Folding energy landscape of cytochrome cb562

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 19, 2009, Pages 7834-7839

  Kimura, Tetsunari ^a   Lee, Jennifer C ^a,b   Gray, Harry B ^a   Winkler, Jay R ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Four helix bundle; Minimal frustration; Protein folding; Time resolved fluorescence energy transfer; Tryptophan

Indexed keywords

APOPROTEIN; CYTOCHROME; CYTOCHROME CB562; HEMOPROTEIN; POLYPEPTIDE; PORPHYRIN; UNCLASSIFIED DRUG;

ARTICLE; ENERGY TRANSFER; ESCHERICHIA COLI; EVOLUTION; FLUORESCENCE ANALYSIS; MIXER; MOLECULAR MECHANICS; NONHUMAN; POPULATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; TIME RESOLVED FLUORESCENCE ENERGY TRANSFER;

BIOCHEMISTRY; CYTOCHROME B GROUP; DATABASES, PROTEIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GUANIDINE; HEME; KINETICS; MODELS, STATISTICAL; MOLECULAR CONFORMATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

ESCHERICHIA COLI;

EID: 66049112399     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902562106     Document Type: Article

References (58)

1. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG (1995) Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins 21:167-195.
2. Dill KA, Chan HS (1997) From Levinthal to pathways to funnels. Nat Struct Biol 4:10-19. (Pubitemid 27020916)
3. Onuchic JN, LutheySchulten Z, Wolynes PG (1997) Theory of protein folding: The energy landscape perspective. Annu Rev Phys Chem 48:545-600.
4. Onuchic JN, Wolynes PG (2004) Theory of protein folding. Curr Opin Struct Biol 14:70-75. (Pubitemid 38249595)
5. Plotkin SS, Onuchic JN (2002) Understanding protein folding with energy landscape theory. Part I. Basic concepts. Q Rev Biophys 35:111-167.
6. Plotkin SS, Onuchic JN (2002) Understanding protein folding with energy landscape theory. Part II. Quantitative aspects. Q Rev Biophys 35:205-286.
7. Portman JJ, Takada S, Wolynes PG (2001) Microscopic theory of protein folding rates. I. Fine structure of the free energy profile and folding routes from a variational approach. J Chem Phys 114:5069-5081.
8. Portman JJ, Takada S, Wolynes PG (2001) Microscopic theory of protein folding rates. II. Local reaction coordinates and chain dynamics. J Chem Phys 114:5082-5096.
9. Wain R, et al. (2001) The cytochrome c fold can be attained from a compact apo state by occupancy of a nascent heme binding site. J Biol Chem 276:45813-45817.
10. Borgia A, Gianni S, Brunori M, Travaglini-Allocatelli C (2008) Fast folding kinetics and stabilization of apocytochrome c. FEBS Lett 582:1003-1007.
11. Moore CD, Lecomte JTJ (1990) Structural properties of apocytochrome b5: Presence of a stable native core. Biochemistry 29:1984-1989.
12. 5 and apocytochrome b5: NMR studies of the histidine residues. Biochemistry 30:8357-8365.
13. Fersht AR, Matouschek A, Serrano L (1992) The folding of an enzyme. 1. Theory of protein engineering analysis of stability and pathway of protein folding. J Mol Biol 224:771-782.
14. 562. J Mol Biol 346:331-344.
15. 562 examined by the dependence of hydrogen exchange on hydrostatic pressure. Biochemistry 37:9877-9883.
16. 5 using equilibrium and kinetic fluorescence measurements. Biochemistry 38:9533-9540.
17. Feng HQ, Takei J, Lipsitz R, Tjandra N, Bai YW (2003) Specific nonnative hydrophobic interactions in a hidden folding intermediate: Implications for protein folding. Biochemistry 42:12461-12465.
18. Feng HQ, Vu ND, Zhou Z, Bai YW (2004) Structural examination of -value analysis in protein folding. Biochemistry 43:14325-14331. (Pubitemid 39491966)
19. 562. J Am Chem Soc 127:5066-5072.
20. Feng H, Zhou Z, Bai Y (2005) A protein folding pathway with multiple folding intermediates at atomic resolution. Proc Natl Acad Sci USA 102:5026-5031. (Pubitemid 40503733)
21. 562 characterized by protein engineering. J Mol Biol 352:757-764.
22. 562 by protein engineering and infrared T-jump. Protein Sci 16:1176-1183.
23. 5. Biochemistry 45:13750-13759.
24. 562 folding triggered by electron transfer: Approaching the speed limit for formation of a four-helix bundle protein. Proc Natl Acad Sci USA 96:6587-6590.
25. Faraone-Mennella J, Gray HB, Winkler JR (2005) Early events in the folding of four-helix bundle heme proteins. Proc Natl Acad Sci USA 102:6315-6319. (Pubitemid 40617440)
26. 562. Biochemistry 45:10504-10511.
27. Lee JC, Gray HB, Winkler JR (2001) cytochrome c′ folding triggered by electron transfer: Fast and slow formation of four-helix bundles. Proc Natl Acad Sci USA 98:7760-7764.
28. Lee JC, Engman KC, Tezcan FA, Gray HB, Winkler JR (2002) Structural features of cytochrome c′ folding intermediates revealed by fluorescence energy-transfer kinetics. Proc Natl Acad Sci USA 99:14778-14782. (Pubitemid 35334560)
29. Kimura T, Lee JC, Gray HB, Winkler JR (2007) Site-specific collapse dynamics guide the formation of the cytochrome c′ four-helix bundle. Proc Natl Acad Sci USA 104:117-122. (Pubitemid 46067994)
30. Pletneva EV, et al. (2007) Probing the cytochrome c′ folding landscape. J Inorg Biochem 101:1768-1775.
31. Hill EE, Morea V, Chothia C (2002) Sequence conservation in families whose members have little or no sequence similarity: The four-helical cytokines and cytochromes. J Mol Biol 322:205-233.
32. Shibata N, et al. (1998) Basis for monomer stabilization in Rhodopseudomonas palustris cytochrome c′ derived from the crystal structure. J Mol Biol 284:751-760.
33. 556. J Biol Inorg Chem 9:224-230.
34. 562. Biochemistry 39:1499-1514.
35. Lyubovitsky JG, Gray HB, Winkler JR (2002) Structural features of the cytochrome c molten globule revealed by fluorescence energy transfer kinetics. J Am Chem Soc 124:14840-14841. (Pubitemid 36014080)
36. Lyubovitsky JG, Gray HB, Winkler JR (2002) Mapping the cytochrome c folding landscape. J Am Chem Soc 124:5481-5485. (Pubitemid 34506946)
37. Pletneva EV, Gray HB, Winkler JR (2005) Snapshots of cytochrome c folding. Proc Natl Acad Sci USA 102:18397-18402. (Pubitemid 43011237)
38. Pletneva EV, Gray HB, Winkler JR (2005) Nature of the cytochrome c molten globule. J Am Chem Soc 127:15370-15371. (Pubitemid 41572501)
39. Pletneva EV, Gray HB, Winkler JR (2005) Many faces of the unfolded state: Conformational heterogeneity in denatured yeast cytochrome c. J Mol Biol 345:855-867.
40. Akiyama S, et al. (2002) Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle X-ray scattering. Proc Natl Acad Sci USA 99:1329-1334.
41. Kimura T, et al. (2005) Specific collapse followed by slow hydrogen bond formation of β-sheet in the folding of single-chain monellin. Proc Natl Acad Sci USA 102:2748-2753.
42. Chu RA, Pei WH, Takei J, Bai YW (2002) Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry 41:7998-8003. (Pubitemid 34655166)
43. Cranz-Mileva S, Friel CT, Radford SE (2005) Helix stability and hydrophobicity in the folding mechanism of the bacterial immunity protein Im9. Protein Eng Des Sel 18:41-50. (Pubitemid 40516990)
44. Gsponer J, et al. (2006) Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7. Proc Natl Acad Sci USA 103:99-104.
45. Le Duff CS, Whittaker SB, Radford SE, Moore GR (2006) Characterisation of the conformational properties of urea-unfolded Im7: Implications for the early stages of protein folding. J Mol Biol 364:824-835.
46. Ferreiro DU, Hegler JA, Komives EA, Wolynes PG (2007) Localizing frustration in native proteins and protein assemblies. Proc Natl Acad Sci USA 104:19819-19824.
47. Sutto L, Latzer J, Hegler JA, Ferreiro DU, Wolynes PG (2007) Consequences of localized frustration for the folding mechanism of the IM7 protein. Proc Natl Acad Sci USA 104:19825-19830.
48. Nozaki Y (1972) The preparation of guanidine hydrochloride. Methods Enzymol 26:43-50.
49. Lee JC, Langen R, Hummel PA, Gray HB, Winkler JR (2004) α-Synuclein structures from fluorescence energy-transfer kinetics: Implications for the role of the protein in Parkinson's disease. Proc Natl Acad Sci USA 101:16466-16471.
50. Beals JM, Haas E, Krausz S, Scheraga HA (1991) Conformational studies of a peptide corresponding to a region of the C terminus of ribonuclease A: Implications as a potential chain-folding initiation site. Biochemistry 30:7680-7692.
51. Beechem JM, Haas E (1989) Simultaneous determination of intramolecular distance distributions and conformational dynamics by global analysis of energy transfer measurements. Biophys J 55:1225-1236.
52. Istratov AA, Vyvenko OF (1999) Exponential analysis in physical phenomena. Rev Sci Instr 70:1233-1257. (Pubitemid 129576178)
53. Livesey AK, Delaye M, Licinio P, Brochon JC (1987) Maximum-entropy analysis of dynamic parameters via the Laplace transform. Faraday Disc 83:247-258.
54. Lawson CL, Hanson RJ (1974) Solving Least Squares Problems (Prentice-Hall, Englewood Cliffs, NJ).
55. Förster T (1948) Ann Phys 2:55-75.
56. Wu P, Brand L (1994) Resonance energy transfer: Methods and applications. Anal Biochem 218:1-13.
57. Jordanides XJ, Scholes GD, Shapley WA, Reimers JR, Fleming GR (2004) Electronic couplings and energy transfer dynamics in the oxidized primary electron donor of the bacterial reaction center. J Phys Chem B 108:1753-1765.
58. Scholes GD, Jordanides XJ, Fleming GR (2001) Adapting the Förster theory of energy transfer for modeling dynamics in aggregated molecular assemblies. J Phys Chem B 105:1640-1651. (Pubitemid 33764169)