Cold denaturation of barstar: 1H,15N and 13C NMR assignment and characterisation of residual structure

Journal of Molecular Biology

Volumn 259, Issue 4, 1996, Pages 805-818

  Wong, Kam Bo ^a   Freund, Stefan M V ^a   Fersht, Alan R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Backbone dynamics; Heteronuclear NMR; Nucleation; Protein folding; Secondary structure

Indexed keywords

ALANINE; CYSTEINE; GLOBULAR PROTEIN; UREA;

AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; TEMPERATURE;

EID: 0030596513     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0359     Document Type: Article

References (63)

1. Agashe, V. R. & Udgaonkar, J. B. (1995). Thermodynamics of denaturation of barstar: evidence for cold denaturation and evaluation of the interaction with guanidine hydrochloride. Biochemistry, 34, 3286-3299 .
2. Agashe, V. R., Shastry, M. C. R. & Udgaonkar, J. B. (1995). Initial hydrophobic collapse in the folding of barstar. Nature, 377, 754-757.
3. Alexandrescu, A. T., Abeygunawardana, C. & Shortle, D. (1995). Structure and dynamics of a denatured 131-residue fragment of staphylococcal nuclease: a heteronuclear NMR study. Biochemistry, 33, 1063-1072.
4. Amodeo, P., Motta, A., Picone, D., Saviano, G., Tancredi, T. & Temussi, P. A. (1991). Viscosity as a conformational sieve. NOE of linear peptides in cryoprotective mixtures. J. Magn. Reson. 95, 201-207.
5. Anderson, A. G. & Hermans, J. (1988). Microfolding: conformational probability map for the alanine dipeptide in water from molecular dynamics simulations. Proteins: Struct. Funct. Genet. 3, 262-265.
6. 1H assignments of its pH-denatured state. Proc. Natl Acad. Sci. USA, 91, 9412-9416.
7. Arcus, V. L., Vuilleumier, S., Freund, S. M. V., Bycroft, M. & Fersht, A. R. (1995). 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, 305-321.
8. Baldwin, R. L. (1993). Pulsed H/D-exchange studies of folding intermediates. Curr. Opin. Struct. Biol. 3, 84-91.
9. Bax, A. & Subramanian, S. (1986). Sensitivity-enhanced two-dimensional heteronuclear shift correlation NMR Spectroscopy. J. Magn. Reson. 67, 565-569.
10. Bax, A., Ikura, M., Kay, L. E., Torchia, D. A. & Tschudin, R. (1990). Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins. J. Magn. Reson. 86, 304-318.
11. Bodenhausen, G. & Ruben, D. L. (1980). Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters, 69, 185-188.
12. Brant, D. A., Miller, W. G. & Flory, P. J. (1967). Conformational energy estimates for statistically coiling polypeptide chains. J. Mol. Biol. 23, 47-65.
13. 15N "random coil" chemical shifts. J. Am. Chem. Soc. 116, 8466-8469.
14. Buckle, A. M., Schreiber, G. & Fersht, A. R. (1994). Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2.0-Å resolution. Biochemistry, 33, 8878-8889.
15. Bycroft, M., Matouschek, A., Kellis, J. T., Jr, Serrano, L. & Fersht, A. R. (1990). Detection and characterization of a folding intermediate by NMR. Nature, 346, 488-490.
16. Dyson, H. J. & Wright, P. E. (1991). Defining solution conformations of small linear peptides. Annu. Rev. Biophys. Biophys. Chem. 20, 519-538.
17. Dyson, H. J., Merutka, G., Waltho, J. P., Lerner, R. A. & Wright, P. E. (1992a). Folding of peptide fragments comprising the complete sequence of proteins. Models for initiation of protein folding. I. Myohemerythrin. J. Mol. Biol. 226, 795-817.
18. Dyson, H. J., Sayre, J. R., Merutka, G., Shin, H.-C., Lerner, R. A. & Wright, P. E. (1992b). Folding of peptide fragments comprising the complete sequence of proteins. Models for initiation of protein folding. II. Plastocyanin. J. Mol. Biol. 226, 819-835.
19. Englander, S. W. & Mayne, L. (1992). Protein folding studied using hydrogen-exchange labeling and 2-dimensional NMR. Annu. Rev. Biophys. Biomol. Struct. 21, 243-265.
20. Esposito, G. & Pastore, A. (1988). An alternative method for distance evaluation from NOESY spectra. J. Magn. Reson. 76, 331-336.
21. Frank, M. K., Clore, G. M. & Gronenborn, A. M. (1995). Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein by multidimensional heteronuclear NMR spectroscopy. Protein Sci. 4, 2605-2615.
22. Frenkiel, T., Bauer, C, Carr, M. D., Birdsall, B. & Feeney, J. (1990). HMQC-NOESY-HMQC, a three-dimensional NMR experiment which allows detection of nuclear Overhauser effects between protons with overlapping signals. J. Magn. Reson. 90, 420-425.
23. Frisch, C., Schreiber, G. & Fersht, A. R. (1995). Characterization of in vitro oxidized barstar. FEBS Letters, 70, 273-277.
24. Grzesiek, S. & Bax, A. (1992a). Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114, 6291-6293.
25. Grzesiek, S. & Bax, A. (1992b). Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J. Magn. Reson. 96, 432-440.
26. Grzesiek, S. & Bax, A. (1993). Amino-acid type determination in the sequential assignment procedure of uniformly C-13/N-15-enriched proteins. J. Biomol. NMR, 3, 185-204.
27. Grzesiek, S., Anglister, J. & Bax, A. (1993). Correlation of backbone amide and aliphatic side-chain resonances in C-13/N-15-enriched proteins by isotropic mixing of C-13 magnetization. J. Magn. Reson. ser. B, 101, 114-119.
28. Guillet, V., Lapthorn, A., Hartley, R. W. & Mauguen, Y. (1993). Recognition between a bacterial ribonuclease, barnase, and its natural inhibitor, barstar. Structure, 1, 165-177.
29. Jardetzky, O. & Roberts, G. C. K. (1981). In NMR in Molecular Biology (Horecker, B., Kaplan, N. O., Marmur, J. & Scheraga, H. A., eds), pp. 115-142, Academic Press, Inc., Orlando, FL.
30. Karplus, M. (1963). Vicinal proton coupling in nuclear magnetic resonance. J. Am. Chem. Soc. 85, 2870.
31. Kay, L. E., Keifer, P. & Saarinen, T. (1992). Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665.
32. Khurana, R. & Udgaonkar, J. B. (1994). Equilibrium unfolding studies of barstar: evidence for an alternative conformation which resembles a molten globule. Biochemistry, 33, 106-115.
33. Kraulis, P. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
34. Levinthal, C. (1968). Are there pathways for protein folding? J. Chem. Phys. 85, 44-45.
35. 15N NMR study of Gramicidin S in water and organic solvents. J. Am. Chem. Soc. 106, 1939-1941.
36. Logan, T. M., Thériault, Y. & Fesik, S. W. (1994). Structural characterization of the FK506 binding protein unfolded in urea and guanidine hydrochloride. J. Mol. Biol. 236, 637-648.
37. 13C assignments of barstar using nuclear magnetic resonance spectroscopy. Biochemistry, 33, 8866-8877.
38. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1β. Biochemistry, 28, 6150-6156.
39. Martínez, J. C., Filimonov, V. V., Mateo, P. L., Schreiber, G. & Fersht, A. R. (1995). A calorimetric study of the thermal stability of barstar and its interaction with barnase. Biochemistry, 34, 5224-5233.
40. Matouschek, A., Kellis, J. T., Jr, Serrano, L. & Fersht, A. R. (1989). Mapping the transition state and pathway of protein folding by protein engineering. Nature, 342, 122-126.
41. Matouschek, A., Kellis, J. T., Jr., Serrano, L., Bycroft, M. & Fersht, A. R. (1990). Transient folding intermediates characterised by protein engineering. Nature, 346, 440-445.
42. Neri, D., Billeter, M., Wider, G. & Wüthrich, K. (1992). NMR determination of residual structure in a urea-denatured protein, the 434-repressor. Science, 257, 1559-1563.
43. Nölting, B., Golbik, R. & Fersht, A. R. (1995). Submillisecond events in protein folding. Proc. Natl Acad. Sci. USA, 92, 10668-10672.
44. Pan, H., Barbar, E., Barany, G. & Woodward, C. (1995). Extensive nonrandom structure in reduced and unfolded bovine pancreatic trypsin inhibitor. Biochemistry, 34, 13974-13981.
45. Piotto, M., Saudek, V. & Sklenár, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
46. Privalov, P. L. (1990). Cold denaturation of proteins. Crit. Rev. Biochem. Mol. Biol. 25, 281-305.
47. Roder, H., Elove, G. A. & Englander, S. W. (1988). Structural characterisation of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature, 335, 700-704.
48. Saulitis, J. & Liepins, E. (1990). Quantitative evaluation of interproton distances in peptides by two-dimensional Overhauser effect spectroscopy. J. Magn. Reson. 87, 80-91.
49. Schreiber, G. & Fersht, A. R. (1993). The refolding of cis- and trans-peptidylprolyl isomers of barstar. Biochemistry, 32, 11195-11203.
50. Shastry, M. C. R. & Udgaonkar, J. B. (1995). The folding mechanism of barstar: evidence for multiple pathways and multiple intermediates. J. Mol. Biol. 247, 1013-1027.
51. Shastry, M. C. R., Agashe, V. R. & Udgaonkar, J. B. (1994). Quantitative analysis of the kinetics of denaturation and renaturation of barstar in the folding transition zone. Protein Sci. 3, 1409-1417.
52. Shortle, D. (1993). Denatured states of proteins and their roles in folding and stability. Curr. Opin. Struct. Biol. 3, 66-74.
53. Spera, S. & Bax, A. (1991). Empirical correlation between protein backbone conformation and C-alpha and C-beta nuclear-magnetic-resonance chemical-shifts. J. Am. Chem. Soc. 113, 5490-5492.
54. Stonehouse, J. & Keeler, J. (1995). A convenient and accurate method for the measurement of the values of spin-spin coupling constants. J. Magn. Reson. ser. A, 112, 43-57.
55. Swindells, M. B., MacArthur, M. W. & Thornon, J. M. (1995). Intrinsic φ, ψ propensities of amino acids, derived from the coil regions of known structures. Nature Struct. Biol 2, 596-603.
56. Udgaonkar, J. B. & Baldwin, R. L. (1988). NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature, 335, 694-699.
57. Waltho, J. P., Feher, V. A., Merutka, G., Dyson, H. J. & Wright, P. E. (1993). Peptide models of protein folding initiation sites. 1. Secondary structure formation by peptides corresponding to the G- and H-helices of myoglobin. Biochemistry, 32, 6337-6347.
58. Wishart, D. S., Sykes, B. D. & Richards, F. M. (1992). The Chemical Shift Index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry, 31, 1647-1651.
59. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbour effects. J. Biomol. NMR, 5, 67-81.
60. Wittekind, M. & Mueller, L. (1993). HNCACB, a high sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha and beta carbon resonances in proteins. J. Magn. Reson. ser. B, 101, 201-205.
61. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids. John Wiley & Sons, Inc., New York.
62. Wüthrich, K. (1994). NMR assignments as a basis for structural characterization of denatured states of globular proteins. Curr. Opin. Struct. Biol. 4, 93-99.
63. Zhang, O. & Forman-Kay, J. D. (1995). Structural characterization of folded and unfolded states of an SH3 domain in equilibrium in aqueous buffer. Biochemistry, 34, 6784-6794.