Snapshots of a protein folding intermediate

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

Volumn 110, Issue 5, 2013, Pages 1606-1610

  Yamada, Seiji ^a,b   Ford, Nicole D Bouley ^a   Keller, Gretchen E ^a   Ford, William C ^a   Gray, Harry B ^a   Winkler, Jay R ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b SONY CORPORATION   (Japan)

Author keywords

FRET; Microfluidic mixing; Protein refolding

Indexed keywords

CYTOCHROME C; CYTOCHROME C552; FLUORESCENT DYE; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMUS THERMOPHILUS;

BACTERIAL PROTEINS; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; CYTOCHROME C GROUP; HEME; KINETICS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; SPECTROMETRY, FLUORESCENCE; THERMUS THERMOPHILUS; TIME FACTORS;

EID: 84873165207     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1221832110     Document Type: Article

References (32)

1. Gomes CM, Wittung-Stafshede P (2011) Protein Folding and Metal Ions: Mechanisms, Biology and Disease (CRC, New York).
2. Prusiner SB (1998) Prions. Proc Natl Acad Sci USA 95(23):13363-13383. (Pubitemid 28525623)
3. Lacor PN, et al. (2004) Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 24(45):10191-10200. (Pubitemid 39492046)
4. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG (1995) Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins 21(3):167-195.
5. Onuchic JN, Luthey-Schulten Z, Wolynes PG (1997) Theory of protein folding: The energy landscape perspective. Annu Rev Phys Chem 48:545-600. (Pubitemid 127443918)
6. Oliveberg M, Wolynes PG (2005) The experimental survey of protein-folding energy landscapes. Q Rev Biophys 38(3):245-288. (Pubitemid 44268537)
7. Pletneva EV, Gray HB, Winkler JR (2005) Snapshots of cytochrome c folding. Proc Natl Acad Sci USA 102(51):18397-18402. (Pubitemid 43011237)
8. Pletneva EV, Gray HB, Winkler JR (2005) Many faces of the unfolded state: Conformational heterogeneity in denatured yeast cytochrome C. J Mol Biol 345(4):855-867. (Pubitemid 39600938)
9. Faraone-Mennella J, Gray HB, Winkler JR (2005) Early events in the folding of fourhelix-bundle heme proteins. Proc Natl Acad Sci USA 102(18):6315-6319. (Pubitemid 40617440)
10. Faraone-Mennella J, Tezcan FA, Gray HB, Winkler JR (2006) Stability and folding kinetics of structurally characterized cytochrome c-b562. Biochemistry 45(35):10504-10511. (Pubitemid 44320466)
11. 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(1):117-122. (Pubitemid 46067994)
12. Kimura T, Lee JC, Gray HB, Winkler JR (2009) Folding energy landscape of cytochrome cb562. Proc Natl Acad Sci USA 106(19):7834-7839.
13. Ivarsson Y, et al. (2007) An on-pathway intermediate in the folding of a PDZ domain. J Biol Chem 282(12):8568-8572. (Pubitemid 47093476)
14. Hon-Nami K, Oshima T (1977) Purification and some properties of cytochrome c-552 from an extreme thermophile, Thermus thermophilus HB8. J Biochem 82(3):769-776. (Pubitemid 8184272)
15. Hon-nami K, Oshima T (1979) Denaturation of thermophilic ferricytochrome c-552 by acid, guanidine hydrochloride, and heat. Biochemistry 18(25):5693-5697.
16. Than ME, et al. (1997) Thermus thermophilus cytochrome-c552: A new highly thermostable cytochrome-c structure obtained by MAD phasing. J Mol Biol 271(4):629-644. (Pubitemid 27373094)
17. Muresanu L, et al. (2006) The electron transfer complex between cytochrome c552 and the CuA domain of the Thermus thermophilus ba3 oxidase. A combined NMR and computational approach. J Biol Chem 281(20):14503-14513. (Pubitemid 43848381)
18. Travaglini-Allocatelli C, et al. (2003) Exploring the cytochrome c folding mechanism: Cytochrome c552 from thermus thermophilus folds through an on-pathway intermediate. J Biol Chem 278(42):41136-41140. (Pubitemid 37280938)
19. Clementi C, Nymeyer H, Onuchic JN (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(5):937-953.
20. Weinkam P, Pletneva EV, Gray HB, Winkler JR, Wolynes PG (2009) Electrostatic effects on funneled landscapes and structural diversity in denatured protein ensembles. Proc Natl Acad Sci USA 106(6):1796-1801.
21. Fee JA, et al. (2000) Integrity of thermus thermophilus cytochrome c552 synthesized by Escherichia coli cells expressing the host-specific cytochrome c maturation genes, ccmABCDEFGH: Biochemical, spectral, and structural characterization of the recombinant protein. Protein Sci 9(11):2074-2084. (Pubitemid 32104144)
22. Pace NC, Shirley BA, Thomson TF (1990) Protein Structure: A Practical Approach (IRL, Oxford), pp 311-330.
23. Ibrahim SM, et al. (2011) Cytochrome c552 from Thermus thermophilus engineered for facile substitution of prosthetic group. Biochemistry 50(45):9826-9835.
24. 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(49):45813-45817.
25. Shastry M C R, Sauder JM, Roder H (1998) Kinetic and structural analysis of submillisecond folding events in cytochrome c. Acc Chem Res 31(11):717-725. (Pubitemid 128474538)
26. Nozaki Y (1972) The preparation of guanidine hydrochloride. Methods Enzymol 26:43-50.
27. 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(31):7680-7692.
28. Beechem JM, Haas E (1989) Simultaneous determination of intramolecular distance distributions and conformational dynamics by global analysis of energy transfer measurements. Biophys J 55(6):1225-1236.
29. Lawson CL, Hanson RJ (1974) Solving Least Squares Problems (Prentice-Hall, Englewood Cliffs, NJ).
30. Wu P, Brand L (1994) Resonance energy transfer: Methods and applications. Anal Biochem 218(1):1-13. (Pubitemid 24124740)
31. 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(5):1753-1765.
32. Scholes GD, Jordanides XJ, Fleming GR (2001) Adapting the Forster theory of energy transfer for modeling dynamics in aggregated molecular assemblies. J Phys Chem B 105(8):1640-1651.