The energy landscape of a fast-folding protein mapped by Ala→Gly substitutions

Nature Structural Biology

Volumn 4, Issue 4, 1997, Pages 305-310

  Burton, Randall E ^a   Huang, Guewha S ^a,b   Daugherty, Margaret A ^a,c   Calderone, Tiffany L ^a   Oas, Terrence G ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REPRESSOR PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CONFORMATIONAL TRANSITION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FOLDING;

ALANINE; DNA-BINDING PROTEINS; GLYCINE; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS; PROTEIN FOLDING; REPRESSOR PROTEINS; THERMODYNAMICS; VIRAL PROTEINS;

MUS;

EID: 0031005061     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb0497-305     Document Type: Article

References (46)

1. Dobson, C.M., Evans, P.A. & Radford, S.E. Understanding how proteins fold: the lysozyme story so far. Trends Biochem. Sci. 19, 31-37 (1994).
2. 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).
3. Udgaonkar, J.B. & Baldwin, R.L. NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 335, 694-699 (1988).
4. 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, 13194-13919 (1995).
5. 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, 771-782 (1992).
6. Harrison, S.C. & Durbin, R. Is there a single pathway for the folding of a polypeptide chain? Proc. Nat. Acad. Sci. USA 82, 4028-4030 (1985).
7. Viguera, A.R., Serrano, L. & Wilmanns, M. Different folding transition states may result in the same native structure. Nature Struct Biol. 3, 874-880 (1996).
8. Wolynes, P.G., Onuchic, J.N. & Thirumalai, D. Navigating the folding routes. Science 267, 1619-1620 (1995).
9. Dill, K.A. et al. Principles of protein folding-A perspective from simple exact models. Protein Sci. 4, 561-602 (1995).
10. Dill, K.A. & Chan, H.S. From Leventhal to pathways to funnels. Nature Struct. Biol. 4, 10-19 (1997).
11. Baldwin, R.L. On-pathway versus off-pathway folding intermediates. Folding and Design 1, R1-R8 (1996).
12. Ptitsyn, O.B. Kinetic and equilibrium intermediates in protein folding. Protein Eng. 7, 593-596 (1994).
13. Huang, G.S. & Oas, T.G. Sub-millisecond folding of monomeric λ repressor. Proc. Nat. Acad. Sci. USA 92, 6878-6882 (1995).
14. 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, 311-322 (1996).
15. Huang, G.S. & Oas, T.G. Structure and stability of monomeric λ repressor: NMR evidence for two-state folding. Biochemistry 34, 3884-3892 (1995).
16. Onuchic, J.N., Socci, N.D., Luthey-Schulten, Z. & Wolynes, P.G. Protein folding funnels: the nature of the transition state ensemble. Folding and Design 1, 441-450 (1996).
17. Pabo, C.O. & Lewis, M. The operator-binding domain of lambda repressor: structure and DNA recognition. Nature 298, 443-447 (1982).
18. D'Aquino, J.A. et al. The magnitude of the backbone conformational entropy change in protein folding. Proteins 25, 143-156 (1996).
19. Lee, B. Estimation of the maximum change in stability of globular proteins upon mutation of a hydrophobic residue to another of smaller size. Protein Sci. 2, 733-738 (1993).
20. Wang, J. & Purisima, E.O. Analysis of Thermodynamic Determinants in Helix Propensities on Nonpolar Amino Acids through a Novel Free Energy Calculation. J. Am. Chem. Soc. 118, 995-1001 (1996).
21. Serrano, L., Sancho, J., Hirshberg, M. & Fersht, A.R. α-helix stablitity in proteins I. emperical correlations concerning substitution of side-chains at the N and C-caps and the replacement of alanine by glycine or serine at solvent-exposed surfaces. J. Mol. Biol. 227, 544-559 (1992).
22. Myers, J.K., Pace, C.N. & Scholtz, J.M. Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2135-2148 (1995).
23. 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).
24. Tanford, C. Protein denaturation. Adv. Protein Chem. 24, 1-95 (1970).
25. Matouschek, A., Kellis, J.T., Jr., Serrano, L. & Fersht, A.R. Mapping the transition state and pathway of protein folding by protein engineering. Nature 340, 122-126 (1989).
26. Levinthal, C. Are there pathways for protein folding? J. Chem. Phys. 65, 44-45 (1968).
27. Waldburger, C.D., Jonsson, T. & Sauer, R.T. Barriers to protein folding: formation of buried polar interactions is a slow step in acquisition of structure. Proc. Nat. Acad. Sci. USA 93, 2629-2634 (1996).
28. Bryngelson, J.D., Onuchic, J.N., Socci, N.D. & Wolynes, P.G. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins 21, 167-195 (1995).
29. Leach, S.J., Nemethy, G. & Scheraga, H.A. Computation of the sterically allowed conformations of peptides. Biopolymers 4, 369-407 (1966).
30. Creamer, T.P. & Rose, G.D. α-helix-forming propensities in peptides and proteins. Proteins 19, 85-97 (1994).
31. 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, 13656-13662 (1995).
32. Hammes, G.G. & Roberts, P.B. Dynamics of the helix-coil transition in poly-l-ornithine.J. Am. Chem. Soc. 91, 1812-1816 (1969).
33. Williams, S., et al. Fast events in protein folding: helix melting and formation in a small peptide. Biochemistry 35, 691-697 (1996).
34. Wang, Y. & Shortle, D. The equilibrium folding pathway of staphylcoccal nuclease: Identification of the most stable chain-chain interactions by NMR and CD spectroscopy. Biochemistry 34, 15895-15905 (1995).
35. Bai, Y.W., Sosnick, T.R., Mayne, L. & Englander, S.W. Protein folding intermediates -native-state hydrogen exchange. Science 269, 192-197 (1995).
36. Bai, Y. & Englander, S.W. Future directions in folding: The multi-state nature of protein structure. Proteins 24, 145-151 (1996).
37. Viguera, A.R., Villegas, V., Aviles, F.X. & Serrano, L. Favourable native-like helical local interactions can accelerate protein folding. Folding and Design 2, 23-33 (1996).
38. Karplus, M. & Weaver, D.L. Protein-folding dynamics. Nature 260, 404-406 (1976).
39. Karplus, M. & Weaver, D.L. Protein folding dynamics: the diffusion-collision model and experimental data. Protein Sci. 3, 650-668 (1994).
40. Kim, P.S. & Baldwin, R.L. Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding. Annu. Rev. Biochem. 51, 459-89 (1982).
41. Kim, P.S. & Baldwin, R.L. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 59, 631-60 (1990).
42. Saven, J.G. & Wolynes, P.G. Local conformational signals and the statistical thermodynamics of collapsed helical proteins. J. Mol. Biol. 257, 199-216 (1996).
43. Marqusee, S. & Sauer, R.T. Contribution of hydrogen bond/salt bridge network to the stability of secondary and tertiary structure in λ repressor. Protein Sci. 3, 2217-2225 (1994).
44. Pace, C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131, 266-280 (1986).
45. Sandstrom, J. Dynamic NMR Spectroscopy (Academic Press, London, 1982).
46. Kraulis, P.K. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950 (1991).