Kinetics of loop formation and breakage in the denatured state of iso-1-cytochrome c

Journal of Molecular Biology

Volumn 353, Issue 3, 2005, Pages 730-743

  Kurchan, Eydiejo ^a   Roder, Heinrich ^b   Bowler, Bruce E ^a  

^a UNIVERSITY OF DENVER   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

Denatured states; Loop formation kinetics; Protein folding; Residual structure; Scaling properties

Indexed keywords

CYTOCHROME C; HEME; HISTIDINE;

AMINO ACID SEQUENCE; ARTICLE; DENATURATION; FLOW MEASUREMENT; KINETICS; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON TRANSPORT;

KOBUS;

EID: 26244436812     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.08.034     Document Type: Article

References (66)

1. D.J. Thirumalai Time scales for the formation of the most probable tertiary contacts in proteins with application to cytochrome c J. Phys. Chem. B 103 1999 608 610
2. W.A. Eaton, V. Munoz, P.A. Thompson, E.R. Henry, and J. Hofrichter Kinetics and dynamics of loops, α-helicies, β-hairpins, and fast-folding proteins Accts Chem. Res. 31 1989 745 753
3. O. Bieri, J. Wirz, B. Heltrung, M. Schutkowski, M. Drewello, and J. Kiefhaber The speed limit for protein folding measured by triplet-triplet energy-transfer Proc. Natl Acad. Sci. USA 96 1999 9597 9601
4. M. Buscaglia, B. Schuler, L.J. Lapidus, W.A. Eaton, and J. Hofrichter Kinetics of intramolecular contact formation in a denatured protein J. Mol. Biol. 332 2003 9 12
5. R.R. Hudgins, F. Huang, G. Gramlich, and W.M. Nau A fluorescence based method for direct measurement of submicrosecond intramolecular contact formation in biopolymers: an exploratory study with polypeptides J. Am. Chem. Soc. 124 2002 556 564
6. H. Neuweiler, A. Schulz, M. Bohmer, J. Enderlein, and M. Sauer Measurement of submicrosecond intramolecular contact formation in peptides at the single-molecule level J. Am. Chem. Soc. 125 2003 5324 5330
7. C. Tanford Protein denaturation Advan. Protein Chem. 23 1968 121 282
8. D. Shortle The denatured state (the other half of the folding equation) and its role in protein stability FASEB J. 10 1996 27 34
9. K.A. Dill Polymer principles and protein folding Protein Sci. 8 1999 1166 1180
10. E. Wandschneider, and B.E. Bowler Conformational properties of the iso-1-cytochrome c denatured state: dependence on guanidine hydrochloride concentration J. Mol. Biol. 339 2004 185 197
11. B.N. Hammack, C.R. Smith, and B.E. Bowler Denatured state thermodynamics: residual structure, chain stiffness and scaling factors J. Mol. Biol. 311 2001 1091 1104
12. S. Godbole, B. Hammack, and B.E. Bowler Measuring denatured state energetics: deviations from random coil behavior and implications for the folding of iso-1-cytochrome c J. Mol. Biol. 296 2000 217 228
13. S. Godbole, and B.E. Bowler A histidine variant of yeast iso-1-cytochrome c that strongly affects the energetics of the denatured state J. Mol. Biol. 268 1997 816 821
14. D. Neri, M. Billeter, G. Wider, and K. Wüthrich NMR determination of residual structure in a urea-denatured protein the 434-repressor Science 257 1992 1559 1563
15. D. Shortle, and M.S. Ackerman Persistence of native-like topology in a denatured protein in 8 M urea Science 293 2001 487 489
16. J. Klein-Seetharaman, M. Oikawa, S.B. Grimshaw, J. Wirmer, E. Duchardt, and T. Ueda Long-range interactions within a nonnative protein Science 295 2002 1719 1722
17. J.C. Lee, K.C. Engman, F.A. Tezcan, H.B. Gray, and J.R. Winkler Structural features of cytochrome c′ folding intermediates revealed by fluorescence energy transfer kinetics Proc. Natl Acad. Sci. USA 99 2002 14778 14782
18. V. Daggett, and A.R. Fersht Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28 2003 18 25
19. Roder, H., Maki, K., Latypov, R. F., Cheng, H. & Shastry, M. C. R. (2005). Early events in protein folding explored by rapid mixing methods. In Protein Folding Handbook, Part I, Wiley-VCH, Weinheim pp. 491-535.
20. H. Roder, and M.C.R. Shastry Methods for exploring early events in protein folding Curr. Opin. Struct. Biol. 9 1999 620 626
21. C.M. Jones, E.R. Henry, Y. Hu, C. Chan, S.D. Luck, and A. Bhuyan Fast events in protein folding initiated by nanosecond laser photolysis Proc. Natl Acad. Sci. USA 90 1993 11860 11864
22. J.D. Bryngelson, and P.G. Wolynes Spin glasses and the statistical mechanics of protein folding Proc. Natl Acad. Sci. USA 84 1987 7524 7528
23. J.D. Bryngelson, J.N. Onuchic, N.D. Socci, and P.G. Wolynes Funnels, pathways, and the energy landscape of protein folding: a synthesis Proteins: Struct. Funct. Genet. 21 1995 167 195
24. M. Karplus, and D.L. Weaver Protein folding dynamics: the diffusion-collision model and experimental data Protein Sci. 3 1994 4650 4668
25. S.J. Hagen, J. Hofrichter, A. Szabo, and W.A. Eaton Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding Proc. Natl Acad. Sci. USA 93 1996 11615 11617
26. S.J. Hagen, J. Hofrichter, and W.A. Eaton Rate of intrachain diffusion of unfolded cytochrome c J. Phys. Chem. B 101 1997 2352 2365
27. L.J. Lapidus, W.A. Eaton, and J. Hofrichter Measuring the rate of intramolecular contact formation in polypeptides Proc. Natl Acad. Sci. USA 97 2000 7220 7225
28. 5(His-33)-Zn-cytochrome c Proc. Natl Acad. Sci. USA 100 2003 3838 3840
29. F. Krieger, B. Fierz, O. Bieri, M. Drewello, and T. Kiefhaber Dynamics of unfolded polypeptide chains as models for the earliest steps in protein folding J. Mol. Biol. 332 2003 265 274
30. A. Möglich, F. Krieger, and T. Kiefhaber Molecular basis for the effect of urea and guanidinium chloride on the dynamics of unfolded polypeptide chains J. Mol. Biol. 345 2005 153 162
31. S.J. Hagen, L. Qiu, and S.A. Pabit Diffusional limits to the speed of protein folding: fact or friction? J. Phys.: Condensed Matter 17 2005 S1503 S1514
32. K.A. Dill, K.M. Fiebig, and H.S. Chan Cooperativity in proteins Proc. Natl Acad. Sci. USA 90 1993 1942 1946
33. T.R. Weikl, and K.A. Dill Folding rates and low-entropy-loss routes of two state proteins J. Mol. Biol. 329 2003 585 598
34. T.R. Weikl, and K.A. Dill Folding kinetics of two-state proteins: effect of circularization, permutation and crosslinks J. Mol. Biol. 332 2003 953 963
35. J. Clarke, A.M. Hounslow, C.J. Bond, A.R. Fersht, and V. Daggett The effects of disulfide bonds on the denatured state of barnase Protein Sci. 9 2000 2394 2404
36. S.V. Kuznetsov, Y. Shen, A.S. Benight, and A. Ansari A semiflexible polymer model applied to loop formation in DNA hairpins Biophys. J. 81 2001 2864 2875
37. Y. Shen, S.V. Kuznetsov, and A. Ansari Loop dependence of the dynamics of DNA hairpins J. Phys. Chem. B 105 2001 12202 12211
38. H.S. Chan, and K.A. Dill The effects of internal constants on the configurations of chain-molecules J. Chem. Phys. 92 1990 3118 3138
39. S. Redner Distribution functions in the interior of polymer chains J. Phys. A 12 1980 3525 3541
40. H.S. Chan, and K.A. Dill Polymer principles in protein structure and stability Annu. Rev. Biophys. Biophys. Chem. 20 1991 447 490
41. A. Ansari, Y. Shen, and S.V. Kuznetsov Misfolded loops decrease the effective rate of DNA hairpin formation Phys. Rev. Letters 88 2002 069801
42. C.R. Smith, N. Mateljevic, and B.E. Bowler Effects of topology and excluded volume on protein denatured state conformational properties Biochemistry 41 2002 10173 10181
43. A.M. Berghuis, J.G. Guillemette, G. McLendon, F. Sherman, M. Smith, and G.D. Brayer The role of a conserved internal water molecule and its associated hydrogen bond network in cytochrome c J. Mol. Biol. 236 1994 786 799
44. G. Das, D.R. Hickey, D. McLendon, G. McLendon, and F. Sherman Dramatic thermostabilization of yeast iso-1-cytochrome c by an asparagine→isoleucine replacement at position 57 Proc. Natl Acad. Sci. USA 86 1989 496 499
45. P. Regenfuss, R.M. Clegg, M.J. Fulwyler, F.J. Barrantes, and T.M. Jovin Mixing liquids in microseconds Rev. Sci. Instrum. 56 1985 283 290
46. M.C.R. Shastry, S.D. Luck, and H. Roder A continuous-flow capillary mixing method to monitor reactions on the microsecond time scale Biophys. J. 74 1998 2714 2721
47. 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
48. H. Roder, K. Maki, H. Cheng, and M.C. Shastry Rapid mixing methods for exploring the kinetics of protein folding Methods 34 2004 15 27
49. L.A. Davis, A. Schejter, and G.P. Hess Alkaline isomerization of oxidized cytochrome c J. Biol. Chem. 249 1973 2624 2632
50. E. Wandschneider, B.N. Hammack, and B.E. Bowler Evaluation of cooperative interactions between substructures of iso-1-cytochrome c using double mutant cycles Biochemistry 42 2003 10659 10666
51. C.R. Smith, E. Wandschneider, and B.E. Bowler Effect of pH on the iso-1-cytochrome c denatured state: changing constraints due to heme ligation Biochemistry 42 2003 2174 2184
52. Adams, P. A., Baldwin, D. A. & Marques, H. M. (1996). The hemepeptides from cytochrome c: preparation, physical and chemical properties, and their use as model compounds for the hemoproteins. In Cytochrome c: A Multidisciplinary Approach (Scott, R. A. & Mauk, A. G., eds), pp. 635-692, University Science Books, Sausalito, CA.
53. S.J. Hagen, R.F. Latypov, D.A. Dolgikh, and H. Roder Rapid intrachain binding of histidine-26 and hisitidine-33 to heme in unfolded ferrocytochrome c Biochemistry 41 2002 1372 1380
54. H.T. Tran, X. Wang, and R. Pappu Reconciling observations of sequence-specific conformational properties with the generic polymeric behavior of denatured proteins Biochemistry 44 2005 11369 11380
55. J.E. Kohn, I.S. Millet, J. Jacob, B. Zagrovic, T.M. Dillon, and N. Cingel Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl Acad. Sci. USA 101 2004 12491 12496
56. N.C. Fitzkee, and G.D. Rose Reassessing random-coil statistics in unfolded proteins Proc. Natl Acad. Sci. USA 101 2004 12497 12502
57. C.J. Camacho, and D. Thurumalai Theoretical predictions of folding pathways by using the proximity rule, with application to bovine pancreatic trypsin inhibitor Proc. Natl Acad. Sci. USA 92 1995 1277 1281
58. E.V. Pletneva, H.B. Gray, and J.R. Winkler Many faces of the unfolded state: conformational heterogeneity in denatured yeast cytochrome c J. Mol. Biol. 345 2005 855 867
59. J.M. Sauder, and H. Roder Amide protections in early folding intermediates of cytochrome c Fold. Des. 3 1998 293 301
60. D. Eisenberg, E. Schwartz, M. Kamaromy, and R. Wall Analysis of membrane and surface protein sequences with the hydrophobic moment plot J. Mol. Biol. 179 1984 125 142
61. B.T. Nall, and M.M. Pierce Coupled kinetic traps in cytochrome c folding: His-heme misligation and proline isomerization J. Mol. Biol. 298 2000 955 969
62. J.G.B. Northey, A.A. Di Nardo, and A.R. Davidson Hydrophobic core packing in the SH3 domain folding transition state Nature Struct. Biol. 9 2002 126 130
63. H. Kaya, and H.S. Chan Simple two-state folding kinetics requires near-Levinthal thermodynamic cooperativity Proteins: Struct. Funct. Genet. 52 2003 510 523
64. H.S. Chan, S. Shimizu, and H. Kaya Cooperativity principles in protein folding Methods Enzymol. 380 2004 350 379
65. W.B.R. Pollock, F.I. Rosell, M.B. Twichett, M.E. Dumont, and A.G. Mauk Bacterial expression of a mitochondrial cytochrome c. Trimethylation of Lys 73 in yeast iso-1-cytochrome c and the alkaline conformational transition Biochemistry 37 1998 6124 6131
66. B. Tonomura, H. Nakatani, M. Ohnishi, J. Yamaguchi-Ito, and K. Hiromi Test reactions for a stopped-flow apparatus. Reduction of 2,6- dichlorophenolindophenol and potassium ferricyanide by l-ascorbic acid Anal. Biochem. 84 1978 370 383