetics: intermediates, traps, and multiple pathways in theory and lattice model simulations. J. Chem. Phys. 101:1994;6052-6062.
116. Nymeyer H., Socci N.D., Onuchic J.N. Landscape approaches for determining the ensemble of folding transition states: success and failure hinge on the degree of frustration. Proc. Natl Acad. Sci. USA. 97:2000;634-639.
117. Socci N.D., Onuchic J.N., Wolynes P.G. Diffusive dynamics of the reaction coordinate for protein folding funnels. J. Chem. Phys. 104:1996;5860-5868.
118. Fersht A.R., Matouschek A., Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224:1992;771-782.
119. Schuler B., Lipman E.A., Eaton W.A. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature. 419:2002;743-747.
120. Matouschek A., Kellis J.T., Serrano L., Bycroft M., Fersht A.R. Characterizing transient folding intermediates by protein engineering. Nature. 346:1990;440-445.
121. Li R., Battiste J.L., Woodward C. Native-like interactions favored in the unfolded bovine pancreatic trypsin inhibitor have different roles in folding. Biochemistry. 41:2002;2246-2253.
122. Oliveberg M. Alternative explanations for "multistate" kinetics in protein folding: transient aggregation and changing transition-state ensembles. Acc. Chem. Res. 31:1998;765-772.
123. Parker M.J., Marqusee S. The cooperativity of burst phase reactions explored. J. Mol. Biol. 293:1999;1195-1210.
124. Du R., Pande V.S., Grosberg A.Y., Tanaka T., Shakhnovich E.I. On the transition coordinate for protein folding. J. Chem. Phys. 108:1998;334-350.
125. Sabelko J., Ervin J., Gruebele M. Observation of strange kinetics in protein folding. Proc. Natl Acad. Sci. USA. 96:1999;6031-6036.
126. Eaton W.A. Searching for "downhill scenarios" in protein folding. Proc. Natl Acad. Sci. USA. 96:1999;5897-5899.
127. Lazaridis T., Karplus M. Effective energy functions for proteins in solution. Proteins: Struct. Funct. Genet. 35:1999;133-152.
128. Day R., Bennion B.J., Ham S., Daggett V. Increasing temperature accelerates protein unfolding without changing the pathway of unfolding. J. Mol. Biol. 322:2002;189-203.
129. ten Wolde P.R., Chandler D. Drying-induced hydrophobic polymer collapse. Proc. Natl Acad. Sci. USA. 99:2002;6539-6543.
130. Fan K., Wang J., Wang W. Modeling two-state cooperativity in protein folding. Phys. Rev. E. 64:2001;. Art. No. 041907.
131. Crippen G.M., Chhajer M. Lattice models of protein folding permitting disordered native states. J. Chem. Phys. 116:2002;2261-2268.