Microsecond protein folding through a compact transition state

Journal of Molecular Biology

Volumn 263, Issue 2, 1996, Pages 311-322

  Burton, Randall E ^a   Huang, Guewha S ^a,b   Daugherty, Margaret A ^a   Fullbright, Paul W ^a   Oas, Terrence G ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

Chemical exchange; Folding pathways; Nuclear magnetic relaxation; Transition state theory; Transverse relaxation

Indexed keywords

ALANINE; GLYCINE; MUTANT PROTEIN; UREA;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; KINETICS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FOLDING; THERMOSTABILITY;

MUS;

EID: 0030601788     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0577     Document Type: Article

References (61)

1. Abkevich, V. I., Gutin, A. M. & Shakhnovich, E. I. (1994). Specific nucleus as the transition state for protein folding: evidence from the lattice model. Biochemistry, 33, 10,026-10,036.
2. Baldwin, R. L. (1989). How does protein folding get started? Trends Biochem. Sci. 14, 291-294.
3. Baldwin, R. L. (1996). On-pathway versus off-pathway intermediates. Folding and Design, 1, R1-R8.
4. 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.
5. 1H NMR titration shifts of amide proton resonances in polypeptide chains. FEBS Letters, 77, 11-14.
6. Carr, H. Y. & Purcell, E. M. (1954). Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys. Rev. 94, 630-638.
7. Chen, B.-L., Baase, W. A. & Schellman, J. A. (1989). Low-temperature unfolding of a mutant of phage T4 lysozyme. 2. Kinetic investigations. Biochemistry, 28, 691-699.
8. Chen, B.-L. Baase, W. A., Nicholson, H. & Schellman, J. A. (1992). Folding kinetics of T4 lysozyme and nine mutants at 12°C. Biochemistry, 31, 1464-1476.
9. Chou, P. Y. & Fasman, G. D. (1978). Prediction of the secondary structure of proteins from their amino acid sequence. Adv. Enzymol. 47, 45-148.
10. D'Aquino, J. A., Gomez, J., Hilser, V. J., Lee, K. H., Amzel, L. M. & Freire, E. (1996). The magnitude of the backbone conformational entropy change in protein folding. Proteins: Struct. Fund. Genet. 25, 143-156.
11. 2-terminal arm of phage λ repressor contributes energy and specificity to repressor binding and determines the effects of operator mutations. Proc. Natl Acad. Sci. USA, 82, 2339-2343.
12. Fersht, A. R. (1985). Enzyme Structure and Mechanism. W. H. Freeman and Company, New York.
13. Fersht, A. R., Matouschek, A. & Serrano, L. (1992). The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224, 771-782.
14. Fersht, A. R. (1995). Optimization of rates of protein folding: the nucleation-condensation mechanism and its implications. Proc. Natl Acad. Sci. USA, 92, 10,869-10,873.
15. Gutin, A. M., Abkevich, V. I. & Shakhnovich, E. I. (1995). Is burst hydrophobic collapse necessary for protein folding? Biochemistry, 34, 3066-3076.
16. Hammes, G. G. & Roberts, P. B. (1969). Dynamics of the helix-coil transition in poly-L-ornithine. J. Am. Chem. Soc. 91, 1812-1816.
17. Harrison, S. C. & Durbin, R. (1985). Is there a single pathway for the folding of a polypeptide chain? Proc. Natl Acad. Sci. USA, 82, 4028-4030.
18. Hecht, M. H., Hehir, K. M., Nelson, H. C., Sturtevant, J. M. & Sauer, R. T. (1985). Increasing and decreasing protein stability: effects of revertant substitutions on the thermal denaturation of phage lambda repressor. J. Cell Biochem. 29, 217-224.
19. Hecht, M. H., Sturtevant, J. M. & Sauer, R. T. (1986). Stabilization of lambda repressor against thermal denaturation by site-directed Gly-Ala changes in alpha-helix 3. Proteins: Struct. Funct. Genet. 1, 43-46.
20. Huang, G. S. & Oas, T. G. (1995a). Structure and stability of a monomeric λ repressor: NMR evidence for two-state folding. Biochemistry, 34, 3884-3892.
21. Huang, G. S. & Oas, T. G. (1995b). Sub-millisecond folding of monomeric λ repressor. Proc. Natl Acad. Sci. USA, 92, 6878-6882.
22. Itzhaki, L. S., Otzen, D. E. & Fersht, A. R. (1995). The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods. J. Mol. Biol. 254, 260-288.
23. Jackson, S. E., Elmasry, N. & Fersht, A. R. (1993). Structure of the hydrophobic core in the transition state for folding of chymotrypsin inhibitor-2 - a critical test of the protein engineering method of analysis. Biochemistry, 32, 11,270-11,278.
24. Karplus, M. & Weaver, D. L. (1976). Protein-folding dynamics. Nature, 260, 404-406.
25. Khorasanizadeh, S., Peters, I. D. & Roder, H. (1996). Evidence for a three-state model of protein folding from kinetic analysis of ubiquitin variants with altered core residues. Nature Struct. Biol. 3, 193-205.
26. Kiefhaber, T. (1995). Kinetic traps in lysozyme folding. Proc. Natl Acad. Sci. USA, 92, 9029-9033.
27. Kim, P. S. & Baldwin, R. L. (1982). Specific itermediates in the folding reactions of small proteins and the mechanism of protein folding. Annu. Rev. Biochem. 51, 459-489.
28. Kim, P. S. & Baldwin, R. L. (1990). Intermediates in the folding reactions of small proteins. Annu Rev. Biochem. 59, 631-660.
29. Kragelund, B. B., Robinson, C. V., Knudsen, J., Dobson, C. M. & Poulsen, F. M. (1995). Folding of a four-helix bundle: studies of acyl-coenzyme A binding protein. Biochemistry, 34, 7217-7224.
30. Kraulis, P. K. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
31. Kraut, J. (1988). How do enzymes work? Science, 242, 533-540.
32. Kunkel, T. A., Roberts, J. D. & Zakour, R. A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
33. Kuszewski, J., Clore, G. M. & Gronenborn, A. M. (1994). Fast folding of a prototypic polypeptide: the immunoglobulin binding domain of streptococcal protein. Protein Sci. 3, 1945-1952.
34. Levinthal, C. (1968). Are there pathways for protein folding? J. Chem. Phy. 65, 44-45.
35. Lewin, B. (1990). Genes IV. Oxford University Press, New York.
36. Lopez-Hernandez, E. & Serrano, L. (1996). Structure of the transition state of folding of the 129 aa protein CheY resembles that of a smaller protein, CI-2. Folding Design, 1, 43-55.
37. Marmorino, J. L. & Pielak, G. J. (1995). A native tertiary in interaction stabilizes the A state of cytochrome c. Biochemistry, 34, 3140-3143.
38. Marquardt, D. W. (1963). An algorithm for least-squares estimation of nonlinear parameters. J. Soc. Industr. Appl. Math. 11, 431-441.
39. Matthews, J. M. & Fersht, A. R. (1995). Exploring the energy surface of protein folding by structure-reactivity relationships and engineered proteins: observation of Hammond behavior for the gross structure of the transition state and anti-Hammond behavior for structural elements for unfolding/folding of barnase. Biochemistry, 34, 6805-6814.
40. Matouschek, A., Kellis, J. T., Jr, Serrano, L. & Fersht, A. R. (1989). Mapping the transition state and pathway of protein folding by protein engineering. Nature, 340, 122-126.
41. Matouschek, A., Otzen, D. E., Itzhaki, L. S., Jackson, S. E. & Fersht, A. R. (1995). Movement of the position of the transition state in protein folding. Biochemistry, 34, 13,656-13,662.
42. Meiboom, S. & Gill, D. (1958). Modified spin-echo method for measuring nuclear relaxation times. Rev. Sci. Instrum. 29, 688-691.
43. Milla, M. E., Brown, B. M., Waldburger, C. D. & Sauer, R. T. (1995). P22 arc repressor: transition state properties in inferred from mutational effects on the rates of protein unfolding and refolding. Biochemistry, 34, 13914-13919.
44. Nilsson, B. & Anderson, S. (1991). Proper and improper folding of proteins in the cellular environment. Annu. Rev. Microbiol. 45, 607-635.
45. Oldfield, E. (1995). Chemical shifts and three-dimensional protein structures. J. Biomol. NMR, 5, 217-225.
46. Orekhov, V. Y., Pervushin, K. V. & Arseniev, A. S. (1994). Backbone dynamics of (1-71)bacterioopsin studied by two-dimensional 1H-15N NMR spectroscopy. Eur. J. Biochem. 219, 887-896.
47. Pabo, C. O. & Lewis, M. (1982). The operator-binding domain of lambda repressor: structure and DNA recognition. Nature, 298, 443.
48. Pace, C. N. (1986). Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131, 266-280.
49. Sandstrom, J. (1982). Dynamic NMR Spectroscopy. Acdemic press, London.
50. Schindler, T., Herrler, M., Marahiel, M. A. & Schmid, F. X. (1995). Extremely rapid protein folding in the absence of intermediates. Nature Struct. Biol. 2, 663-673.
51. Serrano, L., Matouschek, A. & Fersht, A. R. (1992). The folding of an enzyme. III. Structure of the transition state for unfolding of barnase analysed by a protein engineering procedure. J. Mol. Biol. 224, 805-818.
52. Sosnick, T. R., Mayne, L., Hiller, R. & Englander, S. W. (1994). The barriers in protein folding. Struct. Biol. 1, 149-156.
53. Sosnick, T. R., Jackson, S., Wilk, R. R., Englander, S. W. & DeGrado, W. F. (1996). The role of helix formation in the folding of a fully α-helical coiled coil. Proteins: Struct Funct. Genet. 24, 427-432.
54. Studier, F. W., Rosenberg, A. H., Dunn, J. J. & Dubendorff, J. W. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185, 60-89.
55. Tanford, C. (1970). Protein denaturation. Advan. Protein Chem. 24, 1-95.
56. Waldburger, C. D., Jonsson, T. & Sauer, R. T. (1996). Barriers to protein folding: formation of buried polar interactions is a slow step in the acquisition of structure. Proc. Natl Acad. Sci. USA, 93, 2629-2634.
57. Wang, J. & Purisima, E. O. (1996). Analysis of thermodynamic determinants in helix propensities of nonpolar amino acids through a novel free energy calculation. J. Am. Chem. Soc. 118, 995.
58. Weiss, M. A., Pabo, C. O., Karplus, M. & Sauer, R. T. (1987). Dimerization of the operator binding domain of phage λ repressor. Biochemistry, 26, 897-904.
59. Wemmer, D., Ribeiro, A. A., Bray, R. P., Wade-Jardetzky, N. G. & Jardetzky, O. (1981). High-resolution nuclear magnetic resonance studies of the lac repressor. 3. Unfolding of the lac repressor headpiece. Biochemistry, 20, 829-833.
60. Wenzel, T. & Baumeister, W. (1995). Conformational constraints in protein degradation by the 20S proteasome. Nature Struct. Biol. 2, 199-204.
61. Wolynes, P. G., Onuchic, J. N. & Thirumalai, D. (1995) Navigating the Folding Routes. Science 267, 1619-1620.