Implementation of a k/k0 Method to Identify Long-Range Structure in Transition States during Conformational Folding/Unfolding of Proteins

Structure

Volumn 15, Issue 10, 2007, Pages 1178-1189

  Pradeep, Lovy ^a   Kurinov, Igor ^a,b   Ealick, Steven E ^a   Scheraga, Harold A ^a  

^a Cornell University ^*  (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

PROTEINS

Indexed keywords

PANCREATIC RIBONUCLEASE; RIBONUCLEASE A;

ARTICLE; CRYSTAL STRUCTURE; DISULFIDE BOND; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; QUALITATIVE ANALYSIS; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ALANINE; ANIMALS; ARGININE; CATTLE; CRYSTALLOGRAPHY, X-RAY; GUANIDINE; HYDROGEN-ION CONCENTRATION; KINETICS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; RIBONUCLEASE, PANCREATIC; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS; VALINE;

BOVINAE;

EID: 35048900505     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.08.003     Document Type: Article

References (60)

1. Anfinsen C.B. The limited digestion of ribonuclease with pepsin. J. Biol. Chem. 221 (1956) 405-412
2. Anfinsen C.B., and Scheraga H.A. Experimental and theoretical aspects of protein folding. Adv. Protein Chem. 29 (1975) 205-300
3. Arcus V.L., Vuilleumier S., Freund S.M., Bycroft M., and Fersht A.R. A comparison of the pH, urea, and temperature-denatured states of barnase by heteronuclear NMR: implications for the initiation of protein folding. J. Mol. Biol. 254 (1995) 305-321
4. Beals J.M., Haas E., Krausz S., and Scheraga H.A. Conformational studies of a peptide corresponding to a region of the C-terminus of ribonuclease A: implications as a potential chain-folding initiation site. Biochemistry 30 (1991) 7680-7692
5. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
6. Buckler D.R., Haas E., and Scheraga H.A. Analysis of the structure of ribonuclease A in native and partially denatured states by time-resolved nonradiative dynamic excitation energy transfer between site-specific extrinsic probes. Biochemistry 34 (1995) 15965-15978
7. Burton R.E., Huang G.S., Daugherty M.A., Calderone T.L., and Oas T.J. The energy landscape of a fast-folding protein mapped by Ala → Gly substitutions. Nat. Struct. Biol. 4 (1997) 305-310
8. Capaldi A.P., Kleanthous C., and Radford S.E. Im7 folding mechanism: misfolding on a path to the native state. Nat. Struct. Biol. 9 (2002) 209-216
9. Chavez Jr. L.G., and Scheraga H.A. Folding of ribonuclease, S-protein, and des (121-124)-ribonuclease during glutathione oxidation of reduced proteins. Biochemistry 19 (1980) 996-1004
10. Chavez Jr. L.G., and Scheraga H.A. Intrinsic stabilities of portions of the ribonuclease molecule. Biochemistry 19 (1980) 1005-1012
11. Clarke J., and Fersht A.R. Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation. Biochemistry 32 (1993) 4322-4329
12. Dill K.A., and Shortle D. Denatured states of proteins. Annu. Rev. Biochem. 60 (1991) 795-825
13. Dodge R.W., and Scheraga H.A. Folding and unfolding kinetics of the proline-to-alanine mutants of bovine pancreatic ribonuclease A. Biochemistry 35 (1996) 1548-1559
14. Dyson H.J., and Wright P.E. Equilibrium NMR studies of unfolded and partially folded proteins. Nat. Struct. Biol. 5 (1998) 499-503
15. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
16. Feng H., Vu N.-D., Zhou Z., and Bai Y. Structural examination of F{cyrillic}-value analysis in protein folding. Biochemistry 43 (2004) 14325-14331
17. Fersht A.R., Matouschek A., and Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224 (1992) 771-782
18. Fujioka H., and Scheraga H.A. Structural studies of ribonuclease. XVIII. An investigation of the peptic digestion products of ribonuclease. Biochemistry 4 (1965) 2197-2205
19. Grantcharova V.P., Riddle D.S., Santiago G.V., and Baker D. Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nat. Struct. Biol. 5 (1998) 714-720
20. Gruebele M. An intermediate seeks gratification. Nat. Struct. Biol. 9 (2002) 154-155
21. Houry W.A., and Scheraga H.A. Nature of the unfolded state of ribonuclease A: effect of cis-trans X-Pro peptide bond isomerization. Biochemistry 35 (1996) 11719-11733
22. Houry W.A., and Scheraga H.A. Structure of a hydrophobically collapsed intermediate on the conformational folding pathway of ribonuclease A probed by hydrogen-deuterium exchange. Biochemistry 35 (1996) 11734-11746
23. Ittah V., and Haas E. Nonlocal interactions stabilize long range loops in the initial folding intermediates of reduced bovine pancreatic trypsin inhibitor. Biochemistry 34 (1995) 4493-4506
24. Kauzmann W. Relative probabilities of isomers in cystine-containing randomly coiled polypeptides. In: Benesch R., Benesch R.E., Boyer P.D., Klotz I.M., Middlebrook W.R., Szent-Gyorgyi A.G., and Schwartz D.R. (Eds). Sulfur in Proteins (1959), Academic Press, New York 93-108
25. Klink T.A., and Raines R.T. Conformational stability is a determinant of ribonuclease A cytotoxicity. J. Biol. Chem. 275 (2000) 17463-17467
26. Laity J.H., Shimotakahara S., and Scheraga H.A. Expression of wild-type and mutant bovine pancreatic ribonuclease A in Escherichia coli. Proc. Natl. Acad. Sci. USA 90 (1993) 615-619
27. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26 (1993) 283-291
28. 41)-ribonuclease A. Biochemistry 23 (1984) 5504-5512
29. Lin S.H., Konishi Y., Nall B.T., and Scheraga H.A. Influence of an extrinsic cross-link on the folding pathway of ribonuclease A. Kinetics of folding-unfolding. Biochemistry 24 (1985) 2680-2686
30. Logan T.M., Thériault Y., and Fesik S.W. Structural characterization of the FK506 binding protein unfolded in urea and guanidine hydrochloride. J. Mol. Biol. 236 (1994) 637-648
31. Lopez-Hernandez E., and Serrano L. Structure of the transition state for folding of the 129 aa protein cheY resembles that of a smaller protein, CI-2. Fold. Des. 1 (1996) 43-55
32. Matheson Jr. R.R., and Scheraga H.A. A method for predicting nucleation sites for protein folding based on hydrophobic contacts. Macromolecules 11 (1978) 819-829
33. 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
34. Montelione G.T., and Scheraga H.A. Formation of local structures in protein folding. Acc. Chem. Res. 22 (1989) 70-76
35. Navon A., Ittah V., Landsman P., Scheraga H.A., and Haas E. Distributions of intramolecular distances in the reduced and denatured states of bovine pancreatic ribonuclease A. Folding initiation structures in the C-terminal portions of the reduced protein. Biochemistry 40 (2001) 105-118
36. Neri D., Billeter M., Wider G., and Wüthrich K. NMR determination of residual structure in a urea-denatured protein, the 434-repressor. Science 257 (1992) 1559-1563
37. Oliveberg M., Tan Y.-J., and Fersht A.R. Negative activation enthalpies in the kinetics of protein folding. Proc. Natl. Acad. Sci. USA 92 (1995) 8926-8929
38. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-325
39. Otzen D.E., Itzhaki L.S., elMasry N.F., Jackson S.E., and Fersht A.R. Structure of the transition state for the folding/unfolding of the barley chymotrypsin inhibitor 2 and its implications for mechanisms of protein folding. Proc. Natl. Acad. Sci. USA 91 (1994) 10422-10425
40. Pace C.N., Vajdos F., Fee L., Grimsley G., and Gray T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4 (1995) 2411-2423
41. Pappenberger G., Saudan C., Becker M., Merbach A.E., and Kiefhaber T. Denaturant-induced movement of the transition state of protein folding revealed by high pressure stopped-flow measurements. Proc. Natl. Acad. Sci. USA 97 (2000) 17-22
42. Poland D.C., and Scheraga H.A. Statistical mechanics of noncovalent bonds in polyamino acids. VIII. Covalent loops in proteins. Biopolymers 3 (1965) 379-399
43. Rothwarf D.M., and Scheraga H.A. Regeneration of bovine pancreatic ribonuclease A. 1. Steady-state distribution. Biochemistry 32 (1993) 2671-2679
44. Schindler T., and Schmid F.X. Thermodynamic properties of an extremely rapid protein folding reaction. Biochemistry 51 (1996) 16833-16842
45. Schmid F.X., and Baldwin R.L. Acid catalysis of the formation of the slow-folding species of RNase A: evidence that the reaction is proline isomerization. Proc. Natl. Acad. Sci. USA 75 (1978) 4764-4768
46. Schönbrunner N., Pappenberger G., Scharf M., Engels J., and Kiefhaber T. Effect of preformed correct tertiary interactions on rapid two-state tendamistat folding: evidence for hairpins as initiation sites for β-sheet formation. Biochemistry 36 (1997) 9057-9065
47. Schwarzinger S., Wright P.E., and Dyson H.J. Molecular hinges in protein folding: the urea-denatured state of apomyoglobin. Biochemistry 41 (2002) 12681-12686
48. Serrano L., Matouschek A., and Fersht A.R. The folding of an enzyme. 3. Structure of the transition state for unfolding of barnase analyzed by a protein engineering procedure. J. Mol. Biol. 22 (1992) 805-818
49. Shortle D. Denatured states of proteins and their roles in folding and stability. Curr. Opin. Struct. Biol. 3 (1993) 66-74
50. Sosnick T.R., and Trewhella J. Native proteins are surface-molten solids: application of the Lindemann criterion for the solid versus liquid state. Biochemistry 31 (1992) 8329-8335
51. Sosnick T.R., Dothager R.S., and Krantz B.A. Differences in the folding transition state of ubiquitin indicated by φ{symbol} and ψ analyses. Proc. Natl. Acad. Sci. USA 101 (2004) 17377-17382
52. Sosnick T.R., Krantz B.A., Dothager R.S., and Baxa M. Characterizing the protein folding transition state using ψ-analysis. Chem. Rev. 106 (2006) 1862-1876
53. Swadesh J.K., Montelione G.T., Thannhauser T.W., and Scheraga H.A. Local structure involving histidine-12 in reduced S-sulfonated ribonuclease A detected by proton NMR spectroscopy under folding conditions. Proc. Natl. Acad. Sci. USA 81 (1984) 4606-4610
54. Viguera A.R., Serrano L., and Wilmanns M. Different folding transition-states may result in the same native structure. Nat. Struct. Biol. 3 (1996) 874-880
55. Villegas V., Martinez J.C., Avilés 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
56. Wang M.C., and Uhlenbeck G.E. On the theory of the Brownian motion II. Rev. Mod. Physiol. 17 (1945) 323-342
57. 41)-ribonuclease A. J. Mol. Biol. 181 (1985) 453
58. Wedemeyer W.J., Welker E., Narayan M., and Scheraga H.A. Disulfide bonds and protein folding. Biochemistry 39 (2000) 4207-4216
59. Wlodawer A., Svensson L.A., Sjölin L., and Gilliland G.L. Structure of phosphate-free ribonuclease A refined at 1.26 Å. Biochemistry 27 (1988) 2705-2717
60. Yao J., Chung J., Eliezer D., Wright P.E., and Dyson H.J. NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding. Biochemistry 40 (2001) 3561-3571