Real-time NMR kinetic studies provide global and residue-specific information on the non-cooperative unfolding of the β-trefoil protein, interleukin-1β

Journal of Molecular Biology

Volumn 328, Issue 3, 2003, Pages 693-703

  Roy, Melinda ^a   Jennings, Patricia A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cytokine; Interleukin 1 ; Solvent backbone interactions; Unfolding kinetics; trefoil

Indexed keywords

AMINO ACID; INTERLEUKIN 1BETA;

ARTICLE; KINETICS; LOW TEMPERATURE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE;

LOTUS;

EID: 0037414459     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00340-1     Document Type: Article

References (82)

1. Radford S.E., Dobson C.M. From computer simulations to human disease: emerging themes in protein folding. Cell. 97:1999;291-298.
2. Dobson C.M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 24:1999;329-332.
3. Goldenberg D.P., Creighton T.E. Energetics of protein structure and folding. Biopolymers. 24:1985;167-182.
4. Ibragimova G.T., Wade R.C. Stability of the beta-sheet of the WW domain: a molecular dynamics simulation study. Biophys. J. 77:1999;2191-2198.
5. Wang H.W., Sung S.S. Molecular dynamics simulations of three-strand beta-sheet folding. J. Am. Chem. Soc. V122:2000;1999-2009.
6. Pugliese L., Prevost M., Wodak S.J. Unfolding simulations of the 85-102 beta-hairpin of barnase. J. Mol. Biol. 251:1995;432-447.
7. Dinner A.R., Lazaridis T., Karplus M. Understanding beta-hairpin formation. Proc. Natl Acad. Sci. USA. 96:1999;9068-9073.
8. Pande V.S., Rokhsar D.S. Molecular dynamics simulations of unfolding and refolding of a beta-hairpin fragment of protein G. Proc. Natl Acad. Sci. USA. 96:1999;9062-9067.
9. Klimov D.K., Thirumalai D. Mechanisms and kinetics of beta-hairpin formation. Proc. Natl Acad. Sci. USA. 97:2000;2544-2549.
10. 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. Nature Struct. Biol. 4:1997;630-634.
11. Parker M.J., Marqusee S. A kinetic folding intermediate probed by native state hydrogen exchange. J. Mol. Biol. 305:2001;593-602.
12. Englander S.W. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29:2000;213-238.
13. Kiefhaber T., Baldwin R.L. Hydrogen exchange and the unfolding pathway of ribonuclease A. Biophys. Chem. 59:1996;351-356.
14. Sridevi K., Udgaonkar J.B. Unfolding rates of barstar determined in native and low denaturant conditions indicate the presence of intermediates. Biochemistry. 41:2002;1568-1578.
15. Lakshmikanth G.S., Sridevi K., Krishnamoorthy G., Udgaonkar J.B. Structure is lost incrementally during the unfolding of barstar. Nature Struct. Biol. 8:2001;799-804.
16. Ramachandran S., Rami B.R., Udgaonkar J.B. Measurements of cysteine reactivity during protein unfolding suggest the presence of competing pathways. J. Mol. Biol. 297:2000;733-745.
17. Bhuyan A.K., Udgaonkar J.B. Observation of multistate kinetics during the slow folding and unfolding of barstar. Biochemistry. 38:1999;9158-9168.
18. Zaidi F.N., Nath U., Udgaonkar J.B. Multiple intermediates and transition states during protein unfolding. Nature Struct. Biol. 4:1997;1016-1024.
19. Kiefhaber T., Labhardt A.M., Baldwin R.L. Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A. Nature. V375:1995;513-515.
20. Hoeltzli S.D., 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.
21. Sivaraman T., Arrington C.B., Robertson A.D. Kinetics of unfolding and folding from amide hydrogen exchange in native ubiquitin. Nature Struct. Biol. 8:2001;331-333.
22. Arrington C.B., Robertson A.D. Correlated motions in native proteins from MS analysis of NH exchange: evidence for a manifold of unfolding reactions in ovomucoid third domain. J. Mol. Biol. 300:2000;221-232.
23. Arrington C.B., Robertson A.D. Microsecond to minute dynamics revealed by EX1-type hydrogen exchange at nearly every backbone hydrogen bond in a native protein. J. Mol. Biol. 296:2000;1307-1317.
24. Juneja J., Udgaonkar J.B. Characterization of the unfolding of ribonuclease a by a pulsed hydrogen exchange study: evidence for competing pathways for unfolding. Biochemistry. 41:2002;2641-2654.
25. Ervin J., Larios E., Osvath S., Schulten K., Gruebele M. What causes hyperfluorescence: folding intermediates or conformationally flexible native states? Biophys. J. 83:2002;473-483.
26. Yan S., Kennedy S., 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.
27. Rothwell N.J., Luheshi G.N. Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci. 23:2000;618-625.
28. Rubartelli A., Cozzolino F., Talio M., Sitia R. A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J. 9:1990;1503-1510.
29. Finke J.M., Roy M., Zimm B.H., Jennings P.A. Aggregation events occur prior to stable intermediate formation during refolding of interleukin 1beta. Biochemistry. 39:2000;575-583.
30. Griffin W.S., Nicoll J.A., Grimaldi L.M., Sheng J.G., Mrak R.E. The pervasiveness of interleukin-1 in alzheimer pathogenesis: a role for specific polymorphisms in disease risk. Expt. Gerontol. 35:2000;481-487.
31. Griffin W.S., Sheng J.G., Roberts G.W., Mrak R.E. Interleukin-1 expression in different plaque types in Alzheimer's disease: significance in plaque evolution. J. Neuropathol. Expt. Neurol. 54:1995;276-281.
32. Craig S., Schmeissner U., Wingfield P., Pain R.H. Conformation, stability, and folding of interleukin 1 beta. Biochemistry. 26:1987;3570-3576.
33. Covalt J.C. Jr, Roy M., Jennings P.A. Core and surface mutations affect folding kinetics, stability and cooperativity in IL-1 beta: does alteration in buried water play a role? J. Mol. Biol. 307:2001;657-659.
34. Heidary D.K., Jennings P.A. Three topologically equivalent core residues affect the transition state ensemble in a protein folding reaction. J. Mol. Biol. 316:2002;789-798.
35. Wolynes P.G., Onuchic J.N., Thirumalai D. Navigating the folding routes. Science. 267:1995;1619-1620.
36. Dill K.A., Chan H.S. From Levinthal to pathways to funnels. Nature Struct. Biol. 4:1997;10-19.
37. 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.
38. Pande V.S., Grosberg A., Tanaka T., Rokhsar D.S. Pathways for protein folding: is a new view needed? Curr. Opin. Struct. Biol. 8:1998;68-79.
39. Alexandrescu A.T., Evans P.A., Pitkeathly M., Baum J., Dobson C.M. Structure and dynamics of the acid-denatured molten globule state of alpha-lactalbumin: a two-dimensional NMR study. Biochemistry. 32:1993;1707-1718.
40. Driscoll P.C., Clore G.M., Marion D., Wingfield P.T., Gronenborn A.M. Complete resonance assignment for the polypeptide backbone of interleukin 1 beta using three-dimensional heteronuclear NMR spectroscopy. Biochemistry. 29:1990;3542-3556.
41. Spera S., Bax A. Empirical correlation between protein backbone conformation and C-alpha and C-beta C-13 nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. V113:1991;5490-5492.
42. Steegborn C., Schneider-Hassloff H., Zeeb M., Balbach J. Cooperativity of a protein folding reaction probed at multiple chain positions by real-time 2D NMR spectroscopy. Biochemistry. 39:2000;7910-7919.
43. Killick T.R., Freund S.M., Fersht A.R. Real-time NMR studies on folding of mutants of barnase and chymotrypsin inhibitor 2. FEBS Letters. 423:1998;110-112.
44. Balbach J., Forge V., van Nuland N.A., Winder S.L., Hore P.J., Dobson C.M. Following protein folding in real time using NMR spectroscopy. Nature Struct. Biol. 2:1995;865-870.
45. 1H NMR spectroscopy. Biochemistry. 29:1990;7387-7401.
46. Salem G.M., Hutchinson E.G., Orengo C.A., Thornton J.M. Correlation of observed fold frequency with the occurrence of local structural motifs. J. Mol. Biol. 287:1999;969-981.
47. Murzin A.G., Lesk A.M., Chothia C. beta-Trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors interleukins-1 beta and 1 alpha and fibroblast growth factors. J. Mol. Biol. 223:1992;531-543.
48. Finzel B.C., Clancy L.L., Holland D.R., Muchmore S.W., Watenpaugh K.D., Einspahr H.M. Crystal structure of recombinant human interleukin-1 beta at 2.0 Å resolution. J. Mol. Biol. 209:1989;779-791.
49. Clore G.M., Wingfield P.T., Gronenborn A.M. High-resolution three-dimensional structure of interleukin 1 beta in solution by three- and four-dimensional nuclear magnetic resonance spectroscopy. Biochemistry. 30:1991;2315-2323.
50. Nagano N., Hutchinson E.G., Thornton J.M. Barrel structures in proteins: automatic identification and classification including a sequence analysis of TIM barrels. Protein Sci. 8:1999;2072-2084.
51. Murzin A.G., Lesk A.M., Chothia C. Principles determining the structure of beta-sheet barrels in proteins. I. A theoretical analysis. J. Mol. Biol. 236:1994;1369-1381.
52. Murzin A.G., Lesk A.M., Chothia C. Principles determining the structure of beta-sheet barrels in proteins. II. The observed structures. J. Mol. Biol. 236:1994;1382-1400.
53. 1H multiple quantum coherence NMR spectroscopy. Biochemistry. 29:1990;5671-5676.
54. Varley P., Gronenborn A.M., Christensen H., Wingfield P.T., Pain R.H., Clore G.M. Kinetics of folding of the all-beta sheet protein interleukin-1 beta. Science. 260:1993;1110-1113.
55. Heidary D.K., Gross L.A., Roy M., Jennings P.A. Evidence for an obligatory intermediate in the folding of interleukin-1 beta. Nature Struct. Biol. 4:1997;725-731.
56. Chrunyk B.A., Wetzel R. Breakdown in the relationship between thermal and thermodynamic stability in an interleukin-1 beta point mutant modified in a surface loop. Protein Eng. 6:1993;733-738.
57. Clementi C., Jennings P.A., Onuchic J.N. How native-state topology affects the folding of dihydrofolate reductase and interleukin-1beta. Proc. Natl Acad. Sci. USA. 97:2000;5871-5876.
58. Estape D., Rinas U. Folding kinetics of the all-beta-sheet protein human basic fibroblast growth factor, a structural homolog of interleukin-1beta. J. Biol. Chem. 274:1999;34083-34088.
59. Samuel D., Kumar T.K., Balamurugan K., Lin W.Y., Chin D.H., Yu C. Structural events during the refolding of an all beta-sheet protein. J. Biol. Chem. 276:2001;4134-4141.
60. Liu C., Gaspar J.A., Wong H.J., Meiering E.M. Conserved and non-conserved features of the folding pathway of hisactophilin, a beta-trefoil protein. Protein Sci. 11:2002;669-679.
61. 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 beta-barrel protein. J. Biol. Chem. 277:2002;34941-34948.
62. Wooll J.O., Wrabl J.O., Hilser V.J. Ensemble modulation as an origin of denaturant-independent hydrogen exchange in proteins. J. Mol. Biol. 301:2000;247-256.
63. Csermely P. Water and cellular folding processes. Cell. Mol. Biol. (Noisy-le-grand). 47:2001;791-800.
64. Klein-Sietharaman, J., Oikawa, M., Grimashaw, S. B., Wirmer, J., Duchardt, E., Ueda, T. et al. (2002). Long-range interactions within a nonnative protein. Science, 295, 1719-1722.
65. Bai Y., Chung J., Dyson H.J., Wright P.E. Structural and dynamic characterization of an unfolded state of poplar apo-plastocyanin formed under non-denaturing conditions. Protein Sci. 10:2001;1056-1066.
66. Wright P.E., Dyson H.J., Lerner R.A. Conformation of peptide fragments of proteins in aqueous solution: implications for initiation of protein folding. Biochemistry. 27:1988;7167-7175.
67. 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. 224:1992;847-859.
68. Munoz V., Thompson P.A., Hofrichter J., Eaton W.A. Folding dynamics and mechanism of beta-hairpin formation. Nature. 390:1997;196-197.
69. Wang H., Varady J., Ng L., Sung S.S. Molecular dynamics simulations of beta-hairpin folding. Proteins: Struct. Funct. Genet. 37:1999;325-333.
70. Hodsdon M.E., Frieden C. Intestinal fatty acid binding protein: the folding mechanism as determined by NMR studies. Biochemistry. 40:2001;732-742.
71. Choy W.Y., Forman-Kay J.D. Calculation of ensembles of structures representing the unfolded state of an SH3 domain. J. Mol. Biol. 308:2001;1011-1032.
72. Jager M., Nguyen H., Crane J.C., Kelly J.W., Gruebele M. The folding mechanism of a beta-sheet: the WW domain. J. Mol. Biol. 311:2001;373-393.
73. Fersht A.R., Daggett V. Protein folding and unfolding at atomic resolution. Cell. 108:2002;573-582.
74. Shea J.E., Brooks C.L. III. From folding theories to folding proteins: a review and assessment of simulation studies of protein folding and unfolding. Annu. Rev. Phys. Chem. 52:2001;499-535.
75. 13C resonances of interleukin-1 beta using double- and triple-resonance heteronuclear three-dimensional NMR spectroscopy. Biochemistry. 29:1990;8172-8184.
76. Bodenhausen G., Ruben D.J. Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters. 69:1980;185-189.
77. Palmer A.G. III, Cavanagh J., Wright P.E., Rance M. Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J. Magn. Reson. 93:1991;151-170.
78. Kay L.E., Keifer P., Saarinen T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. V114:1992;10663-10665.
79. Schleucher J., Sattler M., Griesinger C. Coherence selection by gradients without signal attenuation - application to the 3-dimensional Hnco experiment. Angewandte Chemie-International Edition in English. V32:1993;1489-1491.
80. Muhandiram D.R., Kay L.E. Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson., ser. B. 103:1994;203-216.
81. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR. 6:1995;135-140.
82. Koradi R., Billeter M., Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;29-32.