Transition-States in Protein Folding Kinetics: The Structural Interpretation of Φ values

Journal of Molecular Biology

Volumn 365, Issue 5, 2007, Pages 1578-1586

  Weikl, Thomas R ^a   Dill, Ken A ^b  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

folding cooperativiy; mutational analysis; transition state structures; two state proteins

Indexed keywords

PROTEIN A; PROTEIN CI2; PROTEIN L; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; DNA HELIX; ENERGY TRANSFER; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 33846026304     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.082     Document Type: Article

References (71)

1. Itzhaki L.S., Otzen D.E., and Fersht A.R. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254 (1995) 260-288
2. Villegas V., Martinez J.C., Aviles F.X., and Serrano L. Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain. J. Mol. Biol. 283 (1998) 1027-1036
3. Chiti F., Taddei N., White P.M., Bucciantini M., Magherini F., Stefani M., and Dobson C.M. Mutational analysis of acylphosphatase suggests the importance of topology and contact order in protein folding. Nat. Struct. Biol. 6 (1999) 1005-1009
4. Ternström T., Mayor U., Akke M., and Oliveberg M. From snapshot to movie: Φ analysis of protein folding transition states taken one step further. Proc. Natl Acad. Sci. USA 96 (1999) 14854-14859
5. Fulton K.F., Main E.R.G., Daggett V., and Jackson S.E. Mapping the interactions present in the transition state for unfolding/folding of FKBP12. J. Mol. Biol. 291 (1999) 445-461
6. Kim D.E., Fisher C., and Baker D. A breakdown of symmetry in the folding transition state of protein L. J. Mol. Biol. 298 (2000) 971-984
7. McCallister E.L., Alm E., and Baker D. Critical role of β-hairpin formation in protein G folding. Nat. Struct. Biol. 7 (2000) 669-673
8. Otzen D.E., and Oliveberg M. 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
9. ‡). Proc. Natl Acad. Sci. USA 101 (2004) 7606-7611
10. Anil B., Sato S., Cho J.H., and Raleigh D.P. Fine structure analysis of a protein folding transition state; distinguishing between hydrophobic stabilization and specific packing. J. Mol. Biol. 354 (2005) 693-705
11. Went H.M., and Jackson S.E. Ubiquitin folds through a highly polarized transition state. Protein Eng. Des. Sel. 18 (2005) 229-237
12. Wilson C.J., and Wittung-Stafshede P. Snapshots of a dynamic folding nucleus in zinc-substituted Pseudomonas aeruginosa azurin. Biochemistry 44 (2005) 10054-10062
13. Kragelund B.B., Osmark P., Neergaard T.B., Schiodt J., Kristiansen K., Knudsen J., and Poulsen F.M. The formation of a native-like structure containing eight conserved hydrophobic residues is rate limiting in two-state protein folding of ACBP. Nat. Struct. Biol. 9 (1999) 594-601
14. Gianni S., Guydosh N.R., Khan F., Caldas T.D., Mayor U., White G.W.N., et al. Unifying features in protein-folding mechanisms. Proc. Natl Acad. Sci. USA 100 (2003) 13286-13291
15. Sato S., Religa T.L., Daggett V., and Fersht A.R. Testing protein-folding simulations by experiment: B domain of protein A. Proc. Natl Acad. Sci. USA 101 (2004) 6952-6956
16. Teilum K., Thormann T., Caterer N.R., Poulsen H.I., Jensen P.H., Knudsen J., et al. Different secondary structure elements as scaffolds for protein folding transition states of two homologous four-helix bundles. Proteins: Struct. Funct. Genet. 59 (2005) 80-90
17. Martinez J.C., and Serrano L. The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved. Nat. Struct. Biol. 6 (1999) 1010-1016
18. Riddle D.S., Grantcharova V.P., Santiago J.V., Alm E., Ruczinski I., and Baker D. Experiment and theory highlight role of native state topology in SH3 folding. Nat. Struct. Biol. 6 (1999) 1016-1024
19. Hamill S.J., Steward A., and Clarke J. The folding of an immunoglobulin-like greek key protein is defined by a common-core nucleus and regions constrained by topology. J. Mol. Biol. 297 (2000) 165-178
20. Fowler S.B., and Clarke J. Mapping the folding pathway of an Immunoglobulin domain: structural detail from Φ value analysis and movement of the transition state. Structure 9 (2001) 355-366
21. Cota E., Steward A., Fowler S.B., and Clarke J. The folding nucleus of a fibronection type III domain is composed of core residues of the immunoglobolin fold. J. Mol. Biol. 305 (2001) 1185-1194
22. Jäger M., Nguyen H., Crane J.C., Kelly J.W., and Gruebele M. The folding mechanism of a β-sheet: the WW domain. J. Mol. Biol. 311 (2001) 373-393
23. Northey J.G.B., Di Nardo A.A., and Davidson A.R. Hydrophobic core packing in the SH3 domain folding transition state. Nat. Struct. Biol. 9 (2002) 126-130
24. Garcia-Mira M.M., Böhringer D., and Schmid F.X. The folding transition state of the cold shock protein is strongly polarized. J. Mol. Biol. 339 (2004) 555-569
25. Matouschek A., Kellis J.T., Serrano L., and Fersht A.R. Mapping the transition state and pathway of protein folding by protein engineering. Nature 340 (1989) 122-126
26. Fersht A.R. In: Freeman W.H. (Ed). Structure and Mechanism In Protein Science (1999), New York
27. Ozkan S.B., Bahar I., and Dill K.A. Transition states and the meaning of Φ-values in protein folding kinetics. Nat. Struct. Biol. 8 (2001) 765-769
28. Zarrine-Afsar A., and Davidson A.R. The analysis of protein folding kinetic data produced in protein engineering experiments. Methods 34 (2004) 41-50
29. Chang I., Cieplak M., Banavar J.R., and Maritan A. What can one learn from experiments about the elusive transition state?. Protein Sci. 13 (2004) 2446-2457
30. Raleigh D.P., and Plaxco K.W. The protein folding transition state: what are Φ-values really telling us?. Protein Pept. Lett. 12 (2005) 117-122
31. Li A., and Daggett V. Characterization of the transition state of protein unfolding by use of molecular dynamics: chymotrypsin inhibitor 2. Proc. Natl Acad. Sci. USA 91 (1994) 10430-10434
32. Li A., and Daggett V. Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations. J. Mol. Biol. 257 (1996) 412-429
33. Lazaridis T., and Karplus M. "New View" of protein folding reconciled with the old through multiple unfolding simulations. Science 278 (1997) 1928-1931
34. Vendruscolo M., Paci E., Dobson C.M., and Karplus M. Three key residues form a critical contact network in a protein folding transition state. Nature 409 (2001) 641-645
35. Li L., and Shakhnovich E.I. Constructing, verifying, and dissecting the folding transition state of chymotrypsin inhibitor 2 with all-atom simulations. Proc. Natl Acad. Sci. USA 98 (2001) 13014-13018
36. Gsponer J., and Caflisch A. Molecular dynamics simulations of protein folding from the transition state. Proc. Natl Acad. Sci. USA 99 (2002) 6719-6724
37. Paci E., Vendruscolo M., Dobson C.M., and Karplus M. Determination of a transition state at atomic resolution from protein engineering data. J. Mol. Biol. 324 (2002) 151-163
38. Guo W., Lampoudi S., and Shea J.-E. Posttransition state desolvation of the hydrophobic core of the src-SH3 protein domain. Biophys. J. 85 (2003) 61-69
39. Settanni G., Gsponer J., and Caflisch A. Formation of the folding nucleus of an SH3 domain investigated by loosely coupled molecular dynamics simulations. Biophys. J. 86 (2004) 1691-1701
40. Paci E., Lindorff-Larsen K., Dobson C.M., Karplus M., and Vendruscolo M. Transition state contact orders correlate with protein folding rates. J. Mol. Biol. 352 (2005) 495-500
41. IJ-values. Proc. Natl Acad. Sci. USA 102 (2005) 12389-12394
42. Chong L.T., Snow C.D., Rhee Y.M., and Pande V.S. Dimerization of the p53 oligomerization domain: identification of a folding nucleus by molecular dynamics simulations. J. Mol. Biol. 345 (2005) 869-878
43. Hubner I.A., Edmonds K.A., and Shakhnovich E.I. Nucleation and the transition state of the SH3 domain. J. Mol. Biol. 349 (2005) 424-434
44. Duan J.X., and Nilsson L. Thermal unfolding simulations of a multimeric protein-transition state and unfolding pathways. Proteins: Struct. Funct. Genet. 59 (2005) 170-182
45. Daggett V., Li A., Itzhaki L.S., Otzen D.E., and Fersht A.R. Structure of the transition state for folding of a protein derived from experiment and simulation. J. Mol. Biol. 257 (1996) 430-440
46. Day R., and Daggett V. Sensitivity of the folding/unfolding transition state ensemble of chymotrypsin inhibitor 2 to changes in temperature and solvent. Protein Sci. 14 (2005) 1242-1252
47. Settanni G., Rao F., and Caflisch A. Φ-value analysis by molecular dynamics simulations of reversible folding. Proc. Natl Acad. Sci. USA 102 (2005) 628-633
48. Lindorff-Larsen K., Paci E., Serrano L., Dobson C.M., and Vendruscolo M. Calculation of mutational free energy changes in transition states for protein folding. Biophys. J. 85 (2003) 1207-1214
49. Alm E., and Baker D. Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures. Proc. Natl Acad. Sci. USA 96 (1999) 11305-11310
50. Muñoz V., and Eaton W.A. A simple model for calculating the kinetics of protein folding from three-dimensional structures. Proc. Natl Acad. Sci. USA 96 (1999) 11311-11316
51. Galzitskaya O.V., and Finkelstein A.V. A theoretical search for folding/unfolding nuclei in three-dimensional protein structures. Proc. Natl Acad. Sci. USA 96 (1999) 11299-11304
52. Clementi C., Nymeyer H., and Onuchic J.N. Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol. 298 (2000) 937-953
53. Guerois R., and Serrano L. The SH3-fold family: experimental evidence and prediction of variations in the folding pathways. J. Mol. Biol. 304 (2000) 967-982
54. Alm E., Morozov A.V., Kortemme T., and Baker D. Simple physical models connect theory and experiment in protein folding kinetics. J. Mol. Biol. 322 (2002) 463-476
55. Kameda T. Importance of sequence specificity for predicting protein folding pathways: Perturbed Gaussian chain model. Proteins: Struct. Funct. Genet. 53 (2000) 616-628
56. Goldenberg D.P. Finding the right fold. Nat. Struct. Biol. 6 (1999) 987-990
57. de los Rios M.A., Daneshi M., and Plaxco K.W. Experimental investigation of the frequency and substitution dependence of negative Φ-values in two-state proteins. Biochemistry 44 (2005) 12160-12167
58. Schuler B., Lipman E., and Eaton W.A. Probing the free-energy surface for protein folding with single molecule fluorescence spectroscopy. Nature 419 (2002) 743-747
59. Akmal A., and Muñoz V. The nature of the free energy barriers to two-state folding. Proteins: Struct. Funct. Genet. 57 (2004) 142-152
60. Merlo C., Dill K.A., and Weikl T.R. Φ values in protein-folding kinetics have energetic and structural components. Proc. Natl Acad. Sci. USA 102 (2005) 10171-10175
61. Muñoz V., and Serrano L. Elucidating the folding problem of α-helical peptides using empirical parameters: II. Helix macrodipole effects and rational modification of the helical content of natural peptides. J. Mol. Biol. 245 (1994) 275-296
62. Muñoz V., and Serrano L. Elucidating the folding problem of α-helical peptides using empirical parameters III: temperature and pH dependence. J. Mol. Biol. 245 (1994) 297-308
63. Lacroix E., Viguera A.R., and Serrano L. Elucidating the folding problem of α-helices: local motifs, long-range electrostatics, ionic strength dependence and prediction of NMR parameters. J. Mol. Biol. 284 (1998) 173-191
64. Pace C.N., and Scholtz J.M. A helix propensity scale based on experimental studies of peptides and proteins. Biophys. J. 75 (1998) 422-427
65. Serrano L., Matouschek A., and Fersht A.R. The folding of an enzyme: III. Structure of the transition state for unfolding of barnase analysed by a protein engineering procedure. J. Mol. Biol. 224 (1992) 805-818
66. Jemth P., Day R., Gianni S., Khan F., Allen M., Daggett V., and Fersht A.R. The structure of the major transition state for folding of an FF domain from experiment and simulation. J. Mol. Biol. 350 (2005) 363-378
67. Zhou Z., Huang Y.Z., and Bai Y.W. An on-pathway hidden intermediate and the early rate-limiting transition state of Rd-apocytochrome b(562) characterized by protein engineering. J. Mol. Biol. 352 (2005) 757-764
68. Scott K.A., Randles L.G., and Clarke J. The folding of spectrin domains II: Φ-value analysis of R16. J. Mol. Biol. 344 (2004) 207-221
69. Fersht A.R., and Sato S. Φ-value analysis and the nature of protein-folding transition states. Proc. Natl Acad. Sci. USA 91 (2004) 10422-10425
70. De los Rios M., Muralidhara B.K., Wildes D., Sosnick T.R., Marqusee S., Wittung-Stafshede P., et al. On the precision of experimentally determined protein folding rates and Φ-values. Protein Sci. 15 (2006) 553-563
71. Sánchez I.E., and Kiefhaber T. Origin of unusual Φ-values in protein folding: evidence against specific nucleation sites. J. Mol. Biol. 334 (2003) 1077-1085