Detection and structure determination of an equilibrium unfolding intermediate of Rd-apocytochrome b562: Native fold with non-native hydrophobic interactions

Journal of Molecular Biology

Volumn 343, Issue 5, 2004, Pages 1477-1485

  Feng, Hanqiao ^a   Vu, Ngoc Diep ^a   Bai, Yawen ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

folding intermediates; folding pathway; hydrophobic repacking; protein structure

Indexed keywords

AMIDE; UREA;

ARTICLE; CONCENTRATION (PARAMETERS); HYDROPHOBICITY; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

EID: 6344291152     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.08.099     Document Type: Article

References (58)

1. Y. Bai, and S.W. Englander Future directions in folding: the multi-state nature of protein structure Proteins: Struct. Funct. Genet. 24 1996 145 151
2. N.D. Vu, H. Feng, and Y. Bai The folding pathway of barnase: the rate-limiting transition state and a hidden intermediate under native conditions Biochemistry 2004
3. P.S. Kim, and R.L. Baldwin Intermediates in the folding of small proteins Annu. Rev. Biochem. 59 1990 631 660
4. C.R. Matthews Pathways of protein folding Annu. Rev. Biochem. 62 1993 653 683
5. J.B. Udgaonkar, and R.L. Baldwin NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A Nature 335 1988 694 699
6. H. Roder, G.A. Elove, and S.W. Englander Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR Nature 335 1988 700 704
7. Y. Bai, T.R. Sosnick, L. Mayne, and S.W. Englander Protein folding intermediates: native-state hydrogen exchange Science 269 1995 192 197
8. A.K. Chamberlain, T.M. Handel, and S. Marqusee Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH Nature Struct. Biol. 3 1996 782 787
9. 2+ binding on the folding kinetics of alpha-lactalbumin J. Mol. Biol. 206 1989 547 561
10. A. Matouschek, J.T. Kellis Jr, L. Serrano, and A.R. Fersht Mapping the transition state and pathway of protein folding by protein engineering Nature 340 1989 122 126
11. T. Kiefhaber, A.M. Labhardt, and R.L. Baldwin Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding ribonuclease A Nature 375 1995 513 515
12. T. Kiefhaber, and R.L. Baldwin Kinetics of hydrogen bond breakage in the process of unfolding of ribonuclease A measured by pulsed hydrogen exchange Proc. Natl Acad. Sci. USA 92 1995 2657 2661
13. S.D. Hoeltzli, and C. Frieden Stopped-flow NMR spectroscopy: real-time unfolding studies of 6-19F- tryptophan-labeled Escherichia coli dihydrofolate reductase Proc. Natl Acad. Sci. USA 92 1995 9318 9322
14. D.V. Laurents, and R.L. Baldwin Characterization of the unfolding pathway of hen egg white lysozyme Biochemistry 36 1997 1496 1504
15. K. Sridevi, and J.B. Udgaonkar Surface expansion is independent of and occurs faster than core solvation during the unfolding of barstar Biochemistry 42 2003 1551 1563
16. M. Roy, and P.A. Jennings Real-time NMR kinetic studies provide global and residue-specific information on the non-cooperative unfolding of the beta-trefoil protein, interleukin-1beta J. Mol. Biol. 328 2003 693 703
17. R.A. Chu, J. Takei, J.R. Knowles, M. Andrykovitch, W. Pei, and A.V. Kajava Redesign of a four-helix bundle protein by phage display coupled with rpoteolysis and strcutural characterization by NMR and X-ray crystallography J. Mol. Biol. 323 2002 253 262
18. H. Feng, and Y. Bai Repacking of hydrophobic residues in a stable mutant of apocytochrome b562 selected by phage-display and proteolysis Proteins: Struct. Funct. Genet. 56 2004 426 429
19. J. Takei, W. Pei, D. Vu, and Y. Bai Populating partially unfolded forms by hydrogen exchange-directed protein engineering Biochemistry 41 2002 12308 12312
20. R.A. Chu, W.H. Pei, J. Takei, and Y. Bai Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein Biochemistry 41 2002 7998 8003
21. H. Feng, J. Takei, R. Lipsitz, N. Tjandra, and Y. Bai Specific non-native hydrophobic interactions in a hidden intermediate: implications for protein folding Biochemistry 42 2003 12461 12465
22. 19F NMR Biochemistry 43 2004 1432 1439
23. F. Arnesano, L. Banci, I. Bertini, D. Koulougliotis, and A. Monti Monitoring mobility in the early steps of unfolding: the case of oxidized cytochrome b(5) in the presence of 2 M guanidinium chloride Biochemistry 39 2000 7117 7130
24. J. Dunbar, H.P. Yennawar, S. Banerjee, J. Luo, and G.K. Farber The effect of denaturants on protein structure Protein Sci. 6 1997 1727 1733
25. C.R. Matthews, and M.R. Hurle Mutant sequences as probes of protein folding mechanisms BioEssays 6 1987 254 257
26. L. Hoang, S. Bedard, M.M.G. Krishna, Y. Lin, and S.W. Englander Cytochrome c folding pathway: kinetic native-state hydrogen exchange Proc. Natl Acad. Sci. USA 99 2002 12173 12178
27. A.R. Fersht A kinetically significant intermediate in the folding of barnase Proc. Natl Acad. Sci. USA 97 2000 14121 14126
28. D. Vu, H. Feng, and Y. Bai The folding pathway of barnase: the rate-limiting transition state and a hidden intermediates under native conditions Biochemistry 42 2004 3346 3356
29. R.L. Baldwin The nature of protein folding pathways: the classical versus the new view J. Biol. NMR 5 1995 103 109
30. P.S. Kim, and R.L. Baldwin Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding Annu. Rev. Biochem. 51 1982 459 489
31. A.R. Fersht, A. Matouschek, and L. Serrano The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding J. Mol. Biol. 224 1992 771 782
32. A. Sali, E. Shakhnovich, and M. Karplus How does a protein fold? Nature 369 1994 248 251
33. J.D. Brygelson, J.N. Onuchic, N.D. Socci, and P.G. Wolynes Funnels, pathways, and energy landscape of protein folding: a synthesis Proteins: Struct. Funct. Genet. 21 1995 167 195
34. K.A. Dill, and H.S. Chan From Levinthal to pathways to funnels Nature Struct. Biol. 4 1997 10 19
35. J.N. Onuchic, N.D. Socci, Z. Luthey-Schulten, and P.G. Wolynes Protein folding funnels: the nature of the transition state ensemble Fold. Des. 1 1996 441 450
36. J. Onuchic, and P.G. Wolynes Theory of protein folding Curr. Opin. Struct. Biol. 14 2004 70 75
37. H. Kaya, and H.S. Chan Polymer principles of protein calorimetric two-state cooperativity Proteins: Struct. Funct. Genet. 40 2000 637 661
38. H. Kaya, and H.S. Chan Toward a consistent modeling of protein thermodynamic and kinetic cooperativity: how applicable is the transition state picture to folding and unfolding? J. Mol. Biol. 315 2002 899 909
39. H. Kaya, and H.S. Chan Contact order dependent protein folding rates: kinetic consequences of a cooperative interplay between favorable nonlocal interactions and local conformational preferences Proteins. 52 2003 524 533
40. H. Kaya, and H.S. Chan Simple two-state protein folding kinetics requires near-Levinthal thermodynamic cooperativity Proteins: Struct. Funct. Genet. 52 2003 510 523
41. H.S. Chan, S. Shimizu, and H. Kaya Cooperativity principles in protein folding Methods Enzymol. 380 2004 350 379
42. S.W. Englander Protein folding intermediates and pathways studied by hydrogen exchange Annu. Rev. Biophys. Biomol. Struct. 29 2000 213 238
43. M. Scalley-Kim, and D. Baker Characterization of the folding energy landscapes of computer generated proteins suggests high folding free energy barriers and cooperativity may be consequences of natural selection J. Mol. Biol. 338 2004 573 583
44. R.L. Baldwin The problem was to find the problem Protein Sci. 6 1997 2031 2034
45. W.F. DeGrado, C.M. Summa, V. Pavone, F. Nastri, and A. Lombardi De novo design and structural characterization of proteins and mettalloproteins Annu. Rev. Biochem. 68 1999 779 819
46. S.T. Walsh, H. Cheng, J.W. Bryson, H. Roder, and W.F. DeGrado Solution structure and dynamics of a de novo designed three-helix bundle protein Proc. Natl Acad. Sci. USA 96 1999 5486 5491
47. S.M. Malakauskas, and S.L. Mayo Design, structure and stability of a hyperthermophilic protein variant Nature Struct. Biol. 5 1998 470 475
48. 2H NMR relaxation methods Biochemistry 40 2001 9560 9569
49. Y. Bai, and H. Feng Selection of stably folded proteins by phage-display with proteolysis Eur. J. Biochem. 271 2004 1609 1614
50. S. Nauli, B. Kuhlman, I.L. Trong, R.E. Stenkamp, D. Teller, and D. Baker Crystal structures and increased stabilization of the protein G variants with switched folding pathways NuG1 and NuG2 Protein Sci. 11 2002 2924 2931
51. B. Kuhlman, G. Dantas, G. Ireton, G. Varani, B. Stoddard, and D. Baker Design of a novel globular protein fold with atomic level accuracy Science 302 2003 1364 1368
52. B. Gillespie, D.M. Vu, P.S. Shah, S.A. Marshall, R.B. Dyer, S.L. Mayo, and K.W. Plaxco NMR and temperature-jump measurements of de novo designed proteins demonstrate rapid folding in the absent of explicit selection for kinetics J. Mol. Biol. 330 2003 813 819
53. V. Daggett, and A.R. Fersht Is there a unifying mechanism for protein folding Trends Biochem. Sci. 28 2003 18 25
54. R. Day, and V. Daggett All atom simulation of protein folding and unfolding Advan. Protein Chem. 66 2003 373 403
55. 15N-enriched proteins J. Am. Chem. Soc. 115 1993 7772 7777
56. F. Delaglio, S. Grzesiek, G. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multi-dimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
57. B.A. Johnson, and R.A. Blevins NMRView: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
58. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallog. 26 1993 283 291