The changing nature of the protein folding transition state: Implications for the shape of the free-energy profile for folding

Journal of Molecular Biology

Volumn 277, Issue 4, 1998, Pages 933-943

  Oliveberg, Mikael ^a   Tan, Yee Joo ^b   Silow, Maria ^a   Fersht, Alan R ^b  

^a CHEMICAL CENTER   (Sweden)

^b MRC CENTRE FOR PROTEIN ENGINEERING   (United Kingdom)

Author keywords

CI2; Energy landscape; Protein engineering; Protein folding; Transition state

Indexed keywords

CHYMOTRYPSIN INHIBITOR;

ARTICLE; ENERGY; GENETIC ENGINEERING; KINETICS; MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING;

EID: 0032503027     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1612     Document Type: Article

References (52)

1. Alexander P., Orban J., Bryan P. Kinetic analysis of folding and unfolding the 56 amino acid IgG-binding domain of streptococcal protein G. Biochemistry. 31:1992;7243-7248
2. Arcus V., Vuilleumier S., Freund S.M.V., Bycroft M., Fersht A.R. Toward solving the folding pathway of barnase the complete 13C, 15N, and 1H NMR assignments of its acid denatured state. Proc. Natl Acad. Sci. USA. 91:1994;9412-9416
3. Baldwin R.L. The nature of protein folding pathways the classic versus the new view. J. Biomol. NMR. 5:1995;103-109
4. Bryngelson J.D., Wolynes P.G. Spin glasses and the statistical mechanics of protein folding. Proc. Natl Acad. Sci. USA. 84:1987;7524-7528
5. Bryngelson J., Onuchic J.N., Socci N.D., Wolynes P. Funnels, pathways, and the energy landscape of protein folding a synthesis. Proteins: Struct. Funct. Genet. 21:1995;167-195
6. Burton R.E., Huang G.S., Daugherty M.A., Fullbright P.W., Oas T.G. Microsecond protein folding through a compact transition state. J. Mol. Biol. 263:1996;311-322
7. Dill K.A., Chan H.S. From Levinthal to pathways to funnels. Nature Struct. Biol. 4:1997;10-19
8. Fersht A.R. Optimization of rates of protein folding the nucleation-condensation mechanism and its applications. Proc. Natl Acad. Sci. USA. 92:1995;10869-10873
9. Finkelstein A.V., Badredtinov A.Y. Rate of protein folding near the point of thermodynamic equilibrium between the coil anf the most stable chain fold. Folding Design. 2:1997;115-121
10. Frauenfelder H., Wolynes P.G. Rate theories and puzzles of hemeprotein kinetics. Science. 229:1985;337-345
11. Hagen S.J., Hofrichter J., Szabo A., Eaton W.A. Diffusion-limited contact formation in unfolded cytochrome c estimating the maximum rate of protein folding. Proc. Natl Acad. Sci. USA. 93:1996;11615-11617
12. Hammond G.S. A correlation of reaction rates. J. Am. Chem. Soc. 77:1955;334-338
13. Hänggi P., Talkner P., Borkovec M. Reaction-rate theory fifty years after Kramers. Rev. Modern Phys. 62:1990;251-341
14. Hao M., Scheraga H.A. How optimization of potential functions affects protein folding. Proc. Natl Acad. Sci. USA. 84:1996;7524-7528
15. Harpaz Y., elMasry N.F., Fersht A.R., Henrick K. Direct observation of better hydration at the N-terminus of an a-helix with glycine rather than alanine as the N-cap residue. Proc. Natl Acad. Sci. USA. 91:1994;311-315
16. Itzhaki L.S., Daniel E.O., Fersht A.R. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering Evidence for a nucleation condensation mechanism for protein folding. J. Mol. Biol. 254:1995;289-304
17. Jackson S.E., Fersht A.R. Folding of chymotrypsin inhibitor 2. 1 evidence for a two-state transition. Biochemistry. 30:1991;10428-10435
18. 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
19. Jonsson T., Waldburger C.D., Sauer T. Nonlinear free energy relationships in arc repressor unfolding imply the existence of unstable, native-like folding intermediates. Biochemistry. 35:1996;4795-4802
20. Kiefhaber T. Kinetic traps in lysozyme folding. Proc. Natl Acad. Sci. USA. 92:1995;9029-9033
21. Kiefhaber T., Labhardt A.M., Baldwin R.L. Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A. Nature. 375:1995;513-515
22. Kragelund B.B., Robinson C.V., Knudsen V., Dobson C.M., Poulsen F.M. Folding of a four-helix bundle studies of acyl-coenzyme A binding protein. Biochemistry. 34:1995;7217-7224
23. Kuszewski J., Clore G.M., Gronenborn A.M. Fast folding of a prototypic polypeptide The immunoglobulin ibinding domain of streptococcal protein G. Protein Sci. 3:1994;1945-1952
24. Lopez-Hernandes I., Serrano L. Structure of the transition state for folding of the 129-amino acid protein Che Y resembles that of the smaller protein CI2. Folding Design. 2:1996;43-55
25. Matouschek A., Fersht A.R. Application of physical organic chemistry to engineered mutants of proteins - Hammond postulate behaviour in the transition state of protein Folding. Proc. Natl Acad. Sci. USA. 90:1993;7814-7818
26. Matouschek A., Kellis J.T. Jr, Serrano L., Fersht A.R. Mapping the transition state and pathway of protein folding by protein engineering. Nature. 342:1989;122-126
27. Matouschek A., Matthews J.M., Johnson C.M., Fersht A.R. Extrapolation to water of kinetic and equilibrium data for the unfolding of barnase in urea solutions. Protein Eng. 7:1994;1089-1095
28. Matouschek A., Otzen D.E., Itzhaki L.S., Jackson S.E., Fersht A.R. Movement of the position of the transition state in protein folding. Biochemistry. 34:1995;13656-13662
29. Matthews J.M., Fersht A.R. Exploring the energy surface of protein folding by structure-reactivity relationships and engineered proteins observations of hammond behaviour for the gross structure of uthe transition state and anti-hammond behaviour for structural elements for unfolding/folding of barnase. Biochemistry. 34:1995;6805-6814
30. Milla M.E., Sauer R.T. P22 Arc repressor folding kinetics of a single-domain, dimeric protein. Biochemistry. 33:1994;1125-1133
31. Milla M.E., Brown B.M., Waldburger C.D., Sauer R.T. P22 Arc repressor transition state properties inferred from mutational effects on the rates of protein unfolding and refolding. Biochemistry. 34:1995;13914-13919
32. Oliveberg M., Fersht A.R. Formation of electrostatic interactions in the protein-folding pathway. Biochemistry. 35:1996;2726-2737
33. Oliveberg M., Fersht A.R. Thermodynamics of transient conformations in the folding pathway of barnase reorganization of the folding intermediate at low pH. Biochemistry. 35:1996;2738-2749
34. Oliveberg M., Tan Y.J., Fersht A.R. Negative activation enthalpy in the kinetics of protein folding. Proc. Natl Acad. Sci. USA. 92:1995;8926-8929
35. Onuchic J.N., Socci N.D., Luthey-Schulten Z., Wolynes P.G. Protein folding funnels the nature of the transition state ensemble. Folding Design. 1:1996;441-450
36. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:1986;266-279
37. Pande V.S., Grosberg A.Y., Tanaka T. On the theory of folding kinetics for short proteins. Folding Design. 2:1997;109-114
38. Parker M.J., Spencer J., Clarke A.R. An integrated kinetic analysis of intermediates and transition states in protein folding reactions. J. Mol. Biol. 253:1995;771-786
39. Parker M.J., Sessions R.B., Badcoe I.G., Clarke A.R. The development of tertiary interactions during the folding of a large protein. Folding Design. 1:1996;145-156
40. Plotkin S.S., Wang J., Wolynes P.G. Statistical mechanics of a correlated energy landscape for protein folding funnels. J. Chem. Phys. 106:1997;2932-2948
41. Sali A., Schaknovich E.I., Karplus M. How does a protein fold? Nature. 369:1994;248-251
42. Schindler T.S., Herrier M., Marahiel M.A., Schmid F.X. Extremely rapid protein folding in the absence of intermediates. Nature Struct. Biol. 2:1995;663-673
43. Shakhnovich E.I. Theoretical studies of protein-folding thermodynamics and kinetics. Curr. Opin. Struct. Biol. 7:1997;29-40
44. Shakhnovich E.I., Farztdinov G., Gutin A.M., Karplus M. Protein folding bottlenecks A lattice Monte Carlo simulation. Phys. Rev. Letters. 67:1991;1665-1668
45. Silow M., Oliveberg M. High-energy channelling in protein folding. Biochemistry. 36:1997;7633-7637
46. Tan Y.J., Oliveberg M., Fersht A.R. Titration properties and thermodynamics of the transition state for folding Comparison of two-state and multi-state folding pathways. J. Mol. Biol. 264:1996;377-389
47. Tanford C. Protein denaturation. C. Theoretical models for the mechanism of denaturation. Advan. Protein Chem. 24:1970;1-95
48. Viguera A.R., Martinez J.C., Filimonov V.V., Mateo P.L., Serrano L. Thermodynamic and kinetic analysis of the SH3 domain of spectrin shows a two-state folding transition. Biochemistry. 33:1994;2142-2150
49. Viguera A.R., Serrano L., Wilmanns M. Different folding transition states may result in the same native structure. Nature Struct. Biol. 3:1996;874-880
50. Villegas V., Azuaga A., Catasus L.I., Reverter D., Mateo P.L., Aviles F.X., Serrano L. Evidence for a two-state transition in the folding process of the activation domain of human procarboxypeptidase A2. Biochemistry. 34:1995;15105-15110
51. Williams S., Causgrove T.P., Gilmanshin R., Fang K.S., Callender R.H., Woodruff W.H., Dyer R.B. Fast events in protein folding helix melting and formation in a small peptide. Biochemistry. 35:1996;691-697
52. Zwanzig R. Two-state models for protein folding kinetics. Proc. Natl Acad. Sci. USA. 94:1997;148-150