Exploring the folding funnel of a polypeptide chain by biophysical studies on protein fragments

Journal of Molecular Biology

Volumn 285, Issue 3, 1999, Pages 1309-1333

  Neira, José L ^a   Fersht, Alan R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Barnase; Chymotrypsin inhibitor 2; Denatured state; Protein fragments

Indexed keywords

BARNASE; CHYMOTRYPSIN INHIBITOR; HISTIDINE; LEUCINE; POLYPEPTIDE; SERINE; THREONINE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BIOPHYSICS; CARBOXY TERMINAL SEQUENCE; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

EID: 0033593272     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2249     Document Type: Article

References (80)

1. 1H NMR assignments of its pH-denatured state. Proc. Natl Acad. Sci. USA. 91:1994;9412-9416.
2. Arcus V. L., Vuilleumier S., Freund S. M. V., Bycroft M., Fersht A. R. A comparison of the pH, urea, and temperature-denatured states of barnase by heteronuclear NMR: implications for the initiation of protein folding. J. Mol. Biol. 254:1995;305-321.
3. Balbach J., Forge V., Lau W. S., Jones J. A., Van Nuland N. A. J. V., Dobson C. M. Detection of residue contacts in a protein folding intermediate. Proc. Natl Acad. Sci. USA. 794:1997;7182-7185.
4. Bax A., Davis D. G. MLEV-17 based two-dimensional homonuclear magnetisation transfer spectroscopy. J. Magn. Reson. 65:1985;355-360.
5. Bond C. L., Wong K., Clarke L., Fersht A. R., Daggett V. Characterization of residual structure in the thermally denatured state of barnase by simulation and experiment: description of the folding pathway. Proc. Natl Acad. Sci. USA. 94:1997;13409-13413.
6. Bothner-By A. A., Stephens R. L., Lee J. M., Warren C. D., Jeanloz R. W. Structure determination of a tetrasaccharide: transient nuclear Overhauser effects in the rotating frame. J. Am. Chem. Soc. 106:1984;811-813.
7. Braunschweiler L., Ernst R. R. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53:1983;521-528.
8. Bryngelson J. D., Onuchic J. N., Socci N. D., Wolynes P. G. Funnels, pathways and the energy landscape of protein folding: a synthesis. Proteins: Struct. Funct. Genet. 21:1995;167-195.
9. 1H-nuclear magnetic resonance spectrum of barnase. Biochemistry. 29:1990;7425-7432.
10. Bycroft M., Ludvigsen S., Fersht A. R., Poulsen F. M. Determination of the three-dimensional structure of barnase using nuclear magnetic resonance spectroscopy. Biochemistry. 30:1991;8697-8701.
11. Caflisch A., Karplus M. Acid and thermal denaturation of barnase investigated by molecular dynamics simulations. J. Mol. Biol. 252:1995;672-708.
12. Cammers-Goodwin A., Allen T. J., Oslick S. L., McClure K. F., Lee J. H., Kemp D. S. Mechanism of stabilisation of helical conformations of polypeptides by water containing trifluoroethanol. J. Am. Chem. Soc. 118:1996;3082-3090.
13. Chan H. S., Dill K. A. Protein folding in the landscape perspective: Chevron plots and non-Arrhenius kinetics. Proteins: Struct. Funct. Genet. 30:1998;2-33.
14. Clarke J., Fersht A. R. Engineered disulphide bonds of the folding pathway of barnase: increasing stability of proteins against the rate of denaturation. Biochemistry. 32:1993;4322-4329.
15. Clarke J., Hounslow A. M., Bycroft M., Fersht A. R. Local breathing and global unfolding in hydrogen exchange of barnase and its relationship to protein folding pathways. Proc. Natl Acad. Sci. USA. 90:1993;9837-9841.
16. Corbett R. J. T., Roche R. S. Use of high speed size-exclusion chromatography for the study of protein folding and stability. Biochemistry. 23:1984;1888-1894.
17. Corrales F. J., Fersht A. R. Towards a mechanism for GroEL:GroES chaperone activity: an ATPase-gated and -pulsed folding and annealing cage. Proc. Natl Acad. Sci. 93:1996;4509-4512.
18. Creighton T. E. Protein-folding-an unfolding story. Curr. Biol. 5:1995;353-356.
19. Dill K. A., Bromberg S., Yue K., Fiebig K. M., Yee D. P., Thomas P. D., Chan H. S. Principles of protein folding-a perspective from simple exact models. Protein Sci. 4:1995;561-602.
20. Dobson C. M., Sali A., Karplus M. Protein folding: a perspective from theory and experiment. Angew. Chem. Int. English Ed. 37:1998;868-893.
21. Fersht A. R. Protein folding and stability: the pathway of folding of barnase. FEBS Letters. 325:1993;5-16.
22. Fersht A. R. Optimisation of rates of protein folding: the nucleation-condensation mechanism and its implications. Proc. Natl Acad. Sci. USA. 92:1995;10869-10873.
23. Fersht A. R. Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7:1997;3-9.
24. Gill S. C., von Hippel P. H. Extinction coefficients from amino acid sequence data. Anal. Biochem. 182:1989;319-326.
25. Gray T. E., Eder L., Bycroft M., Day A. G., Fersht A. R. Refolding of barnase mutants and pro-barnase in the presence and absence of GroEL. EMBO J. 12:1993;4145-4150.
26. Horovitz A., Serrano L., Avron A., Bycroft M., Fersht A. R. Strength and co-operativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216:1990;1031-1044.
27. Itzhaki L. S., Otzen D. E., Fersht A. R. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods. Evidence for a nucleation condensation mechanism for protein folding. J. Mol. Biol. 254:1995a;260-288.
28. Itzhaki L. S., Neira J. L., Ruiz-Sanz L., Prat de Gay G., Fersht A. R. Search for nucleation sites in smaller fragments of chymotrypsin inhibitor-2. J. Mol. Biol. 254:1995b;289-304.
29. Itzhaki L. S., Otzen D. E., Fersht A. R. Nature and consequences of GroEL-protein interactions. Biochemistry. 34:1995c;14581-14587.
30. Jackson S. E., Fersht A. R. Folding of chymotrypsin inhibitor 2. (1) Evidence for a two state transition. Biochemistry. 30:1991;10428-10435.
31. Jeener J., Meier B., Backman P., Ernst R. R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71:1979;4546-4550.
32. Johnson C. M., Fersht A. R. Protein stability as a function of denaturant concentration: the thermal stability of barnase in the presence of urea. Biochemistry. 34:1995;6795-6804.
33. Kippen A. D. PhD thesis. 1994;University of Cambridge.
34. Kippen A. D., Sancho J., Fersht A. R. Folding of barnase in parts. Biochemistry. 33:1994a;3778-3786.
35. Kippen A. D., Arcus V. L., Fersht A. R. Structural studies on peptides corresponding to mutants of the major α-helix of barnase. Biochemistry. 33:1994b;10013-10021.
36. Kolb V. A., Makeyev E. V., Komner A., Spirin A. S. Cotranslational folding of proteins. Biochem. Cell Biol. 73:1995;1217-1220.
37. Kraulis P. J. MOLSCRIPT, a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
38. Lazaridis T., Karplus M. "New view" of protein folding reconciled with the old through multiple unfolding simulations. Science. 278:1997;1928-1931.
39. Levinthal C. Are there pathways for protein folding? J. Chim. Phys. 65:1968;44-45.
40. Li A., Daggett V. Characterisation of the transition state of protein unfolding by use of molecular dynamics: chymotrypsin inhibitor 2. Proc. Natl Acad. Sci. USA. 91:1994;10430-10434.
41. Loewenthal R., Sancho J., Fersht A. R. Fluorescence spectrum of barnase: contributions of three tryptophan residues and a histidine-related pH dependence. Biochemistry. 30:1991;6775-6779.
42. a and contribution to protein stability. J. Mol. Biol. 224:1992;759-770.
43. López-Hernández E., Serrano L. Structure of the transition state for folding of the 129-amino acid protein CheY resembles that of the smaller protein CI2. Folding Des. 1:1996;43-55.
44. Lorimer G. H. A quantitative assessment of the role of chaperonin proteins in protein-folding in vivo. FASEB J. 10:1996;5-9.
45. Luo P., Baldwin R. L. Mechanism of helix induction by trifluoroethanol: a framework for extrapolating the helix-forming propensities of peptides from trifluoroethanol/water mixtures back to water. Biochemistry. 36:1997;8413-8421.
46. Marion D., Wüthrich K. Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of proton-proton spin-spin coupling constants. Biochem. Biophys. Res. Commun. 11:1983;967-975.
47. Martínez J. C., El Harrous M., Filimonov V. V., Mateo P. L., Fersht A. R. A calorimetric study of the thermal stability of barnase and its interaction with 3′ GMP. Biochemistry. 33:1994;3919-3926.
48. Matouschek A., Serrano L., Fersht A. R. The folding of an enzyme IV. Structure of an intermediate in the refolding of barnase analysed by a protein engineering procedure. J. Mol. Biol. 224:1992a;819-835.
49. 2H exchange nuclear magnetic resonance studies on the folding pathway of barnase: complementarity to and agreement with protein engineering studies. J. Mol. Biol. 224:1992b;837-845.
50. Matouschek A., Matthews J. M., Johnson C. M., Fersht A. R. Extrapolation to water of kinetic and equilibrium data for the unfolding of barnase in urea solutions. Protein Eng. 7:1994;1089-1095.
51. Mauguen Y., Hartley R. W., Dodson G. G., Dodson E. J., Bricogne G., Chothia C., Jack A. Molecular structure of a new family of ribonucleases. Nature. 297:1982;162-164.
52. 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR. 5:1995;14-24.
53. Moult J., Unger R. An analysis of protein folding pathways. Biochemistry. 30:1991;3816-3824.
54. Neira J. L., Fersht A. R. An NMR study of the β-hairpin region of barnase. Folding Des. 1:1996;231-241.
55. Neira J. L., Itzhaki L. S., Ladurner A. G., Davis B., Prat de Gay G., Fersht A. R. Following co-operative formation of secondary and tertiary structure in a single protein module. J. Mol. Biol. 268:1997;185-197.
56. Nölting B., Golbik R., Soler-González A. S., Fersht A. R. Circular dichroism of denatured barstar suggests residual structure. Biochemistry. 36:1997;9894-9905.
57. Onuchic J. N., Wolynes P. G., Luthey-Schulten Z., Socci N. D. Towards an outline of the topography of a realistic protein folding funnel. Proc. Natl Acad. Sci. USA. 22:1995;3626-3630.
58. Otzen D. E., Itzhaki L. S., elMasry N. E., Jackson S. E., Fersht A. R. Structure of the transition state for the folding/unfolding of chymotrypsin inhibitor-2 and its implications for mechanisms of protein folding. Proc. Natl Acad. Sci. USA. 91:1994;10422-10425.
59. Piantini U., Sorensen O. W., Ernst R. R. Multiple quantum filter for elucidating NMR coupling networks. J. Am. Chem. Soc. 104:1982;6800-6801.
60. Prat Gay G. de, Ruiz-Sanz J., Neira J. L., Itzhaki L. S., Fersht A. R. Folding of a nascent polypeptide chain in vitro: co-operative formation of structure in a protein module. Proc. Natl Acad. Sci. 92:1995a;3683-3686.
61. Prat Gay G. de, Ruiz-Sanz J., Neira J. L., Corrales F. L., Otzen D. E., Ladurner A. G., Fersht A. R. Conformational pathway of the polypeptide chain of chymotrypsin inhibitor-2 growing from its N terminus in vitro. Parallels with the protein folding pathway. J. Mol. Biol. 254:1995b;968-979.
62. Sali D., Bycroft M., Fersht A. R. Stabilisation of protein structure by interaction of α-helix dipole with a charged side chain. Nature. 335:1988;740-743.
63. Sancho J., Fersht A. R. Dissection of an enzyme by protein engineering. The N- and C-terminal fragments of barnase form a native-like complex with restored enzymatic activity. J. Mol. Biol. 224:1992;741-747.
64. Sancho J., Neira J. L., Fersht A. R. An N-terminal fragment of barnase has residual helical structure similar to that in a refolding intermediate. J. Mol. Biol. 224:1992;749-758.
65. Sanz J. M., Fersht A. R. Rationally designing the accumulation of a folding intermediate of barnase by protein engineering. Biochemistry. 32:1993;13584-13592.
66. Schmid F. X. Creighton T. E. Protein Structure. 1997;261-297 Oxford University Press.
67. Semisotnov G. V., Rodionova N. A., Razgulyaev O. I., Uversky V. N., Gripas A. F., Gilmanshin R. I. Study of the molten globule intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers. 31:1991;119-128.
68. Serrano L., Matouschek A., Fersht A. R. The folding of an enzyme II. Substructure of barnase and the contribution of different interactions to protein stability. J. Mol. Biol. 224:1992a;783-804.
69. Serrano L., Matouschek A., Fersht A. R. The folding of an enzyme III. Structure of the transition state for the unfolding of barnase analysed by a protein engineering procedure. J. Mol. Biol. 224:1992b;805-818.
70. Serrano L., Matouschek A., Fersht A. R. The folding of an enzyme VI. The folding pathway of barnase: comparison with theoretical models. J. Mol. Biol. 224:1992c;847-859.
71. Shortle D. The denatured state (the other half of the folding equation) and its role in protein stability. FASEB J. 10:1996;27-34.
72. Smith L. J., Bolin K. A., Schwalbe H., MacArthur M. W., Thornton J. M., Dobson C. M. Analysis of main chain torsion angles in proteins: prediction of NMR coupling constants for native and random coil conformations. J. Mol. Biol. 255:1996;494-506.
73. a values in the denatured states of proteins. J. Mol. Biol. 254:1995;980-992.
74. Tirado-Rives J., Orozco M., Jorgensen W. L. Molecular dynamics simulations of the unfolding of barnase in water and 8 M aqueous urea. Biochemistry. 36:1997;7313-7329.
75. Tsou C. L. Folding of a nascent peptide chain into a biologically active protein. Biochemistry. 27:1988;1809-1812.
76. Vuilleumier S., Sancho J., Loewenthal R., Fersht A. R. Circular dichroism studies of barnase and its mutants: characterization of the contribution of aromatic side chains. Biochemistry. 32:1993;10303-10313.
77. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of the nearest-neighbour effects. J. Biomol. NMR. 5:1995;67-81.
78. Woody R. W. Circular dichroism. Methods Enzymol. 246:1995;34-71.
79. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;John Wiley & Sons, Inc. New York.
80. Yanagawa H., Yoshida K., Torigoe C., Park J. S., Sato K., Shirai T., Gõ M. Protein anatomy-functional roles of barnase module. J. Biol. Chem. 268:1993;5861-5865.