Lattice models for proteins reveal multiple folding nuclei for nucleation-collapse mechanism

Journal of Molecular Biology

Volumn 282, Issue 2, 1998, Pages 471-492

  Klimov, D K ^a   Thirumalai, D ^a  

^a Bldg 142   (United States)

Author keywords

Broad transition region; Chymotrypsin inhibitor 2; Multiple folding nuclei; Nucleation collapse mechanism; Protein engineering

Indexed keywords

CHYMOTRYPSIN INHIBITOR; FODRIN;

ALGORITHM; ARTICLE; CELL NUCLEUS; GENETIC ENGINEERING; KINETICS; MODEL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROBABILITY; PROTEIN DOMAIN; PROTEIN FOLDING; THERMODYNAMICS;

EID: 0032544484     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1997     Document Type: Article

References (57)

1. Abkevich, V. I., Gutin, A. M. & Shakhnovich, E. (1994). Specific nucleus as the transition state for protein folding: evidence from the lattice model. Biochemistry, 33, 10026-10036.
2. Arnold, U. & Ulbrich-Hofmann, R. (1997). Kinetic and thermodynamic thermal stabilities of ribonuclease A and ribonuclease B. Biochemistry, 36, 2166-2172.
3. Bowie, J. U., Luthy, R. & Eisenberg, S. (1991). A method to identify protein sequences that fold into a known three-dimensional structure. Science, 253, 164-170.
4. Bryngelson, J. D. & Wolynes, P. G. (1990). A simple statistical field theory of heteropolymer collapse with application to protein folding. Biopolymers, 30, 177-188.
5. Bryngelson, J. D., Onuchic, J. N., Socci, N. D. & Wolynes, P. G. (1995). Funnels, pathways and the energy landscape of protein folding: A synthesis. Proteins: Struct. Funct. Genet. 21, 167-195.
6. Camacho, C. J. & Thirumalai, D. (1993). Kinetics and thermodynamics of folding in model proteins. Proc. Natl Acad. Sci. USA, 90, 6369-6372.
7. Camacho, C. J. & Thirumalai, D. (1995). Modeling the role of disulfide bonds in protein folding: Entropic barriers and pathways. Proteins: Struct. Funct. Genet. 22, 27-40.
8. Chan, H. S. & Dill, K. A. (1994). Transition states and folding dynamics of proteins and heteropolymers. J. Chem. Phys. 100, 9238-9257.
9. Daggett, V., Li, A., Itzhaki, L. S., Otzen, D. E. & Fersht, A. R. (1996). Structure of the transition state for folding of a protein derived from experiment and simulation. J. Mol. Biol. 257, 430-440.
10. Dill, K. A. & Chan, H. S. (1997). From Levinthal to pathways to funnels. Nature Struct. Biol. 4, 10-19.
11. Du, R., Pande, V. S., Grosberg, A. Yu., Tanaka, T. & Shakhnovich, E. (1998). On the transition coordinate for protein folding. J. Chem. Phys. 108, 334-350.
12. Ferrenberg, A. M. & Swendsen, R. H. (1989). Optimized Monte Carlo data analysis. Phys. Rev. Letters, 63, 1195-1198.
13. Fersht, A. R. (1995a). Characterizing transition states in protein folding: an essential step in the puzzle. Curr. Opin. Struct. Biol. 5, 79-84.
14. Fersht, A. R. (1995b). Optimization of rates of protein folding: the nucleation-condensation mechanism and its implications. Proc. Natl Acad. Sci. USA, 92, 10869-10873.
15. Fersht, A. R. (1997). Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7, 3-9.
16. Goldstein, R. A., Luthey-Schulten, Z. A. & Wolynes, P. G. (1992). Optimal protein-folding codes from spin-glass theory. Proc. Natl Acad. Sci USA, 89, 4918-4922.
17. Gorindarajan, S. & Goldstein, R. A. (1995). Optimal local propensities for model proteins. Proteins: Struct. Funct. Genet. 22, 413-418.
18. Guo, Z. & Thirumalai, D. (1995). Kinetics of protein folding: nucleation mechanism, time scales, and pathways. Biopolymers, 36, 83-103.
19. Guo, Z. & Thirumalai, D. (1997). The nucleation-collapse mechanism in protein folding: evidence for the nonuniqueness of the folding nucleus. Folding Design, 2, 377-391.
20. Guo, Z., Thirumalai, D. & Honeycutt, J. D. (1992). Folding kinetics of proteins: a model study. J. Chem. Phys. 97, 525-535.
21. Hendsch, Z. S., Jonsson, T., Sauer, R. T. & Tidor, B. (1996). Protein stabilization by removal of unsatisfied polar groups. Computational approaches and experimental tests. Biochemistry, 35, 7621-7625.
22. Itzhaki, L. S., Neira, J. L., Ruiz-Sanz, J., Gay, G. D. & Fersht, A. R. (1995a). Search for nucleation sites in smaller fragments of chymotrypsin inhibitor 2. J. Mol. Biol. 254, 289-304.
23. Itzhaki, L. S., Otzen, D. E. & Fersht, A. R. (1995b). The structure of the transition state of chymotrypsin inhibitor 2 analyzed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254, 260-288.
24. Jackson, S. E. & Fersht, A. R. (1991). Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry, 30, 10428-10435.
25. Karpen, M. E., Tobins, D. J. & Brooks, C. L., III (1993). Statistical clustering techniques for the analysis of long molecular dynamics trajectories: analysis of 2-2 in trajectories of YPGDY. Biochemistry, 32, 412-420.
26. Klimov, D. K. & Thirumalai, D. (1996a). Factors governing the foldability of proteins. Proteins: Struct. Funct. Genet. 26, 411-441.
27. Klimov, D. K. & Thirumalai, D. (1996b). A criterion that determines the foldability of proteins. Phys. Rev. Letters, 76, 4070-4073.
28. Kolinski, A., Godzik, A. & Skolnick, J. (1993). A general method for the prediction of the three-dimensional structure and folding pathway of globular proteins: application to designed helical proteins. J. Chem. Phys. 98, 7420-7433.
29. Kuszewski, J., Clore, G. M. & Gronenborn, A. M. (1994). Fast folding of a prototypic polypeptide: the immunoglobulin binding domain of streptococcal proteins G. Proteins Sci. 3, 1945-1952.
30. Li, A. & Daggett, V. (1996). Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 using molecular dynamics simulations. J. Mol. Biol. 257, 412-429.
31. Matheson, R. R. & Scheraga, H. A. (1978). A method for predicting nucleation sites for protein folding based on hydrophobic contacts. Macromolecules, 11, 814-829.
32. Milla, M. E. & Sauer, R. T. (1994). P22 arc repressor: folding kinetics of a single-domain, dimeric protein. Biochemistry, 33, 1125-1133.
33. Miyazawa, S. & Jernigan, R. L. (1985). Estimation of effective inter-residue contact energies from protein crystal structures: quasi-chemical approximation. Macromolecules, 18, 534-552.
34. Onuchic, J. N., Wolynes, P. G., Luthey-Schulten, Z. & Socci, N. D. (1995). Towards an outline of the topography of a realistic protein folding funnel. Proc. Natl Acad. Sci. USA, 92, 3626-3630.
35. Onuchic, J. N., Socci, N. D., Luthey-Schulten, Z. & Wolynes, P. G. (1996). Protein folding funnels: the nature of the transition state ensemble. Folding Design, 1, 441-450.
36. Oxtoby, D. W. (1988). Nucleation of crystals from the melt. Advan. Chem. Phys. 70, 263-296.
37. Oxtoby, D. W. (1998). Nucleation of first-order phase transitions. Acc. Chem. Res. 31, 91-97.
38. Pande, V. S., Grosberg, A. Yu. & Tanaka, T. (1997). On the theory of folding kinetics for short proteins. Folding Design, 2, 109-114.
39. Pao, Y.-H. (1989). Adaptive Pattern Recognition and Neural Networks, Addison-Welsley, New York.
40. Perl, D., Welker, C., Schindler, T., Schroder, K., Marahiel, M. A., Jaenicke, R. & Schmid, F. X. (1998). Conservation of rapid two-state folding in mesophilic thermophilic, and hyperthermophilic cold shock proteins. Nature Struct. Biol. 5, 229-235.
41. Plaxco, K. W., Spitzfaden, C., Campbell, I. D. & Dobson, C. M. (1997). A comparison of the folding kinetics and thermodynamics of two homologous fibronectin type III modules. J. Mol. Biol. 270, 763-770.
42. Plaxco, K. W., Simons, K. T. & Baker, D. (1998). Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277, 985-994.
43. Sali, A., Shakhnovich, E. & Karplus, M. (1994). Kinetics of protein folding: a lattice model study of the requirements for folding to the native state. J. Mol. Biol. 235, 1614-1636.
44. Schonbrunner, N., Koller, K.-P. & Kiefhaber, T. (1997). Folding of the disulfide-bonded ß-sheet protein tendamistat: rapid two-state folding without hydrophobic collapse. J. Mol. Biol. 268, 526-538.
45. Shakhnovich, E. (1994). Proteins with selected sequences fold into unique native conformation. Phys. Rev. Letters, 72, 3907-3910.
46. Shakhnovich, E. & Gutin, A. M. (1993). A new approach to the design of stable proteins. Protein Eng. 6, 793-800.
47. Shakhnovich, E., Abkevich, V. I. & Ptitsyn, O. (1996). Conserved residue and the mechanisms of protein folding. Nature, 379, 96-98.
48. Socci, N. D. & Onuchic, J. N. (1995). Kinetic and thermodynamic analysis of protein-like heteropolymers: Monte Carlo histogram technique. J. Chem. Phys. 103, 4732-4744.
49. 6 particle molecular dynamics study of homogeneous nucleation of crystals in a supercooled atomic liquid. Phys. Rev. ser B, 41, 7042-7053.
50. ten Wolde, P. R. & Frenkel, D. (1997). Enhancement of protein crystal nucleation by critical density fluctuations. Science, 277, 1975-1978.
51. Unger, R. & Moult, J. (1996). Local interactions dominate folding in a simple protein model. J. Mol. Biol. 259, 988-994.
52. Viguera, A. R., Serrano, L. & Wilmanns, M. (1996). Different folding transition states may result in the same native structure. Nature Struct. Biol. 3, 874-880.
53. Waldburger, C. D., Jonsson, T. & Sauer, R. T. (1996). Barriers to proteins folding: formation of buried polar interactions is a slow step in acquisition of structure. Proc. Natl Acad. Sci. USA, 93, 2629-2634.
54. Wetlaufer, D. (1973). Nucleation, rapid folding, and globular intrachain regions in proteins. Proc. Natl Acad. Sci. USA, 70, 697-701.
55. Wolynes, P. G. (1997). Folding funnels and energy landscapes of larger proteins within the capillarity approximation. Proc. Natl Acad. Sci. USA, 94, 6170-6175.
56. Wolynes, P. G., Onuchic, J. N. & Thirumalai, D. (1995). Navigating the folding routes. Science, 267, 1619-1620.
57. Yang, J., Gould, H., Klein, W. & Mountain, R. D. (1990). Molecular dynamics investigation of deeply quenched liquids. J. Chem. Phys. 93, 711-723.