The folding energy landscape and free energy excitations of cytochrome c

Accounts of Chemical Research

Volumn 43, Issue 5, 2010, Pages 652-660

  Weinkam, Patrick ^b   Zimmermann, Jöirg ^a   Romesberg, Floyd E ^a   Wolynes, Peter G ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PH; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

CYTOCHROMES C; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 77952590099     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar9002703     Document Type: Article

References (52)

1. Sosnick, T. R.; Mayne, L.; Englander, S. W. Molecular collapse: The rate-limiting step in two-state cytochrome c folding Proteins: Struct., Funct, Genet. 1996, 24, 413-426
2. Weinkam, P.; Zong, C. H.; Wolynes, P. G. A funneled energy landscape for cytochrome c directly predicts the sequential folding route inferred from hydrogen exchange experiments Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 12401-12406
3. Babul, J. E. S. Participation of protein ligands in folding of cytochrome c Biochemistry 1972, 11, 1195-1200
4. Privalov, P.; Tsalkova, T. Micro-stabilities and macro-stabilities of globular-proteins Nature 1979, 280, 693-696
5. Northrup, S.; Pear, M.; Mccammon, J.; Karplus, M.; Takano, T. Internal mobility of ferrocytochrome-c Nature 1980, 287, 659-660
6. Roder, H.; Elove, G.; Englander, S. Structural characterization of folding intermediates in cytochrome-c by H-exchange labeling and proton NMR Nature 1988, 335, 700-704
7. Jones, C.; Henry, E.; Hu, Y.; Chan, C.; Luck, S.; Bhuyan, A.; Roder, H.; Hofrichter, J.; Eaton, W. Fast events in protein-folding initiated by nanosecond laser photolysis Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 11860-11864
8. Pascher, T.; Chesick, J. P.; Winkler, J. R.; Gray, H. B. Protein folding triggered by electron transfer Science 1996, 271, 1558-1560
9. 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. U.S.A. 1996, 93, 11615-11617
10. Hagen, S. J.; Hofrichter, J.; Eaton, W. A. Rate of intrachain diffusion of unfolded cytochrome c J. Phys. Chem. B 1997, 101, 2352-2365
11. Chan, C. K.; Hu, Y.; Takahashi, S.; Rousseau, D. L.; Eaton, W. A.; Hofrichter, J. Submillisecond protein folding kinetics studied by ultrarapid mixing Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 1779-1784
12. Pollack, L.; Tate, M. W.; Darnton, N. C.; Knight, J. B.; Gruner, S. M.; Eaton, W. A.; Austin, R. H. Compactness of the denatured state of a fast-folding protein measured by submillisecond small-angle X-ray scattering Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 10115-10117
13. Bai, Y.; Sosnick, T.; Mayne, L.; Englander, S. Protein-folding intermediates-native-state hydrogen-exchange Science 1995, 269, 192-197
14. Maity, H.; Maity, M.; Englander, S. W. How cytochrome c folds, and why: Submolecular foldon units and their stepwise sequential stabilization J. Mol. Biol. 2004, 343, 223-233
15. Panchenko, A. R.; Luthey-Schulten, Z.; Wolynes, P. G. Foldons, protein structural modules, and exons Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 2008-2013
16. Krishna, M. M. G.; Maity, H.; Rumbley, J. N.; Englander, S. W. Branching in the sequential folding pathway of cytochrome c Protein Sci. 2007, 16, 1946-1956
17. Bryngelson, J.; Onuchic, J.; Socci, N.; Wolynes, P. Funnels, pathways, and the energy landscape of protein-folding-a synthesis Proteins: Struct., Funct., Genet. 1995, 21, 167-195
18. Shoemaker, B. A.; Wang, J.; Wolynes, P. G. Structural correlations in protein folding funnels Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 777-782
19. Alm, E.; Baker, D. Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 11305-11310
20. Galzitskaya, O. V.; Finkelstein, A. V. A theoretical search for folding/unfolding nuclei in three-dimensional protein structures Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 11299-11304
21. Munoz, V.; Eaton, W. A. A simple model for calculating the kinetics of protein folding from three-dimensional structures Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 11311-11316
22. Portman, J. J.; Takada, S.; Wolynes, P. G. Variational theory for site resolved protein folding free energy surfaces Phys. Rev. Lett. 1998, 81, 5237-5240
23. Clementi, C.; Nymeyer, H.; Onuchic, J. N. 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. 2000, 298, 937-953
24. Yang, S. C.; Cho, S. S.; Levy, Y.; Cheung, M. S.; Levine, H.; Wolynes, P. G.; Onuchic, J. N. Domain swapping is a consequence of minimal frustration Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 13786-13791
25. Levy, Y.; Cho, S. S.; Shen, T.; Onuchic, J. N.; Wolynes, P. G. Symmetry and frustration in protein energy landscapes: A near degeneracy resolves the Rop dimer-folding mystery Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 2373-2378
26. Ferreiro, D. U.; Cho, S. S.; Komives, E. A.; Wolynes, P. G. The energy landscape of modular repeat proteins: Topology determines folding mechanism in the ankyrin family J. Mol. Biol. 2005, 354, 679-692
27. Cho, S. S.; Weinkam, P.; Wolynes, P. G. Origins of barriers and barrierless folding in BBL Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 118-123
28. Hong, X. L.; Dixon, D. W. NMR-study of the alkaline isomerization of ferricytochrome-c FEBS Lett. 1989, 246, 105-108
29. Rosell, F. I.; Ferrer, J. C.; Mauk, A. G. Proton-linked protein conformational switching: Definition of the alkaline conformational transition of yeast iso-1-ferricytochrome c J. Am. Chem. Soc. 1998, 120, 11234-11245
30. Weinkam, P.; Zimmermann, J.; Sagle, L. B.; Matsuda, S.; Dawson, P. E.; Wolynes, P. G.; Romesberg, F. E. Characterization of alkaline transitions in ferricytochrome c using carbon-deuterium IR probes Biochemistry 2008, 47, 13470-13480
31. Sutto, L.; Latzer, J.; Hegler, J. A.; Ferreiro, D. U.; Wolynes, P. G. Consequences of localized frustration for the folding mechanism of the IM7 protein Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 19825-19830
32. Friedrichs, M.; Wolynes, P. Toward protein tertiary structure recognition by means of associative memory hamiltonians Science 1989, 246, 371-373
33. Papoian, G. A.; Ulander, J.; Eastwood, M. P.; Luthey-Schulten, Z.; Wolynes, P. G. Water in protein structure prediction Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 3352-3357
34. Eastwood, M. P.; Wolynes, P. G. Role of explicitly cooperative interactions in protein folding funnels: A simulation study J. Chem. Phys. 2001, 114, 4702-4716
35. Kolinski, A.; Galazka, W.; Skolnick, J. On the origin of the cooperativity of protein folding: Implications from model simulations Proteins: Struct., Funct., Genet. 1996, 26, 271-287
36. Ejtehadi, M. R.; Avall, S. P.; Plotkin, S. S. Three-body interactions improve the prediction of rate and mechanism in protein folding models Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 15088-15093
37. Gosavi, S.; Chavez, L. L.; Jennings, P. A.; Onuchic, J. N. Topological frustration and the folding of interleukin-1 beta J. Mol. Biol. 2006, 357, 986-996
38. Weinkam, P.; Romesberg, F. E.; Wolynes, P. G. Chemical frustration in the protein folding landscape: Grand canonical ensemble simulations of cytochrome c Biochemistry 2009, 48, 2394-2402
39. Weinkam, P.; Pletneva, E. V.; Gray, H. B.; Winkler, J. R.; Wolynes, P. G. Electrostatic effects on funneled landscapes and structural diversity in denatured protein ensembles Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 1796-1801
40. Robien, M.; Clore, G.; Omichinski, J.; Perham, R.; Appella, E.; Sakaguchi, K.; Gronenborn, A. Three-dimensional solution structure of the E3-binding domain of the dihydrolipoamide succinyl transferase core from the 2-oxoglutarate dehydrogenase multienzyme complex of Escherichia coli Biochemistry 1992, 31, 3463-3471
41. Ferguson, N.; Sharpe, T. D.; Schartau, P. J.; Sato, S.; Allen, M. D.; Johnson, C. M.; Rutherford, T. J.; Fersht, A. R. Ultra-fast barrier-limited folding in the peripheral subunit-binding domain family J. Mol. Biol. 2005, 353, 427-446
42. Sadqi, M.; Fushman, D.; Munoz, V. Atom-by-atom analysis of global downhill protein folding Nature 2006, 442, 317-321
43. Whitford, P. C.; Miyashita, O.; Levy, Y.; Onuchic, J. N. Conformational transitions of adenylate kinase: Switching by cracking J. Mol. Biol. 2007, 366, 1661-1671
44. Englander, S. W.; Sosnick, T. R.; Mayne, L. C.; Shtilerman, M.; Qi, P. X.; Bai, Y. W. Fast and slow folding in cytochrome c Acc. Chem. Res. 1998, 31, 737-744
45. Shastry, M. C. R.; Roder, H. Evidence for barrier-limited protein folding kinetics on the microsecond time scale Nat. Struct. Biol. 1998, 5, 385-392
46. Hagen, S. J.; Eaton, W. A. Two-state expansion and collapse of a polypeptide J. Mol. Biol. 2000, 301, 1019-1027
47. Winkler, J. R. Cytochrome c folding dynamics Curr. Opin. Chem. Biol. 2004, 8, 169-174
48. Banci, L.; Bertini, I.; Bren, K. L.; Gray, H. B.; Turano, P. pH-Dependent equilibria of yeast Met80Ala-iso-1-cytochrome-c probed by NMR-spectroscopy-A comparison with the wild-type protein Chem. Biol. 1995, 2, 377-383
49. Dopner, S.; Hildebrandt, P.; Rosell, F. I.; Mauk, A. G. Alkaline conformational transitions of ferricytochrome c studied by resonance Raman spectroscopy J. Am. Chem. Soc. 1998, 120, 11246-11255
50. Maity, H.; Rumbley, J. N.; Englander, S. W. Functional role of a protein foldon-An Omega-Loop foldon controls the alkaline transition in ferricytochrome c Proteins: Struct. Funct. Bioinf. 2006, 63, 349-355
51. Krishna, M. M. G.; Maity, H.; Rumbley, J. N.; Lin, Y.; Englander, S. W. Order of steps in the cytochrome c folding pathway: Evidence for a sequential stabilization mechanism J. Mol. Biol. 2006, 359, 1410-1419
52. Shastry, M. C. R.; Sauder, J. M.; Roder, H. Kinetic and structural analysis of submillisecond folding events in cytochrome c Acc. Chem. Res. 1998, 31, 717-725