Role of unfolded state heterogeneity and en-route ruggedness in protein folding kinetics

Protein Science

Volumn 15, Issue 3, 2006, Pages 564-582

  Ellison, Paul A ^a   Cavagnero, Silvia ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Kinetics; Landscapes; Pathways; Protein folding; Single exponential; Stretched exponential

Indexed keywords

PROTEIN;

ARTICLE; CONFORMATION; ENERGY; KINETICS; MICROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING;

KINETICS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 33644554831     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.051758206     Document Type: Article

References (57)

1. Ansari, A., Jones, C.M., Henry, E.R., Hofrichter, J., and Eaton, W.A. 1992. The role of solvent viscosity in the dynamics of protein conformational changes. Science 256: 1796-1798.
2. Baldwin, R.L. 1995. The nature of protein folding pathways: The classical versus the new view. J. Biomol. NMR 5: 103-109.
3. Brooks III, C.L. 2002. Protein and peptide folding explored with molecular simulations. Acc. Chem. Res. 35: 447-454.
4. Brooks III, C.L., Gruebele, M., Onuchic, J.N., and Wolynes, P.G. 1998. Chemical physics of protein folding. Proc.Natl. Acad. Sci. 95: 11037-11038.
5. Bryngelson, J.D., Onuchic, J.N., Socci, N.D., and Wolynes, P.G. 1995. Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins 21: 167-195.
6. Capaldi, A.P., Ferguson, S.J., and Radford, S.E. 1999. The Greek key protein apo-pseudoazurin folds through an obligate on-pathway intermediate. J. Mol. Biol. 286: 1621-1632.
7. Capaldi, A.P., Shastry, M.C., Kleanthous, C., Roder, H., and Radford, S.E. 2001. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nat. Struct. Biol. 8: 68-72.
8. Chattopadhyay, K., Elson, E.L., and Frieden, C. 2005. The kinetics of conformational fluctuations in an unfolded protein measured by fluorescence methods. Proc. Natl. Acad. Sci. 102: 2385-2389.
9. Clementi, C., Nymeyer, H., and Onuchic, J.N. 2000. Topological and energetic factors: What determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol. 298: 937-953.
10. Creighton, T.E. 1988. Toward a better understanding of protein folding pathways. Proc. Natl. Acad. Sci. 85: 5082-5086.
11. _. 1994. The protein folding problem. In Mechanisms of protein folding (ed. R.H. Pain), pp. 1-25. Oxford University Press, Oxford.
12. Deniz, A.A., Laurence, T.A., Beligere, G.S., Dahan, M., Martin, A.B., Chemla, D.S., Dawson, P.E., Schultz, P.G., and Weiss, S. 2000. Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc. Natl. Acad. Sci. 97: 5179-5184.
13. Dill, K.A. and Shortle, D. 1991. Denatured states of proteins. Annu. Rev. Biochem. 60: 795-825.
14. Dyson, H.J. and Wright, P.E. 2002. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. In Unfolded proteins, pp. 311-340. Academic Press, San Diego, CA.
15. _ 2004. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 104: 3607-3622.
16. _. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6: 197-208.
17. Evans, P.A. and Radford, S.E. 1994. Probing the structure of folding intermediates. Curr. Opin. Struct. Biol. 4: 100-106.
18. Flanagan, J.M., Kataoka, M., Shortle, D., and Engelman, D.M. 1992. Truncated staphylococcal nuclease is compact but disordered. Proc. Natl. Acad. Sci. 89: 748-752.
19. Garcia-Mira, M.M., Sadqi, M., Fischer, N., Sanchez-Ruiz, J.M., and Muñoz, V. 2002. Experimental identification of downhill protein folding. Science 298: 2191-2195.
20. Gillespie, B. and Plaxco, K.W. 2004. Using protein folding rates to test protein folding theories. Annu. Rev. Biochem. 73: 837-859.
21. Gruebele, M. 1999. The fast protein folding problem. Ann. Rev. Phys. Chem. 50: 485-516.
22. _. 2002. Protein folding: The free energy surface. Curr. Opin. Struct. Biol. 12: 161-168.
23. Hindmarsh, A.C. 1983. ODEPACK: A systematised collection of ODE solvers. In Scientific computing (eds. R.S. Stepleman and M. Carver), pp. 55-64. North Holland Publishing Company, Amsterdam.
24. Jackson, S.E. 1998. How do small single-domain proteins fold? Fold. Des. 3: R81-R91.
25. Jennings, P.A. and Wright, P.E. 1993. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262: 892-896.
26. Karplus, M. and Weaver, D.L. 1976. Protein-folding dynamics. Nature 260: 404-406.
27. _. 1994. Protein folding dynamics: The diffusion-collision model and experimental data. Protein Sci. 3: 650-668.
28. Kim, P.S. and Baldwin, R.L. 1982. Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding. Annu. Rev. Biochem. 51: 459-489.
29. _. 1990. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 59: 631-660.
30. Lietzow, M.A., Jamin, M., Jane Dyson, H.J., and Wright, P.E. 2002. Mapping long-range contacts in a highly unfolded protein. J. Mol. Biol. 322: 655-662.
31. Lipman, E.A., Schuler, B., Bakajin, O., and Eaton, W.A. 2003. Single-molecule measurement of protein folding kinetics. Science 301: 1233-1235.
32. Ma, H.R. and Gruebele, M. 2005. Kinetics are probe-dependent during downhill folding of an engineered λ(6-85) protein. Proc. Natl. Acad. Sci. 102: 2283-2287.
33. Mendes, P. 1993. GEPASI: A software package for modelling the dynamics, steady states and control of biochemical and other systems. Comput. Appl. Biosci. 9: 563-571.
34. _. 1997. Biochemistry by numbers: Simulation of biochemical pathways with Gepasi 3. Trends Biochem. Sci. 22: 361-363.
35. Mendes, P. and Kell, D. 1998. Non-linear optimization of biochemical pathways: Applications to metabolic engineering and parameter estimation. Bioinformatics 14: 869-883.
36. Muñoz, V., Thompson, P.A., Hofrichter, J., and Eaton, W.A. 1997. Folding dynamics and mechanism of b-hairpin formation. Nature 390: 196-199.
37. Naganathan, A.N., Perez-Jimenez, R., Sanchez-Ruiz, J.M., and Muñoz, V. 2005. Robustness of downhill folding: Guidelines for the analysis of equilibrium folding experiments on small proteins. Biochemistry 44: 7435-7449.
38. Navon, A., Ittah, V., Landsman, P., Scheraga, H.A., and Haas, E. 2001. Distributions of intramolecular distances in the reduced and denatured states of bovine pancreatic ribonuclease A: Folding initiation structures in the C-terminal portions of the reduced protein. Biochemistry 40: 105-118.
39. Nevo, R., Brumfeld, V., Kapon, R., Hinterdorfer, P., and Reich, Z. 2005. Direct measurement of protein energy landscape roughness. EMBO Rep. 6: 482-486.
40. Nguyen, H., Jager, M., Moretto, A., Gruebele, M., and Kelly, J.W. 2003. Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation. Proc. Natl. Acad. Sci. 100: 3948-3953.
41. Nishimura, C., Dyson, H.J., and Wright, P.E. 2002. The apomyoglobin folding pathway revisited: Structural heterogeneity in the kinetic burst phase intermediate. J. Mol. Biol. 322: 483-489.
42. Ozkan, S.B., Dill, K.A., and Bahar, I. 2002. Fast-folding protein kinetics, hidden intermediates and the sequential stabilization model. Protein Sci. 11: 1958-1970.
43. Petzold, L.R. 1983. Automatic selection of methods for solving stiff and nonstiff systems of ordinary differential equations. SIAM J. Sci. Statistical Comput. 4: 136-148.
44. Pletneva, E.V., Gray, H.B., and Winkler, J.R. 2005. Many faces of the unfolded state: Conformational heterogeneity in denatured yeast cytochrome C. J. Mol. Biol. 345: 855-867.
45. Roder, H. 2004. Stepwise helix formation and chain compaction during protein folding. Proc. Natl. Acad. Sci. 101: 1793-1794.
46. Sabelko, J., Ervin, J., and Gruebele, M. 1999. Observation of strange kinetics in protein folding. Proc. Natl. Acad. Sci. 96: 6031-6036.
47. Schuler, B., Lipman, E.A., and Eaton, W.A. 2002. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419: 743-747.
48. Schwarzinger, S., Wright, P., and Dyson, H. 2002. Molecular hinges in protein folding: The urea-denatured state of apomyoglobin. J. Biomol. NMR 41: 12681-12686.
49. Snow, C.D., Nguyen, H., Pande, V.S., and Gruebele, M. 2002. Absolute comparison of simulated and experimental protein-folding dynamics. Nature 420: 102-106.
50. Spudich, G.M., Miller, E.J., and Marqusee, S. 2004. Destabilization of the Escherichia coli RNase H kinetic intermediate: Switching between a two-state and three-state folding mechanism. J. Mol. Biol. 335: 609-618.
51. Talaga, D.S., Lau, W.L., Roder, H., Tang, J., Jia, Y., DeGrado, W.F., and Hochstrasser, R.M. 2000. Dynamics and folding of single twostranded coiled-coil peptides studied by fluorescent energy transfer confocal microscopy. Proc. Natl. Acad. Sci. 97: 13021-13026.
52. Tsui, V., Garcia, C., Cavagnero, S., Siuzdak, G., Dyson, H.J., and Wright, P.E. 1999. Quench-flow experiments combined with mass spectrometry show apomyoglobin folds through and obligatory intermediate. Protein Sci. 8: 45-49.
53. Wagner, C. and Kiefhaber, T. 1999. Intermediates can accelerate protein folding. Proc. Natl. Acad. Sci. 96: 6716-6721.
54. Walkenhorst, W.F., Green, S.M., and Roder, H. 1997. Kinetic evidence for folding and unfolding intermediates in staphylococcal nuclease. Biochemistry 36: 5795-5805.
55. Wolynes, P.G., Onuchic, J.N., and Thirumalai, D. 1995. Navigating the folding routes. Science 267: 1619-1620.
56. Yao, J., Chung, J., Eliezer, D., Wright, P.E., and Dyson, H.J. 2001. NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding. Biochemistry 40: 3561-3571.
57. Zwanzig, R. 1997. Two-state models of protein folding kinetics. Proc. Natl. Acad. Sci. 94: 148-150.