Population of On-pathway Intermediates in the Folding of Ubiquitin

Journal of Molecular Biology

Volumn 360, Issue 5, 2006, Pages 1053-1066

  Crespo, Maria D ^a   Simpson, Emma R ^a   Searle, Mark S ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

folding intermediates; peptide isomerisation; protein folding; reaction kinetics; ubiquitin

Indexed keywords

POLYPEPTIDE; UBIQUITIN;

ARTICLE; CHEMICAL REACTION KINETICS; FLUORESCENCE; ISOMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION;

EID: 33745965316     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.05.061     Document Type: Article

References (75)

1. Kim P.S., and Baldwin R.L. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 59 (1990) 631-660
2. Jackson S.E., and Fersht A.R. Folding of chymotrypsin inhibitor 2: Evidence for a two-state transition state. Biochemistry 30 (1991) 10428-10435
3. Jackson S.E. How do small single-domain proteins fold?. Fold. Des. 3 (1998) R81-R91
4. Tanford C. Protein dentauration part C. Theoretical models for the mechanism of denaturation. Advan. Protein Chem. 24 (1970) 1-95
5. Bachmann A., and Kiefhaber T. Apparent two-state tendamistat folding is a sequential process along a defined route. J. Mol. Biol. 306 (2001) 375-386
6. Sanchez I.E., and Kiefhaber T. Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding. J. Mol. Biol. 325 (2003) 367-376
7. Onuchic J.N., Luthey-Schulten Z., and Wolynes P.G. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48 (1997) 545-600
8. Dobson C.M., Sali A., and Karplus M. Protein folding: a perspective from theory and experiment. Angew. Chem. In. Ed. 37 (1998) 868-893
9. Baldwin R.L. The nature of protein folding pathways: the classical versus the new view. J. Biomol. NMR 5 (1995) 103-109
10. Wright C.F., Lindorff-Larsen K., Randles L.G., and Clarke J. Parallel protein-unfolding pathways revealed and mapped. Nature Struct. Biol. 8 (2003) 658-662
11. Wright C.F., Steward A., and Clarke J. Thermodynamic characterization of two transition states along parallel protein folding pathways. J. Mol. Biol. 338 (2004) 445-451
12. Kiefhaber T. Kinetic traps in lysozyme folding. Proc. Natl Acad. Sci. USA 92 (1995) 9029-9033
13. Wildegger G., and Kiefhaber T. Three-state model for lysozyme folding: triangular folding mechanism with an energetically trapped intermediate. J. Mol. Biol. 270 (1997) 294-304
14. Dinner A.R., Sali A., Smith L.J., Dobson C.M., and Karplus M. Understanding protein folding via free energy surfaces from theory and experiment. Trends Biochem. Sci. 25 (2000) 331-339
15. Zadi F.N., Nath U., and Udgaonkar J.B. Multiple intermediates and transition states during protein folding. Nature Struct. Biol. 4 (1997) 1016-1023
16. 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
17. Kamagata K., Sawano Y., Tanokura M., and Kuwajima K. Multiple parallel-pathway folding of proline-free staphyloccal nuclease. J. Mol. Biol. 332 (2003) 1143-1153
18. Jennings P.A., Finn B.E., Jones B.E., and Matthews C.R. A re-examination of the folding mechanism of dihydrofolate reductase from E. coli: verification and refinement of a four-channel model. Biochemistry 32 (1993) 3783-3789
19. Wallace L.A., and Matthews C.R. Highly divergent dihydrofolate reductases conserve complex folding mechanisms. J. Mol. Biol. 315 (2002) 193-211
20. Goldbeck R.A., Thomas Y.G., Chen E., Esquerra R.M., and Kliger D.S. Multiple pathways on a protein-folding energy landscape: kinetic evidence. Proc. Natl Acad. Sci. USA 96 (1999) 2782-2787
21. Vijay-Kumar S., Bugg C.E., Wilkinson K.D., Vierstra R.D., Hatfield P.M., and Cook W.J. Comparison of the three-dimensional structures of human, yeast and oat ubiquitin. J. Biol. Chem. 262 (1987) 6396-6399
22. Makhatadze G.I., Loladze V.V., Ermolenko D.M., Chen X.F., and Thomas S.T. Contribution of surface salt bridges to protein stability: guidelines for protein engineering. J. Mol. Biol. 327 (2003) 1135-1148
23. Ermolenko D.N., Thomas S.T., Aurora R., Gronenborn A.M., and Makhatadze G.I. Hydrophobic interactions at the C-cap position of the C-capping motif of α-helices. J. Mol. Biol. 322 (2002) 1123-1135
24. Loladze V.V., Ermolenko D.N., and Makhatadze G.I. Thermodynamic consequences of burial of polar and non-polar amino acid residues in the protein interior. J. Mol. Biol. 320 (2002) 343-357
25. Jourdan M., and Searle M.S. Co-operative assembly of a native-like ubiquitin structure through peptide fragment complexation: energetics of peptide association and folding. Biochemistry 39 (2000) 12355-12364
26. Jourdan M., and Searle M.S. Insights into the stability of native and partially folded states of ubiquitin: effects of co-solvents and denaturants on the thermodynamics of protein folding. Biochemistry 40 (2001) 10317-10325
27. Krantz B.A., and Sosnick T.R. Distinguishing between two-state and three-state models for ubiquitin folding. Biochemistry 39 (2000) 11696-11701
28. Briggs M.S., and Roder H. Early hydrogen bonding events in the folding reaction of ubiquitin. Proc. Natl Acad. Sci. USA 89 (1992) 2017-2021
29. Khorasanizadeh S., Peters I.D., Butt T.R., and Roder H. Folding and stability of a tryptophan containing mutant of ubiqutin. Biochemistry 32 (1993) 7054-7063
30. Khorasanizadeh S., Peters I.D., and Roder H. Evidence for a three state-model of protein folding from kinetic analysis of ubiquitin variants with altered core residues. Nature Struct. Biol. 3 (1996) 193-205
31. Gladwin S.T., and Evans P.A. Structure of the very early protein folding intermediates: new insights through a variant of hydrogen exchange labelling. Fold. Des. 1 (1996) 407-417
32. Platt G.W., Simpson S.A., Layfield R., and Searle M.S. Stability and folding kinetics of a ubiquitin mutant with a strong propensity for non-native β-hairpin conformation in the unfolded state. Biochemistry 42 (2003) 13726-13771
33. Went H.M., Benitez-Cardoza C.G., and Jackson S.E. Is an intermediate state populated on the folding pathway of ubiquitin?. FEBS Letters 567 (2004) 333-338
34. Krantz B.A., Dothager R.S., and Sosnick T.R. Discerning the structure and energy of multiple transition states in protein folding using psi-analysis. J. Mol. Biol. 337 (2004) 463-475
35. Went H.M., and Jackson S.E. Ubiquitin folds through a highly polarized transition state. Protein Eng. 18 (2004) 239-246
36. Crespo M.D., Platt G.W., Bofill R., and Searle M.S. Context-dependent effects of proline residues on the stability and folding of ubiquitin. Eur. J. Biochem. 271 (2004) 4474-4484
37. Larios E., Li J.S., Schulten K., Kihara H., and Gruebele M. Multiple probes reveal a native-like intermediate during low-temperature refolding of ubiquitin. J. Mol. Biol. 340 (2004) 115-125
38. Odefey C., Mayr L.M., and Schmid F.X. Non-prolyl cis-trans peptide bond isomerisation as a rate-determining step in protein unfolding and refolding. J. Mol. Biol. 245 (1995) 69-78
39. Sanchez I.E., Morillas M., Zobeley E., Kiefhaber T., and Glockshuber R. Fast folding of the two-domain semliki forest virus capsid protein explains co-translational proteolytic activity. J. Mol. Biol. 338 (2004) 159-167
40. Pappenberger G., Aygun H., Engels J.W., Reimer U., Fischer G., and Kiefhaber T. Non-prolyl cis peptide bonds in unfolded proteins cause complex folding kinetics. Nature Struct. Biol. 8 (2001) 452-458
41. Walkenhurst W.F., Green S.M., and Roder H. Kinetic evidence for folding and unfolding intermediates in staphylococcal nuclease. Biochemistry 36 (1997) 5795-5805
42. Maki K., Ikura T., Hayano T., Takahashi N., and Kuwajima K. Effects of proline mutations on the folding of staphylococcal nuclease. Biochemistry 38 (1999) 2213-2223
43. Scherer G., Kramer M.L., Schutkowski M., Reimer U., and Fischer G. Barriers to rotation of secondary amide peptide bonds. J. Am. Chem. Soc. 120 (1998) 5568-5574
44. Reimer U., Scherer G., Drewello M., Kruber S., Schutkowski M., and Fischer G. Side-chain effects on petidyl-prolyl cis/trans isomerisation. J. Mol. Biol. 279 (1998) 449-460
45. Brandts J.F., Halvorson H.R., and Brennan M. Consideration of the possibility that the slow step in protein denaturation reactions is due to cis trans isomerism of proline residues. Biochemistry 14 (1975) 4953-4963
46. Kiefhaber T. Protein folding kinetics. In: Shirley B.A. (Ed). Methods in Molecular Biology, Protein Stability and Folding Protocols vol. 40 (1995), Humana Press, Totowa, NJ 313-341
47. Bieri O., Wildegger G., Bachmann A., Wagner C., and Kiefhaber T. A salt-induced kinetic intermediate is on a new parallel pathway of lysozyme folding. Biochemistry 38 (1999) 12460-12470
48. Bachmann A., and Kiefhaber T. Kinetic mechanisms in protein folding. In: Kiefhaber T., and Buchner J. (Eds). Protein Folding Handbook (2005), part I, Wiley-VCH, Weinheim, Germany
49. Roder H., Maki K., Latypov R.F., Cheng H., and Ramachandra Shastry M.C. Early events in protein folding explored by rapid mixing methods. In: Kiefhaber T., and Buchner J. (Eds). Protein Folding Handbook (2005), part I, Wiley-VCH, Weinheim, Germany
50. Vallee-Belisle A., Turcotte J.-F., and Michnick S.W. raf RBD and ubiquitin proteins share similar folds, folding rates and mechanisms despite having unrelated amino acid sequences. Biochemistry 43 (2004) 8447-8458
51. Bofill R., Simpson E.R., Platt G.W., Crespo M.D., and Searle M.S. Extending the folding nucleus of ubiquitin with an independently folding β-hairpin finger: hurdles to rapid folding arising from the stabilisation of local interactions. J. Mol. Biol. 349 (2005) 205-221
52. Qin Z., Ervin J., Larios E., Gruebele M., and Kihara H. Formation of a compact structured ensemble without fluorescence signature early during ubiquitin folding. J. Phys. Chem. ser. B. 106 (2002) 13040-13046
53. Marianayagam N.J., and Jackson S.E. The folding pathway of ubiquitin from all-atom molecular dynamics simulations. Biophys. Chem. 111 (2004) 159-171
54. Zhang X., Qin M., and Wang W. Multiple folding mechanisms of protein ubiquitin. Proteins: Struct. Funct. Bioinf. 59 (2005) 565-579
55. Ferguson N., and Fersht A.R. Early events in protein folding. Curr. Opin. Struct. Biol. 13 (2003) 75-81
56. Magg C., and Schmid F.X. Rapid collapse precedes the fast two-state folding of the cold shock protein. J. Mol. Biol. 335 (2004) 1309-1323
57. Arai M., Ito K., Inobe T., Nakao M., Maki K., Kamafgata K., et al. Fast compaction of α-lactalbumin during folding studied by stopped-flow X-ray scattering. J. Mol. Biol. 321 (2002) 121-132
58. Roder H., and Colon W. Kinetic role of early intermediates in protein folding. Curr. Opin. Struct. Biol. 7 (1997) 15-28
59. Levitt M. Effect of proline residues on protein folding. J. Mol. Biol. 145 (1981) 251-263
60. Jullien M., and Baldwin R.L. The role of proline residues in the folding kinetics of bovine pancreatic trypsin inhibitor derivative RCAM (14-38). J. Mol. Biol. 145 (1981) 265-280
61. Krebs H., Schmid F.X., and Jaenicke R. Folding of homologous proteins: the refolding of different ribonucleases is independent of sequence variations, proline content and glycosylation. J. Mol. Biol. 169 (1983) 619-635
62. 1. 2. Kinetic models for the folding and unfolding reactions. Biochemistry 29 (1990) 3061-3066
63. Pappenburger G., Bachmann A., Muller R., Aygun H., Engels J.W., and Kiefhaber T. Kinetic mechanism and catalysis of a native-state prolyl isomerisation reaction. J. Mol. Biol. 326 (2003) 235-246
64. Schindler T., Herrler M., Marahiel M.A., and Schmid F.X. Extremely rapid protein folding in the absence of intermediates. Nature Struct. Biol. 2 (1995) 663-673
65. Plaxco K.W., Guijarro J.L., Morton C.J., Pitkeathly M., Campbell I.D., and Dobson C.M. The folding kinetics and thermodynamics of the Fyn-SH3 domain. Biochemistry 37 (1998) 2529-2537
66. Cook K.H., Schmid F.X., and Baldwin R.L. Role of proline isomerisation in the folding of ribonuclease A at low temperatures. Proc. Natl Acad. Sci. USA 76 (1979) 6157-6161
67. Krebs H., Schmid F.X., and Jaenicke R. Refolding of four RNases. Biochemistry 24 (1985) 3848-3852
68. Kiefhaber T., Grunert H.P., Hahn U., and Schmid F.X. Folding of RNase T1 is decelerated by a specific tertiary contact in a folding intermediate. Proteins: Struct. Funct. Genet. 12 (1992) 171-179
69. Williamson M.P. The structure and function of proline-rich regions of proteins. Biochem. J. 197 (1994) 249-260
70. Siligardi G., and Drake A.F. The importance of extended conformations and, in particular, the PII conformation for the molecular recognition of peptides. Biopolymers 37 (1995) 281-292
71. Plaxco K.W., Spitzfaden C., Campbell I.D., and Dobson C.M. Rapid refolding of a proline-rich all β-sheet fibronectin type III module. Proc. Natl Acad. Sci. USA 93 (1996) 10703-10706
72. Simpson E.R., Meldrum J.K., Bofill R., Crespo M.D., Holmes E., and Searle M.S. Engineering enhanced protein stability through β-turn optimisation: insights for the design of stable peptide β-hairpin systems. Angew. Chem. Int. Ed. 44 (2005) 4939-4944
73. Simpson E.R., Meldrum J.K., and Searle M.S. Engineering diverse changes in β-turn propensities in the N-terminal β-hairpin of ubiquitin reveals significant effects on stability and kinetics but a robust folding transition state. Biochemistry 45 (2006) 4220-4230
74. Pace N.C., and Scholtz J.M. In: Creighton T.E. (Ed). Protein Structure-A Practical Approach. 2nd Edit, (1997), IRL Press, New York
75. Schmid F.X. Mechanism of folding of ribonuclease A. Slow refolding is a sequential reaction via structural intermediates. Biochemistry 22 (1983) 4690-4696