Dependence of the size of the initially collapsed form during the refolding of barstar on denaturant concentration: Evidence for a continuous transition

Journal of Molecular Biology

Volumn 353, Issue 3, 2005, Pages 704-718

  Sinha, Kalyan K ^a   Udgaonkar, Jayant B ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Burst phase; Collapse; Cooperativity; FRET; Non cooperative

Indexed keywords

CYSTEINE; NITROBENZOIC ACID DERIVATIVE; POLYPEPTIDE;

ANALYTIC METHOD; ARTICLE; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); DENATURATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR SIZE; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 26244466045     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.08.056     Document Type: Article

References (80)

1. V.R. Agashe, M.C. Shastry, and J.B. Udgaonkar Initial hydrophobic collapse in the folding of barstar Nature 377 1995 754 757
2. T.R. Sosnick, L. Mayne, and S.W. Englander Molecular collapse: the rate-limiting step in two state cytochrome c folding Proteins: Struct. Funct. Genet. 24 1996 413 426
3. C.K. Chan, H. Yi, S. Takahashi, D.L. Rousseau, W.A. Eaton, and J. Hofrichter Submillisecond protein folding kinetics studied by ultrarapid mixing Proc. Natl Acad. Sci. USA 94 1997 1779 1784
4. M. Lorch, J.M. Mason, J.R. Clarke, and J.M. Parker Effect of core mutations on the folding of a beta-sheet protein: implications for backbone organization in the I-state Biochemistry 38 1999 1377 1385
5. S. Akiyama, S. Takahashi, K. Ishimori, and I. Morishima Stepwise formation of α-helices during cytochrome c folding Nature Struct. Biol. 7 2000 514 520
6. J.C. O'Neill Jr, and C.R. Matthews Localized, stereochemically sensitive hydrophobic packing in an early folding intermediate of dihydrofolate reductase from Escherichia coli J. Mol. Biol. 295 2000 737 744
7. M. Arai, K. Ito, T. Inobe, M. Nakao, K. Maki, and K. Kamagata Fast compaction of α-lactalbumin during folding studied by stopped flow X-ray scattering J. Mol. Biol. 321 2002 121 132
8. B.R. Rami, and J.B. Udgaonkar Mechanism of formation of a productive molten globule form of barstar Biochemistry 41 2002 1710 1716
9. 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
10. M.M. Garcia-Mira, M. Sadqui, N. Fischer, J.M. Sanchoz-Rulz, and V. Munoz Experimental identification of downhill protein folding Science 298 2002 1291 1295
11. E.A. Lipman, B. Schuler, O. Bakajin, and W.A. Eaton Single-molecule measurement of protein folding kinetics Science 301 2003 1233 1235
12. C. Magg, and F.X. Schmid Rapid collapse precedes the fast two-state folding of the cold shock protein J. Mol. Biol. 335 2004 1309 1323
13. Y. Maki, N. Sasaki, and M. Nakata Memory effect in the chain-collapse process in a dilute polymer solution Macromolecule 37 2004 5703 5709
14. M. Sadqi, M.J. Lapidus, and V. Munoz How fast is protein hydrophobic collapse? Proc. Natl Acad. Sci. USA 100 2003 12117 12122
15. S. Enoki, K. Saeki, K. Maki, and K. Kuwajima Acid denaturation and refolding of green fluorescent protein Biochemistry 43 2004 14238 14248
16. A.R. Dinner, A. Sali, L.J. Sith, C.M. Dobson, and M. Karplus Understanding protein folding via free-energy surfaces from theory and experiment Trends Biochem. Sci. 25 2000 331 339
17. A. Sali, E. Shakhnovich, and M. Karplus How does a protein fold? Nature 369 1994 248 251
18. A.M. Gutin, V.I. Abkevich, and E.I. Shakhnovich Is burst hydrophobic collapse necessary for protein folding? Biochemistry 34 1995 3066 3076
19. H.S. Chan, and K.A. Dill Polymer principles in protein structure and stability Annu. Rev. Biophys. Biophys. Chem. 20 1991 447 490
20. A. Noppert, K. Gast, D. Zirwer, and G. Damaschun Initial hydrophobic collapse is not necessary for folding RNase A Fold. Des. 3 1998 213 221
21. J. Jacob, B. Krantz, R.S. Dothager, P. Thiyagarajan, and T.R. Sosnick Early collapse is not an obligate step in protein folding J. Mol. Biol. 338 2004 369 382
22. N. Schonbrunner, K.P. Koller, and T. Kiefhaber Folding of disulfide bonded β-sheet protein Tendamistat: rapid two-state folding without hydrophobic collapse J. Mol. Biol. 256 1997 526 538
23. K.W. Plaxco, I.S. Millett, D.J. Segel, S. Doniach, and D. Baker Chain collapse can occur concomitantly with the rate-limiting step in protein folding Nature Struct. Biol. 6 1999 554 556
24. D. Stigter, D.O.V. Alonso, and K.A. Dill Protein stability: electrostatics and compact denatured states Proc. Natl Acad. Sci. USA 88 1991 4176 4188
25. K.W. Meisner, and T.R. Sosnick Barrier-limited, microsecond folding of a stable protein measured with hydrogen exchange: implications for downhill folding Proc. Natl Acad. Sci. USA 101 2004 15639 15644
26. P.G. de Gennes Kinetics of collapse for a flexible coil J. Phys. Letters 46 1985 L-639 L-642
27. W.A. Eaton Searching for downhill scenarios in protein folding Proc. Natl Acad. Sci. USA 96 1999 5897 5899
28. M. Gruebele The fast protein folding problem Annu. Rev. Phys. Chem. 50 1999 485 516
29. W.A. Eaton, V. Munoz, S.J. Hagen, G.S. Jas, L.J. Lapidus, E.R. Henery, and J. Hofrichter Fast kinetics and mechanisms in protein folding Annu. Rev. Biophys. Biomol. Struct. 29 2000 327 359
30. J. Kubelka, J. Hofrichter, and W.A. Eaton The protein folding 'speed limit' Curr. Opin. Struct. Biol. 14 2004 76 88
31. M.C. Shastry, and H. Roder Evidence for barrier-limited protein folding kinetics on the microsecond time scale Nature Struct. Biol. 5 1998 385 392
32. N. Haruta, and T. Kitagawa Time-resolved UV resonance Raman investigation of protein folding using a rapid mixer: characterization of kinetic folding intermediates of apomyoglobin Biochemistry 41 2002 6595 6604
33. T. Uzawa, S. Akiyama, T. Kimura, S. Takahashi, K. Ishimori, I. Morishima, and T. Fujisawa Collapse and search dynamics of apomyoglobin folding revealed by sub-millisecond observations of α-helical content and compactness Proc. Natl Acad. Sci. USA 101 2004 1171 1176
34. T.R. Sosnick, M.D. Shtilerman, L. Mayne, and S.W. Englander Ultra fast signals in protein folding and the polypeptide contracted state Proc. Natl Acad. Sci. USA 94 1997 8545 8550
35. P.X. Qi, T.R. Sosnick, and S.W. Englander The burst phase in Ribonuclease A folding and solvent dependence of the unfolded state Nature Struct. Biol. 5 1998 882 884
36. L. Chen, G. Wildegger, T. Kiefhaber, K.O. Hodgson, and S. Doniach Kinetics of lysozyme refolding: structural characterization of a nonspecifically collapsed state using time-resolved X-ray scattering J. Mol. Biol. 276 1998 225 237
37. A.K. Bhuyan, and J.B. Udgaonkar Relevance of burst phase changes in optical signals of polypeptides during protein folding M. Vijayan N. Yathindra A.S. Kolaskar Perspectives in Structural Biology 1999 Universities Press Hyderabad 293
38. J. Juneja, and J.B. Udgaonkar NMR studies of protein folding Curr. Sci. 84 2003 157 172
39. L. Pradeep, and J.B. Udgaonkar Osmolytes induce structure in an early intermediate on the folding pathway of barstar J. Biol. Chem. 279 2004 40303 40313
40. B.A. Krantz, L. Mayne, J. Rubmbley, S.W. Englander, and T.R. Sosnick Fast and slow intermediate accumulation and the initial barrier mechanism in protein folding J. Mol. Biol. 324 2002 359 371
41. G. Schreiber, and A.R. Fersht The refolding of cis- and trans-peptidylprolyl isomers of barstar Biochemistry 32 1993 11195 11203
42. M.C.R. Shastry, V.R. Agashe, and J.B. Udgaonkar Quantitative analysis of the kinetics of denaturation and renaturation of barstar in the folding transition zone Protein Sci. 3 1994 1409 1417
43. M.C.R. Shastry, and J.B. Udgaonkar The folding mechanism of barstar: evidence for multiple pathways and multiple intermediates J. Mol. Biol. 247 1995 1013 1027
44. B. Nolting, R. Golbik, and A.R. Fersht Submillisecond events in protein folding Proc. Natl Acad. Sci. USA 92 1995 10668 10672
45. L. Pradeep, and J.B. Udgaonkar Differential salt-induced stabilization of structure in the initial folding intermediate ensemble of barstar J. Mol. Biol. 324 2002 331 347
46. K. Sridevi, and J.B. Udgaonkar Unfolding rates of barstar determined in native and low denaturant conditions indicate the presence of intermediates Biochemistry 41 2002 1568 1578
47. G.S. Lakshmikant, K. Sridevi, G. Krishnamoorhty, and J.B. Udgaonkar Structure is lost incrementally during the unfolding of barstar Nature Struct. Biol. 8 2001 799 804
48. K. Sridevi, and J.B. Udgaonkar Surface expansion is independent of and occurs faster than core salvation during the unfolding of barstar Biochemistry 42 2003 1551 1563
49. J.R. Lakowicz Principles of Fluorescence Spectroscopy Kluwer Academic 1999 Plenum Publishers New York
50. P. Wu, and L. Brand Resonance energy transfer: methods and applications Anal. Biochem. 218 1994 1 13
51. F. Krieger, B. Fierz, O. Bieri, M. Drewello, and T. Kiefhaber Dynamics of unfolded polypeptide chains as model for the earliest steps in protein folding J. Mol. Biol. 332 2003 265 274
52. N.S. Bhavesh, J. Juneja, J.B. Udgaonkar, and R.V. Hosur Native and nonnative conformational preferences in urea unfolded state of barstar Protein Sci. 13 2004 3085 3091
53. D.P. Goldenberg Computational simulation of the statistical properties of unfolded proteins J. Mol. Biol. 326 2003 1615 1633
54. N.C. Fitzkee, and G.D. Rose Reassessing random coil statistics in unfolded proteins Proc. Natl Acad. Sci. USA 101 2004 12497 12502
55. E.A. Lipman, B. Schuler, O. Bakajin, and W.A. Eaton Single-molecule measurement of protein folding kinetics Science 301 2003 1233 1235
56. S. Akiyama, S. Takahashi, T. Kimura, K. Ishimori, I. Morishima, Y. Nishikawa, and T. Fujisawa Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle X-ray scattering Proc. Natl Acad. Sci. USA 99 2002 1329 1334
57. B.R. Rami, G. Krishnamoorthy, and J.B. Udgaonkar Dynamics of the core tryptophan during the formation of a productive molten globule intermediate of barstar Biochemistry 42 2003 7986 8000
58. R.E. Georgescu, J.H. Lee, M.E. Goldberg, M.L. Tasayko, and A.F. Chaffotte Proline isomerization-independent accumulation of early intermediate and heterogeneity of the folding pathways of a mixed alpha/beta protein Escherichia coli thioredoxin Biochemistry 37 1998 10286 10297
59. M.J. Parker, and S. Marqusee The cooperativity of burst phase reactions explored J. Mol. Biol. 293 1999 1195 1210
60. K.A. Dill, and D. Shortle Denatured states of proteins Annu. Rev. Biochem. 60 1991 795 825
61. A.V. Finkelstein, and O.B. Ptitsyn Protein Physics 2002 Academic Press London 207 237
62. 1H NMR Biochemistry 32 1993 13198 13203
63. B.A. Schulman, P.S. Kim, C.M. Dobson, and C. Redfield A residue-specific NMR view of the non-cooperative unfolding of a molten globule Nature Struct. Biol. 4 1997 630 634
64. B.R. Rami, and J.B. Udgaonkar Mechanism of formation of a productive molten globule form of barstar Biochemistry 41 2002 1710 1716
65. U. Mayor, J.G. Grossmann, N.W. Foster, S.M.V. Freund, and A.R. Fersht The denatured state of Engrailed homeodomain under denaturing and native conditions J. Mol. Biol. 333 2003 977 991
66. S.J. Hagen, and W.A. Eaton Two-state expansion and collapse of a polypeptide J. Mol. Biol. 297 2002 781 789
67. S.J. Hagen Experimental decay kinetics in "downhill" protein folding Proteins: Struct. Funct. Genet. 50 2003 1 4
68. C. Williams, F. Brochard, and H.L. Frisch Polymer collapse Annu. Rev. Phys. Chem. 32 1981 433 451
69. D. Thirumalai From minimal models to real proteins: time scales for protein folding kinetics J. Phys. 5 1995 1457 1467
70. J. Ma, J.E. Straub, and E.I. Shakhnovich Simulation study of the collapse of linear and ring homopolymers J. Chem. Phys. 103 1995 2615 2624
71. E. Pitard, and H. Orland Dynamics of the swelling or collapse of a homopolymer Europhys. Letters 41 1998 467 472
72. K.A. Dill Dominant forces in protein folding Biochemistry 29 1990 7133 7155
73. Y.A. Kuznetsov, E.G. Timoshenko, and K.A. Dawson Kinetics of the collapse transition of homopolymers and random copolymers J. Chem. Phys. 103 1995 4807 4818
74. V.S.J. Pande, and D.S. Rokhsar Is the molten globule a third phase of proteins? Proc. Natl Acad. Sci. USA 95 1998 1490 1494
75. H.S. Chan, and K.A. Dill Origin of structure in globular proteins Proc. Natl Acad. Sci. USA 87 1990 6388 6392
76. K.A. Dill, K.M. Fiebig, and H.S. Chan Cooperitivity in protein-folding kinetics Proc. Natl Acad. Sci. USA 90 1993 1942 1946
77. K. Sridevi, J. Juneja, A.K. Bhuyan, G. Krishnamoorthy, and J.B. Udgaonkar The slow folding reaction of barstar: the core tryptophan region attains tight packing before substantial secondary and tertiary structure formation and final compaction of the polypeptide chain J. Mol. Biol. 302 2000 479 495
78. C. Frieden The kinetics of side chain stabilization during protein folding Biochemistry 42 2003 12439 12446
79. V.R. Agashe, and J.B. Udgaonkar Thermodynamics of denaturation of barstar: evidence for cold denaturation and evaluation of the interaction with guanidine hydrochloride Biochemistry 34 1995 3286 3299
80. 13C assignments of barstar using nuclear magnetic resonance spectroscopy Biochemistry 33 1994 8866 8877