Monitoring protein folding at atomic resolution

Accounts of Chemical Research

Volumn 37, Issue 12, 2004, Pages 929-936

  Kumar, Thallapuranam Krishnaswamy S ^a,d   Yu, Chin ^a,b,c  

^a UNIVERSITY OF ARKANSAS   (United States)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^d OSMANIA UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

BINDING KINETICS; EQUILIBRIUM CONSTANT; MOLECULAR MECHANICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPTICAL RESOLUTION; PROTEIN CONFORMATION; PROTEIN FOLDING; REACTION ANALYSIS; REVIEW; SPECIES IDENTIFICATION; STRUCTURE ANALYSIS;

APOPROTEINS; FIBROBLAST GROWTH FACTOR 1; HYDROGEN; KINETICS; MYOGLOBIN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEINS;

EID: 11244260589     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar020156z     Document Type: Review

References (52)

1. Gunasekaran, K.; Eyles, S. J.; Hagler, A. T.; Gierasch, L. M. Keeping it in the family: Folding studies of related proteins. Curr. Opin. Struct. Biol. 2001, 11, 83-93.
2. Bilsel, O.; Matthews, C. R. Barriers in protein folding reactions. Adv. Protein Chem. 2000, 53, 153-207.
3. Dobson, C. M. Protein folding and misfolding. Nature 2003, 426, 884-890.
4. Dyson, H. J.; Wright, P. E. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 2002, 12, 54-60.
5. Daggett, V.; Fersht, A. R. Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 2003, 28, 18-25.
6. Weikl, T. R.; Palassini, M.; Dill, K. A. Cooperativity in two-state protein folding kinetics. Protein Sci. 2004, 13, 822-829.
7. Vendruscolo, M.; Paci, E.; Karplus, M.; Dobson, C. M. Structures and relative free energies of partially folded states of proteins. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 14817-14821.
8. Arai, M.; Kuwajima, K. Role of the molten globule state in protein folding. Adv. Protein Chem. 2000, 53, 209-282.
9. Samuel, D.; Kumar, T. K.; Srimathi, T.; Hsieh, H.; Yu, C. Identification and characterization of an equilibrium intermediate in the unfolding pathway of an all β-barrel protein. J. Biol. Chem. 2000, 275, 34968-34975.
10. Redfield, C. Using nuclear magnetic resonance spectroscopy to study molten globules of proteins. Methods 2004, 34, 121-132.
11. Schulman, B. A.; Kim, P. S.; Dobson, C. M.; Redfield, C. A residue-specific NMR view of the non-cooperative unfolding of a molten globule. Nat. Struct. Biol. 2000, 4, 630-634.
12. Eliezer, D.; Chung, J.; Dyson, H. J.; Wright, P. E. Native and non-native secondary structure and dynamics in the pH 4 intermediate of apomyoglobin. Biochemistry 2000, 39, 2894-2901.
13. Srimathi, T.; Kumar, T. K.; Chi, Y. H.; Chiu, I. M.; Yu, C. Characterization of the structure and dynamics of a near-native equilibrium intermediate in the unfolding pathway of an all β-barrel protein. J. Biol. Chem. 2002, 277, 47507-47516.
14. Maity, H.; Lim, W. K.; Rumbley, J. N.; Englander, S. W. Protein hydrogen exchange mechanism: Local fluctuations. Protein Sci. 2003, 12, 153-160.
15. Englander, S. VV. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 213-238.
16. Huyghues-Despointes, B. M.; Pace, C. N.; Englander, S. W.; Scholtz, J. M. Measuring the conformational stability of a protein by hydrogen exchange. Methods Mol. Biol. 2001, 168, 69-92.
17. Lacroix, E.; Bruix, M.; Lopez-Hernandez, E.; Serrano, L.; Rico, M. Amide hydrogen exchange and internal dynamics in the chemotactic protein CheY from Escherichia coli. J. Mol. Biol. 1997, 271, 472-487.
18. Chi, Y. H.; Kumar, T. K.; Kathir, K. M.; Lin, D. H.; Zhu, G.; Chiu, I. M.; Yu, C. Investigation of the structural stability of the human acidic fibroblast growth factor by hydrogen-deuterium exchange. Biochemistry 2002, 41, 15350-15359.
19. Li, R.; Woodward, C. The hydrogen exchange core and protein folding. Protein Sci. 8, 1999, 1571-1590.
20. Sivaraman, T.; Kumar, T. K.; Yu, C. Investigation of the structural stability of carciotoxin analogue III from the Taiwan cobra by hydrogen-deuterium exchange kinetics. Biochemistry 1999, 38, 9899-9905.
21. Clarke, J.; Itzhaki, L. S.; Fersht, A. R. Hydrogen exchange at equilibrium: A short cut for analysing protein-folding pathways? Trends Biochem. Sci. 1997, 22, 284-287.
22. Bai, Y.; Sosnick, T. R.; Mayne, L.; Englander, S. W. Protein folding intermediates: Native-state hydrogen exchange. Science 1995, 269, 192-197.
23. Mayo, S. L.; Baldwin, R. L. Guanidinium chloride induction of partial unfolding in amide proton exchange in RNase A. Science 1993, 262, 873-876.
24. Chi, Y. H.; Kumar, T. K.; Chiu, I. M.; Yu, C. Identification of rare partially unfolded states in equilibrium with the native conformation in an all β-barrel protein. J. Biol. Chem. 2002, 277, 34941-34948.
25. Chu, R.; Pei, W.; Takei, J.; Bai, Y. Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry 2002, 41, 7998-8003.
26. Bai, Y. Hidden intermediates and Levinthal paradox in the folding of small proteins. Biochem. Biophys. Res. Commun. 2003, 305, 785-788.
27. Fersht, A. R. A kinetically significant intermediate in the folding of barnase. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 14121-14126.
28. Schwarzinger, S.; Wright, P. E.; Dyson, H. J. Molecular hinges in protein folding: The urea-denatured state of apomyoglobin. Biochemistry 2002, 41, 12681-12686.
29. Dyson, H. J.; Wright, P. E. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv. Protein Chem. 2002, 62, 311-340.
30. Mayor, U.; Grossman, J. G.; Foster, N. W.; Freund, S. M.; Fersht, A. R. The denatured state of engrailed homeodomain under denaturing and native conditions. J. Mol. Biol. 2003, 333, 977-991.
31. Crowhurst, K. A.; Forman-Kay, J. D. Aromatic and methyl NOEs highlight hydrophobic clustering in the unfolded state of an SH3 domain. Biochemistry 2003, 42, 8687-8695.
32. Chi, Y.; Kumar, T. K.; Wang, H. M.; Ho, M. C.; Chiu, I. M.; Yu, C. Thermodynamic characterization of the human acidic fibroblast growth factor: Evidence for cold denaturation. Biochemistry 2001, 40, 7746-7753.
33. Fieber, W.; Kristjansdottir, S.; Poulsen, F. M. Short range, long range, and transition state interactions in the denatured state of ACBP from residual dipolar couplings. J. Mol. Biol. 2004, 339, 1191-1199.
34. Mohana-Borgs, R.; Goto, N. K.; Kroon, G. A.; Dyson, H. J.; Wright, P. E. Structural characterization of the unfolded states of apomyoglobin using residual dipolar couplings. J. Mol. Biol. 2004, 340, 1131-1142.
35. Ackerman, M. S.; Shortle, D. Molecular alignment of denatured states of staphylococcal nuclease with strained polyacrylamide gels and surfactant liquid crystalline phases. Biochemistry 2002, 41, 3089-3095.
36. Lietzow, M. A.; Jamin, M.; Dyson, H. J.; Wright, P. E. Mapping long-range contacts in a highly unfolded protein. J. Mol. Biol. 2002, 322, 655-662.
37. Gillespie, J. R.; Shortle, D. Characterization of long-range structure in the denatured state of staphylococcal nuclease. I. Paramagnetic relaxation enhancement by nitroxide spin labels. J. Mol. Biol. 1997, 268, 158-169.
38. 2H spin relaxation study of Δ131Δ. J. Am. Chem. Soc. 2003, 125, 1748-1758.
39. Jacobs, M. D.; Fox, R. D. Staphylococcal nuclease folding intermediate characterized by hydrogen exchange and NMR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 449-463.
40. Roder, H.; Elove, G. A.; Englander, S. W. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 1988, 335, 700-704.
41. Udgaonkar, J. B.; Baldwin, R. L. NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 1988, 335, 694-699.
42. Radford, S. E.; Dobson, C. M.; Evans, P. A. The folding of hen lysozyme involves partially structured intermediates and multiple pathways. Nature 1992, 358, 302-307.
43. Samuel, D.; Kumar, T. K.; Balamurugan, K.; Lin, W. Y.; Chin, D. H.; Yu, C. Structural events during the refolding of an all β-sheet protein. J. Biol. Chem 2001, 276, 4134-4141.
44. Sivaraman, T.; Kumar, T. K.; Chang, D. K.; Lin, W. Y.; Yu, C. Events in the kinetic folding pathway of a small, all β-sheet protein. J. Biol. Chem. 1998, 273, 10181-10189.
45. Laurents, D. V.; Bruix, M.; Jamin, M.; Baldwin, R. L. A pulse-chasecompetition experiment to determine if a folding intermediate is on- or off-pathway: Application to ribonuclease A. J. Mol. Biol. 1998, 283, 669-678.
46. Balbach, J.; Forge, V.; Lau, W. S.; van Nuland, N. A.; Brew, K.; Dobson, C. M. Protein folding monitored at individual residues during a two-dimensional NMR experiment. Science 1996, 274, 1161-1163.
47. Roy, M.; Jennings, P. A. Real-time NMR kinetic studies provide global and residue-specific information on the non-cooperative unfolding of the β-trefoil protein, interleukin-1β. J. Mol. Biol. 2003, 328, 693-703.
48. Kathir, K. M.; Kumar, T. K. S.; Yu, C. Monitoring folding of human acidic fibroblast growth factor in real time. 2004, manuscript unpublished.
49. Mizuguchi, M.; Kroon, G. J.; Wright, P. E.; Dyson, H. J. Folding of a β-sheet protein monitored by real-time NMR spectroscopy. J. Mol. Biol. 2003, 328, 1161-1171.
50. 19F]tryptophan- labeled Escherichia coli dihydrofolate reductase in the presence of ligand: A stopped-flow NMR spectroscopy study. Biochemistry 1998, 37, 387-398.
51. Buevich, A. V.; Baum, J. Residue-specific real-time NMR diffusion experiments define the association states of proteins during folding. J. Am. Chem. Soc. 2002, 124, 7156-7162.
52. Canet, D.; Lyon, C. E.; Scheek, R. M.; Robillard, G. T.; Dobson, C. M.; Hore, P. J.; van Nuland, N. A. Rapid formation of non-native contacts during the folding of HPr revealed by real-time photo-CIDNP NMR and stopped-flow fluorescence experiments. J. Mol. Biol. 2003, 330, 397-407.