Symmetric connectivity of secondary structure elements enhances the diversity of folding pathways

Journal of Molecular Biology

Volumn 353, Issue 5, 2005, Pages 1171-1186

  Klimov, Dmitri K ^a   Thirumalai, D ^b  

^a GEORGE MASON UNIVERSITY   (United States)

^b Bldg 142   (United States)

Author keywords

Folding and unfolding pathways; Native symmetry; Secondary structure connectivity; Structural database analysis; Symmetry index

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; DATA BASE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SIMULATION; WILD TYPE;

EID: 27144510594     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.09.029     Document Type: Article

References (62)

1. D. Baker A surprising simplicity of protein folding Nature 405 2000 39 42
2. A.R. Fersht 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. USA 97 2000 1525 1529
3. D. Riddle, V. Grantcharova, J. Santiago, E. Aim, I. Ruczinski, and D. Baker Experiment and theory highlight role of native topology in SH3 folding Nature Struct. Biol. 6 1999 1016 1024
4. J.C. Martinez, and L. Serrano The folding transition states between SH3 domains is conformationally restricted and evolutionary conserved Nature Struct. Biol. 6 1999 1010 1016
5. D.K. Klimov, and D. Thirumalai Stiffness of the distal loop restricts the structural heterogeneity of the transition state ensemble in SH3 domains J. Mol. Biol. 315 2002 721 737
6. R. Guerois, and L. Serrano The SH3-fold family: experimental evidence and prediction of variations in the folding pathways J. Mol. Biol. 304 2000 967 982
7. J.-E. Shea, J.N. Onuchic, and C.L. Brooks Probing the folding free energy landscape of the src-SH3 protein domain Proc. Natl Acad. Sci. USA 99 2002 16064 16068
8. T. Ternstrom, U. Mayor, M. Akke, and M. Oliveberg From snapshot to movie: φ analysis of protein folding transition states taken one step further Proc. Natl Acad. Sci. USA 96 1999 14854 14859
9. V. Villegas, J.C. Martinez, F.X. Aviles, and L. Serrano Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain J. Mol. Biol. 283 1998 1027 1036
10. M. Oliveberg Characterization of the transition states for protein folding: towards a new level of mechanistic details in protein engineering analysis Curr. Opin. Struct. Biol. 11 2001 94 100
11. D.E. Otzen, and M. Oliveberg Conformational plasticity in folding of the split β-α-β protein S6: evidence for burst-phase disruption of the native state J. Mol. Biol. 317 2002 613 627
12. I.A. Hubner, M. Oliveberg, and E.I. Shakhnovich Simulation, experiment, and evolution: understanding nucleation in protein S6 folding Proc. Natl Acad. Sci. USA 101 2004 8354 8359
13. J. Clarke, E. Cota, S. Fowler, and S. Hamill Folding studies of immunoglobulin-like β-sandwich proteins suggest that they share a common folding pathway Struct. Fold. Des. 7 1999 1145 1153
14. C.D. Geierhaas, E. Paci, M. Vendruscolo, and J. Clarke Comparison of the transition states for folding of two Ig-like proteins from different superfamilies J. Mol. Biol. 343 2004 1111 1123
15. A.R. Viguera, L. Serrano, and M. Wilmanns Different folding transition states may result in the same native structure Nature Stract. Biol. 3 1996 874 880
16. V.P. Grantcharova, and D. Baker Circularization changes the folding transition state in the src SH3 domain J. Mol. Biol. 306 2001 555 563
17. M.O. Lindberg, J. Tangrot, D.E. Otzen, D.A. Dolgikh, A.V. Finkelstein, and M. Oliveberg Folding of circular permutants with decreased contact order: general trend balanced by protein stability J. Mol. Biol. 314 2001 891 900
18. M. Lindberg, J. Tangrot, and M. Oliveberg Complete change of the protein folding transition state upon circular permutation Nature Struct. Biol. 9 2002 818 822
19. D.E. Otzen, and M. Oliveberg Conformational plasticity in folding of the split β-α-β protein S6: evidence for burst-phase disruption of the native state J. Mol. Biol. 317 2002 613 627
20. D.K. Klimov, and D. Thirumalai Lattice models for proteins reveal multiple folding nuclei for nucleation-collapse mechanism J. Mol. Biol. 282 1998 471 492
21. L. Li, and E. Shakhnovich Different circular permutations produced different folding nuclei in proteins: a computational study J. Mol. Biol. 306 2001 121 132
22. P. Ferrara, and A. Caflisch Native topology or specific interactions: what is more important for protein folding? J. Mol. Biol. 306 2001 837 850
23. R. Davis, C.M. Dobson, and M. Vendruscolo Determination of the structures of distinct transition state ensembles for a β-sheet peptide with parallel folding pathways J. Chem. Phys. 117 2002 9510 9517
24. N. Go Theoretical studies of protein folding Annu. Rev. Biophys. Bioeng. 12 1983 183 210
25. J.N. Onuchic, and P.C. Wolynes Theory of protein folding Curr. Opin. Struct. Biol. 14 2004 70 75
26. C. Clementi, P. Jennings, and J. Onuchic How native-state topology affects the folding of dihydrofolate reductase and interleukin-l Proc. Natl Acad. Sci. USA 97 2000 5871 5876
27. C. Clementi, P.A. Jennings, and J.N. Onuchic Prediction of folding mechanism for circular-permuted proteins J. Mol. Biol. 311 2001 879 890
28. D.K. Klimov, and D. Thirumalai Mechanisms and kinetics of β-hairpin formation Proc. Natl Acad. Sci. USA 97 2000 2544 2549
29. E. Alm, and D. Baker Matching theory and experiment in protein folding Curr. Opin. Struct. Biol. 9 1999 189 196
30. P.G. Wolynes Symmetry and the energy landscape of biomolecules Proc. Natl Acad. Sci. USA 93 1996 14249 14255
31. S.S. Plotkin, and J.N. Onuchic Investigation of routes and funnels in protein folding by free energy functional methods Proc. Natl Acad. Sci. USA 97 2000 6509 6514
32. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures unfolding J. Mol. Biol. 247 1995 536 540
33. D.K. Klimov, and D. Thirumalai Cooperativity in protein folding: from lattice models with side chains to real proteins Fold. Des. 3 1998 127 139
34. M.C.R. Shastry, and H. Roder Evidence for barrier-limited protein folding kinetics on the microsecond time scale Nature Struct. Biol. 5 1998 385 392
35. R.L. Baldwin, and G.D. Rose Is protein folding hierarchic? I. Local structure and peptide folding Trends Biochem. Sci. 24 1999 26 33
36. R.L. Baldwin, and G.D. Rose Is protein folding hierarchic? II. Folding intermediates and transition states Trends Biochem. Sci. 24 1999 77 83
37. D.K. Klimov, and D. Thirumalai Progressing from folding trajectories to transition state ensemble in proteins Chem. Phys. 307 2004 251 258
38. E. McCallister, E. Alm, and D. Baker Critical role of β-hairpin in protein G folding Nature Struct. Biol. 7 2000 669 673
39. P. Kim, and R.L. Baldwin Intermediates in the folding reactions of small proteins Annu. Rev. Biochem. 59 1990 631 660
40. J.C. Martinez, A.R. Viguera, R. Berisio, M. Wilmanns, P.L. Mateo, V.V. Filimonov, and L. Serrano Thermodynamic analysis of α-spectrin SH3 and two of its circular permutants with different loop length: descerning the reasons for rapid folding in proteins Biochemistry 38 1999 549 559
41. H. Gu, D. Kim, and D. Baker Contrasting roles for symmetrically disposed α-turns in the folding of a small protein J. Mol. Biol. 274 1997 588 596
42. D.E. Kim, C. Fisher, and D. Baker A breakdown of symmetry in the folding transition state of protein L J. Mol. Biol. 298 2000 971 984
43. K. Kuwata, R. Shastry, H. Cheng, M. Hashino, C. Batt, Y. Goto, and H. Roder Structural and kinetic characterization of early folding events in α-lactoglobulin Nature Struct. Biol. 8 2001 151 155
44. C. Camacho, and D. Thirumalai Theoretical predictions of folding pathways using the proximity rule with applications to BPTI Proc. Natl Acad. Sci. USA 92 1995 1277 1281
45. V. Dagget, and M. Levitt A model of the molten globule state from molecular dynamics simulations Proc. Natl Acad. Sci. USA 89 1992 5142 5146
46. A. Li, and V. Daggett Molecular dynamics simulations of the unfolding of barnase: characterization of the major intermediate J. Mol. Biol. 275 1998 677 694
47. C.L. Brooks Simulations of protein folding and unfolding Curr. Opin. Struct. Biol. 8 1998 222 226
48. V. Daggett Long timescale simulations Curr. Opin. Struct. Biol. 10 1998 160 164
49. A.R. Dinner, and M. Karplus Is protein unfolding the reverse of protein folding? A lattice simulation analysis J. Mol. Biol. 292 1999 403 419
50. J.-E. Shea, and C.L. Brooks 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
51. C.F. Wright, K. Lindorff-Larsen, L.G. Randles, and J. Clarke Parallel protein-unfolding pathways revealed and mapped Nature Struct. Biol. 10 2003 658 662
52. A.R. Fersht Characterizing transition states in protein folding Curr. Opin. Struct. Biol. 5 1995 79 84
53. K. Plaxco, K. Simons, and D. Baker Contact order, transition state placement and the refolding rates of single domain proteins J. Mol. Biol. 277 1998 985 994
54. D.N. Ivankov, S.O. Garbuzynskiy, E. Alm, K.W. Plaxco, D. Baker, and A.V. Finkelstein Contact order revisited: influence of protein size on the folding rate Protein Sci. 12 2003 2057 2062
55. K.A. Dill, S. Bromberg, K. Yue, K.M. Fiebig, D.P. Yee, P.D. Thomas, and H.S. Chan Principles of protein folding-a perspective from simple exact models Protein Sci. 1995 1995 561 602
56. D. Thirumalai, and D.K. Klimov Deciphering the timescales and mechanisms of protein folding using minimal off-lattice models Curr. Opin. Struct. Biol. 9 1999 197 207
57. T. Veitshans, D.K. Klimov, and D. Thirumalai Protein folding kinetics: time scales, pathways, and energy landscapes in terms of sequence dependent properties Fold. Des. 2 1997 1 22
58. D.K. Klimov, M.R. Betancourt, and D. Thirumalai Virtual atom representation of hydrogen bonds in minimal off-lattice models of α-helices: effect on stability, cooperativity and folding kinetics Fold. Des. 3 1998 481 496
59. E. Shakhnovich, and A.M. Gutin A new approach to the design of stable proteins Protein Eng. 6 1993 793 800
60. E. Shakhnovich Proteins with selected sequences fold into unique native conformation Phys. Rev. Letters 72 1994 3907 3910
61. A.M. Ferrenberg, and R.H. Swendsen Optimized Monte Carlo data analysis Phys. Rev. Letters 63 1989 1195 1198
62. R. Koradi, M. Billeter, and K. Wuthrich Molmol: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55