The Folding Pathway of T4 Lysozyme: An On-pathway Hidden Folding Intermediate

Journal of Molecular Biology

Volumn 365, Issue 3, 2007, Pages 881-891

  Kato, Hidenori ^a   Vu, Ngoc Diep ^a   Feng, Hanqiao ^a   Zhou, Zheng ^a   Bai, Yawen ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

hidden intermediate; hydrogen exchange; protein engineering; protein folding; T4 lysozyme

Indexed keywords

HYDROGEN; LYSOZYME; T4 LYSOZYME; UNCLASSIFIED DRUG;

ARTICLE; ENERGY; ENZYME STRUCTURE; KINETICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS;

EID: 33845796109     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.048     Document Type: Article

References (49)

1. Baldwin R.L., and Roder H. Characterizing protein folding intermediates. Curr. Biol. 1 (1991) 218-220
2. Englander S.W., and Mayne L. Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR. Annu. Rev. Biophys. Biomol. Struct. 21 (1992) 243-265
3. Englander S.W. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29 (2000) 213-238
4. Krishna M.M., Hoang L., Lin Y., and Englander S.W. Hydrogen exchange methods to study protein folding. Methods 34 (2004) 51-64
5. Roder H., Elove G.A., and Englander S.W. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335 (1988) 700-704
6. Udgaonkar J.B., and Baldwin R.L. NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 335 (1988) 694-699
7. Miranker A., Robinson C.V., Radford S.E., Aplin R.T., and Dobson C.M. Detection of transient protein folding populations by mass spectrometry. Science 262 (1993) 896-900
8. Jennings P.A., and Wright P.E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262 (1993) 892-896
9. Raschke T.M., and Marqusee S. The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions. Nature Struct. Biol. 4 (1997) 298-304
10. Bai Y., Sosnick T.R., Mayne L., and Englander S.W. Protein folding intermediates: native-state hydrogen exchange. Science 269 (1995) 192-197
11. Chamberlain A.K., Handel T.M., and Marqusee S. Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH. Nature Struct. Biol. 3 (1996) 782-787
12. Llinas M., Gillespie B., Dahlquist F.W., and Marqusee S. The energetics of T4 lysozyme reveal a hierarchy of conformations. Nature Struct. Biol. 6 (1999) 1072-1078
13. Yan S., Kennedy S.D., and Koide S. Thermodynamic and kinetic exploration of the energy landscape of Borrelia burgdorferi OspA by native-state hydrogen exchange. J. Mol. Biol. 323 (2002) 363-375
14. Silverman J.A., and Harbury P.B. The equilibrium unfolding pathway of a beta/alpha8 barrel. J. Mol. Biol. 324 (2002) 1031-1040
15. Lu J., and Dahlquist F.W. Detection and characterization of an early folding intermediate of T4 lysozyme using pulsed hydrogen exchange and two-dimensional NMR. Biochemistry 31 (1992) 4749-4756
16. Bai Y. Kinetic evidence for an on-pathway intermediate in the folding of cytochrome c. Proc. Natl Acad. Sci. USA 96 (1999) 477-480
17. Heidary D.K., O'Neill Jr. J.C., Roy M., and Jennings P.A. An essential intermediate in the folding of dihydrofolate reductase. Proc. Natl Acad. Sci. USA 97 (2000) 5866-5870
18. Capaldi A.P., Shastry M.C., Kleanthous C., Roder H., and Radford S.E. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nature Struct. Biol. 8 (2001) 68-72
19. Takei J., Pei W., Vu D., and Bai Y. Populating partially unfolded forms by hydrogen exchange-directed protein engineering. Biochemistry 41 (2002) 12308-12312
20. Krantz B.A., Mayne L., Rumbley J., Englander S.W., and Sosnick T.R. Fast and slow intermediate accumulation and the initial barrier mechanism in protein folding. J. Mol. Biol. 324 (2002) 359-371
21. Chu R.A., Takei J., Barchi Jr. J.J., and Bai Y. Relationship between the native-state hydrogen exchange and the folding pathways of barnase. Biochemistry 38 (1999) 14119-14124
22. Silow M., and Oliveberg M. Transient aggregates in protein folding are easily mistaken for folding intermediates. Proc. Natl Acad. Sci. USA 94 (1997) 6084-6086
23. Nawrocki J.P., Chu R.A., Pannell L.K., and Bai Y. Intermolecular aggregations are responsible for the slow kinetics observed in the folding of cytochrome c at neutral pH. J. Mol. Biol. 293 (1999) 991-995
24. Gassner N.C., Baase W.A., Lindstrom J.D., Lu J., Dahlquist F.W., and Matthews B.W. Methionine and alanine substitutions show that the formation of wild-type-like structure in the carboxy-terminal domain of T4 lysozyme is a rate-limiting step in folding. Biochemistry 38 (1999) 14451-14460
25. Roder H., and Wuthrich K. Protein folding kinetics by combined use of rapid mixing techniques and NMR observation of individual amide protons. Proteins: Struct. Funct. Genet. 1 (1986) 34-42
26. Takei J., Chu R.A., and Bai Y. Absence of stable intermediates on the folding pathway of barnase. Proc. Natl Acad. Sci. USA 97 (2000) 10796-10801
27. Bai Y., Milne J.S., Mayne L., and Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17 (1993) 75-86
28. Silow M., and Oliveberg M. High-energy channeling in protein folding. Biochemistry 36 (1997) 7633-7637
29. Chan H.S., Shimizu S., and Kaya H. Cooperativity principles in protein folding. Methods Enzymol. 380 (2004) 350-379
30. Bai Y. Energy barriers, cooperativity, and hidden intermediates in the folding of small proteins. Biochem. Biophys. Res. Commun. 340 (2006) 976-983
31. Hvidt A., and Nielsen S.O. Hydrogen exchange in proteins. Advan. Protein Chem. 21 (1966) 287-386
32. Zhou Z., Huang Y., and Bai Y. An on-pathway hidden intermediate and the early rate-limiting transition state of Rd-apocytochrome b562 characterized by protein engineering. J. Mol. Biol. 352 (2005) 757-764
33. Kim P.S., and Baldwin R.L. Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding. Annu. Rev. Biochem. 51 (1982) 459-489
34. Matthews C.R. Pathways of protein folding. Annu. Rev. Biochem. 62 (1993) 653-683
35. Kiefhaber T., and Baldwin R.L. 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
36. Hoeltzli S.D., and Frieden C. 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
37. Kiefhaber T., Bachmann A., Wildegger G., and Wagner C. Direct measurement of nucleation and growth rates in lysozyme folding. Biochemistry 36 (1997) 5108-5112
38. Roy M., and Jennings P.A. 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
39. Sosnick T.R., Mayne L., and Englander S.W. Molecular collapse: the rate-limiting step in two-state cytochrome c folding. Proteins: Struct. Funct. Genet. 24 (1996) 413-426
40. Bai Y., and Englander S.W. Future directions in folding: the multi-state nature of protein structure. Proteins: Struct. Funct. Genet. 24 (1996) 145-151
41. Chu R., Pei W., Takei J., and Bai Y. Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry 41 (2002) 7998-8003
42. Feng H., Vu N.D., and Bai Y. Detection of a hidden folding intermediate of the third domain of PDZ. J. Mol. Biol. 346 (2005) 345-353
43. Fersht A.R. A kinetically significant intermediate in the folding of barnase. Proc. Natl Acad. Sci. USA 97 (2000) 14121-14126
44. Vu N.D., Feng H., and Bai Y. The folding pathway of barnase: the rate-limiting transition state and a hidden intermediate under native conditions. Biochemistry 43 (2004) 3346-3356
45. Llinas M., and Marqusee S. Subdomain interactions as a determinant in the folding and stability of T4 lysozyme. Protein Sci. 7 (1998) 96-104
46. Levinthal C. Are there pathways for protein folding?. J. Chim. Phys. 65 (1968) 44-45
47. Wetlaufer D.B. Nucleation, rapid folding, and globular intrachain regions in proteins. Proc. Natl Acad. Sci. USA 70 (1973) 697-701
48. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
49. Johnson B.A., and Blevins R.A. NMRView: a computer program for the visulization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614