From levinthal to pathways to funnels

Nature Structural Biology

Volumn 4, Issue 1, 1997, Pages 10-19

  Dill, Ken A ^a   Chan, Hue Sun ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLOBULAR PROTEIN;

CHEMICAL REACTION KINETICS; EQUILIBRIUM CONSTANT; MOLECULAR MODEL; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; REVIEW;

KINETICS; MODELS, CHEMICAL; PROTEIN FOLDING;

EID: 1842298212     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb0197-10     Document Type: Review

References (109)

1. Baldwin, R.L. Matching speed and stability. Natute 369, 183-184 (1994).
2. Baldwin, R.L. The nature of protein folding pathways: The classical versus the new view.J Biomolec. NMR 5, 103-109(1995).
3. Anfinsen, C.B., Haber, E., Sela, M. & White, F.H. Jr. The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc. Natl. Acad. Sci. USA 47, 1309-1314(1961).
4. Anfinsen, C.B. Principles that govern the folding of protein chains. Science 181, 223-230(1973).
5. Levinthal, C. Are there pathways for protein folding? J. Chim. Phys. 65, 44-45 (1968).
6. Levinthal, C. in Mossbauer Spectroscopy in Biological Systems. Proceedings of a meeting held at Allerton house, Monticello, Illinois. (eds P. Debrunner, J. Tsibris, & E. Munck) 22-24 (University of Illinois Press, Urbana, Illinois, 1969).
7. Wetlaufer, D.B. Nucleation, rapid folding, and globular intrachain regions in proteins. Proc Natl. Acad Sci. USA 70, 697-701 (1973).
8. Dill, K.A. Theory for the folding and stability of globular proteins. Biochemistry 24, 1501-1509(1985).
9. Zwanzig, R., Szabo, A. & Bagchi, B. Levinthal's paradox. Proc. Natl. Acad. Sci. USA 89, 20-22(1992).
10. Ikai, A. & Tanford, C. Kinetic evidence for incorrectly folded intermediate states in the refolding of denatured proteins. Nature 230, 100-102(1971).
11. Tsong, T.Y., Baldwin, R.L. & Elson, E.L. The sequential unfolding of ribonucleases A: Detection of a fast initial phase in the kinetics of unfolding. Proc. Natl. Acad. Sci. USA 68,2712-2715(1971).
12. Creighton, T.E. Conformational restrictions on the pathway of folding and unfolding of the pancreatic trypsin inhibitor. J. Mol. Biol. 113, 275-293 (1977).
13. Creighton, T.E. Experimental studies of protein folding and unfolding. Prog. Biophys. Mol. Biol. 33, 231-297 (1978).
14. Weissman, J.S. & Kim, P.S. Reexamination of the folding of BPTI: Predominance of native intermediates. Science 253, 1386-1393 (1991).
15. Weissman, J.S. & Kim, P.S. Kinetic role of nonnative species in the folding of bovine pancreatic trypsin inhibitor. Proc. Natl. Acad. Sci. USA 89, 9900-9904 (1992).
16. Brandts, J.F., Halvorson, H.R. & Brennan, M. Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry 14, 4953-4963 (1975).
17. Hagerman, P.J. Kinetic analysis of the reversible folding reactions of small proteins: Application to the folding of lysozyme and cytochrome c. Biopolymers 16, 731-747 (1977).
18. Schmid, F.X. & Baldwin, R. L. Acid catalysis of the formation of the slow-folding species of RNase A: Evidence that the reaction is proline isomerization. Proc Natl. Acad. Sci. USA 75, 4764-4768 (1978).
19. Kim, P.S. & Baldwin, R.L. Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding. Ann. Rev. Biochem. 51, 459-489 (1982).
20. Kim, P.S. & Baldwin, R.L. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 59, 631-660 (1990).
21. Mann, C.J., Shao, X. & Matthews, C.R. Characterization of the slow folding reactions of trp aporepressor from Escherichia coll by mutational analysis of prolines and catalysis by a peptidyl-prolyl isomerase. Biochemistry 34, 14573-14580 (1995).
22. Englander, S.W. & Poulsen A. Hydrogen-tritium exchange of the random chain polypeptide. Biopolymers 7, 329-393 (1969).
23. Woodward, C.K. & Rosenberg, A. Studies of hydrogen exchange in proteins. Vl. Urea effects on RNase hydrogen exchange kinetics leading to a general model for hydrogen exchange from folded proteins J. Biol. Chem. 246, 4114-4121 (1971).
24. Englander, S.W., Downer, N.W., & Teitelbaum, H. Hydrogen exchange. Annu. Rev. Biochem. 41,903-924 (1972).
25. Woodward, C.K. & Hilton, B.D. Hydrogen exchange kinetics and internal motions in proteins and nucleic acids. Annu. Rev. Biophys. Bioeng. 8,99-127 (1979).
26. Bai, Y., Sosnick, T.R., Mayne, L. & Englander, S.W. Protein folding intermediates: NativeState hydrogen exchange. Science 269, 192-197 (1995).
27. Bai, Y. & Englander, S.W. Future directions in folding: The multi-state nature of protein structure. Proteins: Struct. Funct Genet. 24, 145-151 (1996).
28. Balbach, J. et al. Following protein folding in real time using NMR spectroscopy. Nature Struct. Biol. 2, 865-870 (1995).
29. Udgaonkar, J.B. & Baldwin, R-L. NMR evidence for an early framework inter mediate on the folding pathway of ribonuclease A. Nature 335, 694-699 (1988).
30. Roder, H., Elöve, G.A. & Englander, S.W. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335, 700-704 (1988).
31. Radford, S.E., Dobson, C.M. & Evans, P.A. The folding of hen lysozyme involves partially structured intermediates and multiple pathways. Nature 358, 302-307 (1992).
32. Miranker, A., Robinson, CV., Radford, SE., Aplin, R.T. & Dobson, CM. Detection of transient protein folding populations by mass spectrometry. Science 262, 896-900 (1993).
33. Radford, S.E. & Dobson, C.M. Insights into protein folding using physical techniques: Studies of lysozyme and α-lactalbumin. Phil. Trans. R. Soc. Lond. B348, 17-25 (1995).
34. Miranker, A., Robinson, C. V., Radford, S. E. & Dobson, C. M. Investigation of protein folding by mass spectrometry. Faseb J. 10,93-101 (1996).
35. Chen, B.-L, Baase, W. A. & Schellman, J. A. Low-temperature unfolding of a mutant of phage T4 lysozyme. 2. Kinetic investigations. Biochemistry 28, 691-699 (1989).
36. Matouschek, A., Kellis, J.T. Jr., Serrano, L., Bycroft, M. & Fersht, A.R. Transient folding intermediates characterized by protein engineering. Nature 346, 440-445 (1990).
37. Fersht, A.R. Characterizing transition states in protein folding: An essential step in the puzzle. Curr. Opin. Struct Biol. 5, 79-84 (1995).
38. Neira, J.L. et al. Towards the complete structural characterization of a protein folding pathway: the structures of the denatured, transition and native states for the association/folding of two complementary fragments of cleaved chymotrypsin inhibitor 2. Direct evidence for a nucleation-condensation mechanism. Folding & Design 1, 189-208 (1996).
39. Jones, C. M. et al. Fast events in protein folding initiated by nanosecond laser photolysis. Proc. Natl. Acad. Sci. USA 90,11860-11864 (1993).
40. Williams, S. et al. Fast events in protein folding: Helix melting and formation in a small peptide. Biochemistry 35, 691-697 (1996).
41. Pascher, T., Chesick, J.P., Winkler, J.R. & Gray, H.B. Protein folding triggered by electron transfer. Science 271,1558-1560 (1996).
42. Miranker, A.D. & Dobson, C.M. Collapse and cooperativity in protein folding. Curr. Opin. Struct. Biol. 6, 31-42 (1996).
43. Jackson, S.E. & Fersht, A.R. Folding of chymotrypsin inhibitor 2.1. Evidence for a two-state transition. Biochemistry 30, 10428-10435 (1991).
44. Fersht, A.R. Optimization of rates of protein folding: The nucleation-condensation mechanism and its implications. Proc. Natl. Acad. Sci. USA 92,10869-10873 (1995).
45. Sosnick, TR., Mayne, L., Miller, R. & Englander, S.W. The barriers in protein folding. Nature Struct. Biol. 1, 149-156 (1994).
46. Huang, G.S. & Oas, T.G. Submillisecond folding of monomeric λ represser. Proc Natl. Acad. Sci. USA 92, 6878-6882 (1995).
47. Schindler, T., Herrler, M., Marahiel, M.A. & Schmid. F.X. Extremely rapid protein folding in the absence of intermediates. Nature Struct. Biol. 2, 663-673 (1995).
48. Sosnick, T.R., Mayne, L. & Englander, S.W. Molecular collapse: The rate-limiting step in two-state cytochrome c folding. Proteins Struct. Funct Genet. 24, 413-426 (1996).
49. Chan, H.S. & Dill, K.A. Polymer principles in protein structure and stability. Annu. Rev. Biophys. Biophys. Chem. 20, 447-490 (1991).
50. Chan, H.S. & Dill, K.A. Comparing folding codes for proteins and polymers. Proteins: Struct. Funct. Genet. 24, 335-344 (1996).
51. 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, 167-195 (1995).
52. Wolynes, P. G., Onuchic, J. N. & Thirumalai, D. Navigating the folding routes. Science 267,1619-1620 (1995).
53. Onuchic, J.N., Wolynes, P.G., Luthey-Schulten, Z. & Socci, N.D. Towards an outline of the topography of a realistic protein folding funnel. Proc. Natl. Acad. Sci. USA 92, 3626-3630 (1995).
54. Socci, N.D., Onuchic, J.N. & Wolynes, P.G Diffusive dynamics of the reaction coordinate for protein folding funnels. J. Chem. Phys. 104, 5860-5868 (1996).
55. Dill, K. A. The stabilities of globular proteins. In Protein Engineering (eds Oxender, D. L. & Fox, C. F.) 187-192 (Alan R. Liss. Inc., New York, 1987).
56. Bryngelson, J.D. & Wolynes, P.G. Intermediates and barrier crossing in a random energy model (with applications to protein folding). J. Phys. Chem. 93, 6902-6915 (1989).
57. Shakhnovich, E.I., Farztdinov, G., Gutin, A.M. & Karplus, M. Protein folding bottlenecks: A lattice Monte Carlo simulation. Phys. Rev. Lett. 67, 1665-1668 (1991).
58. Camacho, C.J. & Thirumalai, D. Kinetics and thermodynamics of folding in model proteins. Proc. Natl. Acad. Sci. USA 90, 6369-6372 (1993).
59. Chan, H.S. & Dill, K.A. Transition states and folding dynamics of proteins and heteropolymers. J. Chem. Phys. 100, 9238-9257 (1994).
60. Socci, N.D. & Onuchic, J.N. Folding kinetics of protein-like heteropolymers. J. Chem. Phys. 101, 1519-1528 (1994).
61. 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, 6052-6062 (1994).
62. Sail, A., Shakhnovich, E. & Karplus, M. How does a protein fold? Nature 369, 248-251 (1994).
63. Dill, K.A. et al. Principles of protein folding - A perspective from simple exact models. Protein Sci. 4, 561-602 (1995).
64. Hao, M.-H. & Scheraga, H.A. Statistical thermodynamics of protein folding: Sequence dependence. J. Phys. Chem. 98, 9882-9893 (1994).
65. Hao, M.-H. & Scheraga, H.A. How optimization of potential functions affects protein folding. Proc. Natl. Acad. Sci. USA 93, 4984-4989 (1996).
66. Bryngelson, J.D. & Wolynes, P.G. Spin-glass and the statistical mechanics of protein folding. Proc. Natl. Acad. Sci. USA 84, 7524-7528 (1987),
67. Leopold, P.E., Montai, M. & Onuchic, J.N. Protein folding funnels: A kinetic approach to the sequence-structure relationship. Proc. Natl. Acad. Sci. USA 89, 8721-8725 (1992).
68. Guo, Z. & Thirumalai, D. Kinetics of protein folding: Nucleation mechanism, time scales, and pathways. Biopolymers 36, 83-102 (1995).
69. Socci, N.D. & Onuchic, J.N. Kinetic and thermodynamic analysis of proteinlike heteropolymers: Monte Carlo histogram technique. J. Chem. Phys. 103, 4732-4744 (1995).
70. Thirumalai, D. From minimal models to real proteins: Time scales for protein folding kinetics.J.Phys.15, 1457-1467 (1995).
71. Mirny, L.A., Abkevich, V. & Shakhnovich, E.I. Universality and diversity of the protein folding scenarios: A comprehensive analysis with the aid of a lattice model. Folding & Design 1,103-116 (1996).
72. Thirumalai, D. & Woodson, S.A. Kinetics of folding of proteins and RNA. Acc. Chem. Res. 29,433-439 (1996).
73. Chan, H.S. & Dill, K.A. Protein folding kinetics from the perspectives of simple models. Proteins: Struct. Funct. Genet. in the press.
74. Chan, H.S. & Dill, K.A. Energy landscapes and the collapse dynamics of homopolymers. J. Chem. Phys. 99,2116-2127 (1993).
75. Kuroda, Y., Hamada, D., Tanaka, T. & Goto, Y. High helicity of peptide fragments corresponding to β-strand regions of β-lactoglobulin observed by 2D-NMR spectroscopy. Folding & Design 1, 243-251 (1996).
76. Hamada, D., Segawa, S.-I. & Goto, Y. Non-native α-helical intermediate in the refolding of β-lactoglobulin, a predominantly β-sheet protein. Nature Struct. Biol. 3, 868-873(1996).
77. Landry, S.J. & Gierasch, L.M. Polypeptide interactions with molecular chaperones and their relationship to in vivo protein folding. Annu. Rev. Biophys. Biomol. Struct. 23, 645-669 (1994).
78. Hlodan, R. & Hartl, F.U. in Mechanisms of Protein Folding (ed. R.H. Pain) 194-228 (Oxford University Press, New York, 1994).
79. Thirumalai, D. in Statistical Mechanics, Protein Structure, and Protein-Substrate Interactions (ed. S. Doniach) 115-134 (Plenum, New York, 1994).
80. Chan, H.S. & Dill, K.A. A simple model of chaperonin-mediated protein folding. Proteins: Struct. Funct. Genet. 24, 345-351 (1996).
81. Todd, M.J., Lorimer, G.H. & Thirumalai, D. Chaperonin-facilitated protein folding: Optimization of rate and yield by an iterative annealing mechanism. Proc. Natl. Acad. Sci. USA 93, 4030-4035 (1996).
82. Sfatos, C.D., Gutin, A.M., Abkevich, V.I. & Shakhnovich, E.I. Simulations of chaperoneassisted folding. Biochemistry 35, 334-339 (1996).
83. Gutin, A.M., Abkevich, V, I. & Shakhnovich, E.I. Is burst hydrophobic collapse necessary for protein folding? Biochemistry 34, 3066-3076 (1995).
84. 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, 9206-9209 (1995).
85. Klimov, D.K. & Thirumalai, D. A criterion that determines the foldability of proteins. Phys. Rev. Lett. 76, 4070-4073 (1996).
86. Klimov, D.K. & Thirumalai, D. Factors governing the foldability of proteins. Proteins: Struct. Funct. Genet. In the press.
87. Hill, T.L. Effect of rotation on the diffusion-controlled rate of ligand-protein association. Proc. Natl. Acad. Sci. USA 72,4918-4922 (1975).
88. Hill, T. L. Diffusion frequency factors in some simple examples of transition-state rate theory. Proc. Natl. Acad. Sci. USA 73, 679-683 (1976).
89. Steinfeld, J.I., Francisco, J.S. & Hase, W.L. Chemical Kinetics and Dynamics (Prentice-Hall, Englewood Cliffs, New Jersey, 1989).
90. Zhou, H.-X. & Zwanzig, R. A rate process with an entropy barrier. J. Chem. Phys. 94, 6147-6152 (1991).
91. Tanford, C. Protein denaturation. Adv. Protein Chem. 23, 121-282 (1968).
92. Matthews, C.R., Crisanti, M.M., Manz, J.T. & Gepner, G.L. Effects of a single amino acid substitution on the folding of the α-subunit of tryptophan synthase. Biochemistry 22, 1445-1452 (1983).
93. Segawa, S.-I. & Sugihara, M. Characterization of the transition state of lysozyme unfolding. I. Effect of protein-solvent interactions on the transition state. Biopolymers 23, 2473-2488 (1984).
94. Chen, B.-L., Baase, W.A., Nicholson, H. & Schellman, J.A. Folding kinetics of T4 lysozyme and nine mutants at 12 °C. Biochemistry 31,1464-1476 (1992).
95. Shortle, D., Chan, H.S. & Dill, K.A. Modeling the effects of mutations on the denatured states of proteins. Protein Sci. 1, 201-215 (1992).
96. Chan, H.S. Kinetics of protein folding. Nature 373, 664-665 (1995).
97. Unger, R. & Moult, J. Local interactions dominate folding in a simple protein model. J. Mol. Biol. 259,988-994 (1996).
98. Fukugita, M., Lancaster, D. & Mitchard, M.G. A heteropolymer model study for the mechanism of protein folding. Biopolymers, in the press.
99. Dill, K.A., Fiebig, K.M. & Chan, H.S. Cooperativity in protein folding kinetics. Proc. Natl. Acad. Sci. USA 90, 1942-1946 (1993).
100. Abkevich, V.I., Gutin, A.M. & Shakhnovich, E.I. Specific nucleus as the transition state for protein folding: Evidence from the lattice model. Biochemistry 33, 10026-10036 (1994).
101. Onuchic, J.N., Socci, N.D., Luthey-Schulten, Z. & Wolynes, P.G. Protein folding funnels: The nature of the transition state ensemble. Folding & Design, in the press.
102. Kiefhaber, T. & Baldwin, R.L. Kinetics of hydrogen bond breakage in the process of unfolding of ribonuclease A measured by pulsed hydrogen exchange. Proc. Natl. Acad. Sci. USA 92, 2657-2661 (1995).
103. 19F-tryptophan-labeled Escherichia coli dihydrofolate reductase. Proc. Natl. Acad. Sci. USA 92, 9318-9322 (1995).
104. Hvidt, A. & Nielsen, S.O. Hydrogen exchange in proteins. Adv. Protein Chem. 21, 287-386 (1966).
105. Miller, D.W. & Dill, K. A. A statistical mechanical model for hydrogen exchange in globular proteins. Protein Sci. 4, 1860-1873 (1995).
106. Alonso, D.O. V. & Dill, K.A. Solvent denaturation and stabilization of globular proteins. Biochemistry 30, 5974-5985 (1991).
107. Dill, K.A., Alonso, D.O.V. & Hutchinson, K. Thermal stabilities of globular proteins. Biochemistry 28, 5439-5449 (1989).
108. Hagen, S.J., Hofrichter, J., Szabo, A. & Eaton, W.A. Diffusion-limited contact formation in unfolded cytochrom c: Estimating the maximum rate of protein folding. Proc. Natl. Acad.Sci. USA 93, 11615-11617 (1996).
109. McCammon, J.A. A speed limit for protein folding. Proc. Natl. Acad. Sci. USA 93, 11426-11427 (1996).