Contact order revisited: Influence of protein size on the folding rate

Protein Science

Volumn 12, Issue 9, 2003, Pages 2057-2062

  Ivankov, Dmitry N ^a   Garbuzynskiy, Sergiy O ^a   Alm, Eric ^b   Plaxco, Kevin W ^c   Baker, David ^b   Finkelstein, Alexei V ^a  

^a INSTITUTE OF PROTEIN RESEARCH   (Russian Federation)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Contact order; Multistate kinetics; Protein folding kinetics; Protein size; Protein topology; Rate of folding; Two state kinetics

Indexed keywords

PROTEIN;

ACCURACY; ARTICLE; CONTACT ORDER; CORRELATION ANALYSIS; MATHEMATICAL MODEL; MOLECULAR SIZE; PEPTIDE ANALYSIS; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; THEORETICAL MODEL;

ANIMALS; KINETICS; MODELS, CHEMICAL; MODELS, STATISTICAL; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEINS; PROTEOMICS; THERMODYNAMICS; TIME FACTORS; WATER;

EID: 0042510944     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0302503     Document Type: Article

References (65)

1. Bernstein, F.C., Koetzle, T.F., Williams, G.J.B., Meyer, E.F., Brice, M.D., Rogers, J.R., Kennard, O., Shimanouchi, T., and Tasumi, M. 1977. The Protein Bank: A computer-based archival file for macromolecular structures. Eur. J. Biochem. 80: 319-324.
2. Burns, L.L., Dalessio, P.M., and Ropson, I.J. 1998. Folding mechanism of three structurally similar β-sheet proteins. Proteins 33: 107-118.
3. Burton, R.E., Huang, G.S., Daugherty, M.A., Fullbright, P.W., and Oas, T.G. 1996. Microsecond protein folding through a compact transition state. J. Mol. Biol. 263: 311-322.
4. Cavagnero, S., Dyson, H.J., and Wright, P.E. 1999. Effect of H helix destabilizing mutations on the kinetic and equilibrium folding of apomyoglobin. J. Mol. Biol. 285: 269-282.
5. Choe, S.E., Matsudaira, P.T., Osterhout, J., Wagner, G., and Shakhnovich, E.I. 1998. Folding kinetics of villin 14T, a protein domain with a central β-sheet and two hydrophobic cores. Biochemistry 37: 14508-14518.
6. Clarke, J., Hamill, S.J., and Johnson, C.M. 1997. Folding and stability of a fibronectin type III domain of human tenascin. J. Mol. Biol. 270: 771-778.
7. Clarke, J., Cota, E., Fowler, S.B., and Hamill, S.J. 1999. Folding studies of immunoglobulin-like β-sandwich proteins suggest that they share a common folding pathway. Struct. Fold. Des. 7: 1145-1153.
8. Cota, E. and Clarke, J. 2000. Folding of β-sandwich proteins: Three-state transition of a fibronectin type III module. Protein Sci. 9: 112-120.
9. Dalessio, P.M. and Ropson, I.J. 2000. β-Sheet proteins with nearly identical structures have different folding intermediates. Biochemistry 39: 860-871.
10. Ferguson, N., Capaldi, A.P., James, R., Kleanthous, C., and Radford, S.E. 1999. Rapid folding with and without populated intermediates in the homologous four-helix proteins Im7 and Im9. J. Mol. Biol. 286: 1597-1608.
11. Fersht, A.R. 2000. Transition-state structure as a unifying basis in protein-folding mechanisms: Contact order, chain topology, stability, and the extended nucleus mechanism. Proc. Natl. Acad. Sci. 97: 1525-1529.
12. Finkelstein, A.V. and Badretdinov, A.Y. 1997a. Physical reasons for a rapid folding of stable protein structures: A solution of Levinthal's paradox. Mol. Biol. 31: 391-398.
13. -. 1997b. Rate of protein folding near the point of thermodynamic equilibrium between the coil and the most stable chain fold. Fold Des. 2: 115-121.
14. Finkelstein, A.V and Ptitsyn, O.B. 2002. Protein physics. Lectures 19-21. Academic Press, New York.
15. Fowler, S.B. and Clarke, J. 2001. Mapping the folding pathway of an immunoglobulin domain: Structural detail from ø value analysis and movement of the transition state. Struct. Fold Des. 9: 355-366.
16. Galzitskaya, O.V., Ivankov, D.N., and Finkelstein, A.V. 2001. Folding nuclei in proteins. FEBS Lett. 489: 113-118.
17. Galzitskaya, O.V., Garbuzynskiy, S.O., Ivankov, D.N., and Finkelstein, A.V. 2003. Chain length is the main determinant of the folding rate for proteins with three-state folding kinetics. Proteins 51: 162-166.
18. Golbik, R., Zahn, R., Harding, S.E., and Fersht, A.R. 1998. Thermodynamic stability and folding of GroEL minichaperones. J. Mol. Biol. 276: 505-515.
19. 2 subunit is a "molten globule." FEBS Lett. 263: 51-56.
20. Grantcharova, V.P. and Baker, D. 1997. Folding dynamics of the src SH3 domain. Biochemistry 36: 15685-15692.
21. Grantcharova, V., Alm, E.J., Baker, D., and Horwich, A.L. 2001. Mechanisms of protein folding. Curr. Opin. Struct. Biol. 11: 70-82.
22. Guerois, R. and Serrano, L. 2000. The SH3-fold family: Experimental evidence and prediction of variations in the folding pathways. J. Mol. Biol. 304: 967-982.
23. Guijarro, J.I., Morton, C.J., Plaxco, K.W., Campbell, I.D., and Dobson, C.M. 1998. Folding kinetics of the SH3 domain of PI3 kinase by real-time NMR combined with optical spectroscopy. J. Mol. Biol. 276: 657-667.
24. Gutin, A.M., Abkevich, V.I., and Shakhnovich E.I. 1996. Chain length scaling of protein folding time. Phys. Rev. Lett. 77: 5433-5436.
25. Ikura, T., Hayano, T., Takahashi, N., and Kuwajima, K. 2000. Fast folding of Escherichia coli cyclophilin A: A hypothesis of a unique hydrophobic core with a phenylalanine cluster. J. Mol. Biol. 297: 791-802.
26. Jackson, S.E. 1998. How do small single-domain proteins fold? Fold. Des. 3: R81-R91.
27. Jackson, S.E. and Fersht, A.R. 1991. Folding of chymotrypsin inhibitor 2, 1: Evidence for a two-state transition. Biochemistry 30: 10428-10435.
28. Jager, M., Nguyen, H., Crane, J.C., Kelly, J.W., and Gruebele, M. 2001. The folding mechanism of a β-sheet: The WW domain. J. Mol. Biol. 311: 373-393.
29. Jennings, P.A., Finn, B.E., Jones, B.E., and Matthews, C.R. 1993. A reexamination of the folding mechanism of dihydrofolate reductase from Escherichia coli: Verification and refinement of a four-channel model. Biochemistry 32: 3783-3789.
30. Khorasanizadeh, S., Peters, I.D., and Roder, H. 1996. Evidence for a three-state model of protein folding from kinetic analysis of ubiquitin variants with altered core residues. Nat. Struct. Biol. 3: 193-205.
31. Kim, D.E., Fisher, C., and Baker, D. 2000. A breakdown of symmetry in the folding transition state of protein L. J. Mol. Biol. 298: 971-984.
32. Koga, N., and Takada, S. 2001. Roles of native topology and chain-length scaling in protein folding: A simulation study with a Go-like model. J. Mol. Biol. 313: 171-180.
33. Kragelund, B.B., Robinson, C.V., Knudsen, J., Dobson, C.M., and Poulsen. F.M. 1995. Folding of a four-helix bundle: Studies of acyl-coenzyme A binding protein. Biochemistry 34: 7217-7224.
34. Kuhlman, B., Luisi, D.L., Evans, P.A., and Raleigh, D.P. 1998. Global analysis of the effects of temperature and denaturant on the folding and unfolding kinetics of the N-terminal domain of the protein L9. J. Mol. Biol. 284: 1661-1670.
35. Laurents, D.V., Corrales, S., Elias-Amanz, M., Sevilla, P., Rico, M., and Padmanabhan, S. 2000. Folding kinetics of phage 434 Cro protein. Biochemistry 39: 13963-13973.
36. Main, E.R., Fulton, K.F., and Jackson, S.E. 1999. Folding pathway of FKBP12 and characterisation of the transition state. J. Mol. Biol. 291: 429-444.
37. Matouschek, A., Kellis Jr., J.T., Serrano, L., Bycroft, M., and Fersht, A.R. 1990. Transient folding intermediates characterized by protein engineering. Nature 346: 440-445.
38. McCallister, E.L., Alm, E., and Baker, D. 2000. Critical role of β-hairpin formation in protein G folding. Nat. Struct. Biol. 7: 669-673.
39. Munoz, V., Lopez, E.M., Jager, M., and Serrano, L. 1994. Kinetic characterization of the chemotactic protein from Escherichia coli, CheY: Kinetic analysis of the inverse hydrophobic effect. Biochemistry 33: 5858-5866.
40. Munoz, V., Thompson, P.A., Hofrichter, J., and Eaton, W.A. 1997. Folding dynamics and mechanism of β-hairpin formation. Nature 390: 196-199.
41. Ogasahara, K. and Yutani, K. 1994. Unfolding-refolding kinetics of the tryptophan synthase α subunit by CD and fluorescence measurements. J. Mol. Biol. 236: 1227-1240.
42. Otzen, D.E. and Oliveberg, M. 1999. Salt-induced detour through compact regions of the protein folding landscape. Proc. Natl. Acad. Sci. 96: 11746-11751.
43. Parker, M.J. and Marqusee, S. 1999. The cooperativity of burst phase reactions explored. J. Mol. Biol. 293: 1195-1210.
44. Parker, M.J., Spencer, J., and Clarke, A.R. 1995. An integrated kinetic analysis of intermediates and transition states in protein folding reactions. J. Mol. Biol. 253: 771-786.
45. Parker, M.J., Sessions, R.B., Badcoe, I.G., and Clarke, A.R. 1996. The development of tertiary interactions during the folding of a large protein. Fold. Des. 1: 145-156.
46. Parker, M.J., Dempsey, C.E., Lorch, M., and Clarke, A.R. 1997. Acquisition of native β-strand topology during the rapid collapse phase of protein folding. Biochemistry 36: 13396-13405.
47. Perl, D., Welker, C., Schindler, T., Schroder, K., Marahiel, M.A., Jaenicke, R., and Schmid, F.X. 1998. Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nat. Struct. Biol. 5: 229-235.
48. Plaxco, K.W., Spitzfaden, C., Campbell, I.D., and Dobson, C.M. 1997. A comparison of the folding kinetics and thermodynamics of two homologous fibronectin type III modules. J. Mol. Biol. 270: 763-770.
49. Plaxco, K.W., Guijarro, J.I., Morton. C.J., Pitkeathly, M., Campbell, I.D., and Dobson, C.M. 1998a. The folding kinetics and thermodynamics of the Fyn-SH3 domain. Biochemistry 37: 2529-2537.
50. Plaxco, K.W., Simons, K.T., and Baker, D. 1998b. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277: 985-994.
51. Privalov, P.L. 1979. Stability of proteins: Small globular proteins. Adv. Protein Chem. 33: 167-241.
52. Reid, K.L., Rodriguez, H.M., Hillier, B.J., and Gregoret, L.M. 1998. Stability and folding properties of a model β-sheet protein, Escherichia coli CspA. Protein Sci. 7: 470-479.
53. Schindler, T., Herrler, M., Marahiel, M.A., and Schmid, F.X. 1995. Extremely rapid protein folding in the absence of intermediates. Nat. Struct. Biol. 2: 663-673.
54. Schreiber, G. and Fersht, A.R. 1993. The refolding of cis- and trans-peptidyl-prolyl isomers of barstar. Biochemistry 32: 11195-11203.
55. Schymkowitz, J.W., Rousseau, F., Irvine, L.R., and Itzhaki, L.S. 2000. The folding pathway of the cell-cycle regulatory protein p13sucl: Clues for the mechanism of domain swapping. Struct. Fold Des. 8: 89-100.
56. Silow, M. and Oliveberg, M. 1997. High-energy channeling in protein folding. Biochemistry 36: 7633-7637.
57. Spector, S. and Raleigh, D.P. 1999. Submillisecond folding of the peripheral subunit-binding domain. J. Mol. Biol. 293: 763-768.
58. Tang, K.S., Guralnick, B.J., Wang, W.K., Fersht, A.R., and Itzhaki, L.S. 1999. Stability and folding of the tumour suppressor protein p16. J. Mol. Biol. 285: 1869-1886.
59. Thirumalai, D. 1995. From minimal models to real proteins: Time scales for protein folding kinetics. J. Phys. 5: 1457-1469.
60. Thompson, P.A., Eaton, W.A., and Hofrichter. J. 1997. Laser temperature jump study of the helix⇔coil kinetics of an alanine peptide interpreted with a "kinetic zipper" model. Biochemistry 36: 9200-9210.
61. Van Nuland, N.A., Chiti, F., Taddei, N., Raugei, G., Ramponi, G., and Dobson, C.M. 1998a. Slow folding of muscle acylphosphatase in the absence of intermediates. J. Mol. Biol. 283: 883-891.
62. Van Nuland, N.A., Meijberg, W., Warner, J., Forge, V., Scheek, R.M., Robillard, G.T., and Dobson, C.M. 1998b. Slow cooperative folding of a small globular protein HPr, Biochemistry 37: 622-637.
63. Viguera, A.R., Serrano, L., and Wilmanns, M. 1996. Different folding transition states may result in the same native structure. Nat. Struct. Biol. 3: 874-880.
64. Villegas, V., Azuaga, A., Catasus, L., Reverter, D., Mateo, P.L., Aviles, F.X., and Serrano, L. 1995. Evidence for a two-state transition in the folding process of the activation domain of human procarboxypeptidase A2. Biochemistry 34: 15105-15110.
65. Wittung-Stafshede, P., Lee, J.C., Winkler, J.R., and Gray, H.B. 1999. Cytochrome b562 folding triggered by electron transfer: Approaching the speed limit for formation of a four-helix-bundle protein. Proc. Natl. Acad. Sci. 96: 6587-6590.