Distinct unfolding and refolding pathways of ribonuclease a revealed by heating and cooling temperature jumps

Biophysical Journal

Volumn 94, Issue 10, 2008, Pages 4056-4065

  Torrent, Joan ^a,b   Marchal, Stéphane ^a,b   Ribó, Marc ^c   Vilanova, Maria ^c   Georges, Cédric ^d   Dupont, Yves ^d,e   Lange, Reinhard ^a,b  

^a UNIV MONTPELLIER   (France)

^b PSL RESEARCH UNIVERSITY   (France)

^c UNIVERSITY OF GIRONA   (Spain)

^d Savigne Sur   (France)

^e Laboratoire de Biophysique Moleculaire et Cellulaire   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE;

ARTICLE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COLD; COMPUTER SIMULATION; HEAT; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; ULTRASTRUCTURE;

COLD; COMPUTER SIMULATION; HEAT; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; RIBONUCLEASES;

EID: 43849098038     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.123893     Document Type: Article

References (62)

1. Ballew, R. M., J. Sabelko, and M. Gruebele. 1996. Observation of distinct nanosecond and microsecond protein folding events. Nat. Struct. Biol. 3:923-926.
2. Callender, R. H., R. B. Dyer, R. Gilmanshin, and W. H. Woodruff. 1998. Fast events in protein folding: the time evolution of primary processes. Annu. Rev. Phys. Chem. 49:173-202.
3. Huang, C. Y., Z. Getahun, Y. Zhu, J. W. Klemke, W. F. DeGrado, and F. Gai. 2002. Helix formation via conformation diffusion search. Proc. Natl. Acad. Sci. USA. 99:2788-2793.
4. Kubelka, J., W. A. Eaton, and J. Hofrichter. 2003. Experimental tests of villin subdomain folding simulations. J. Mol. Biol. 329:625-630.
5. Leeson, D. T., F. Gai, H. M. Rodriguez, L. M. Gregoret, and R. B. Dyer. 2000. Protein folding and unfolding on a complex energy landscape. Proc. Natl. Acad. Sci. USA. 97:2527-2532.
6. Munoz, V., P. A. Thompson, J. Hofrichter, and W. A. Eaton. 1997. Folding dynamics and mechanism of β-hairpin formation. Nature. 390:196-199.
7. Phillips, C. M., Y. Mizutani, and R. M. Hochstrasser. 1995. Ultrafast thermally induced unfolding of RNase A. Proc. Natl. Acad. Sci. USA. 92:7292-7296.
8. Qiu, L., S. A. Pabit, A. E. Roitberg, and S. J. Hagen. 2002. Smaller and faster: the 20-residue Trp-cage protein folds in 4 micros. J. Am. Chem. Soc. 124:12952-12953.
9. Snow, C. D., L. Qiu, D. Du, F. Gai, S. J. Hagen, and V. S. Pande. 2004. Trp zipper folding kinetics by molecular dynamics and temperature-jump spectroscopy. Proc. Natl. Acad. Sci. USA. 101:4077-4082.
10. Chavez, L. L., S. Gosavi, P. A. Jennings, and J. N. Onuchic. 2006. Multiple routes lead to the native state in the energy landscape of the β-trefoil family. Proc. Natl. Acad. Sci. USA. 103:10254-10258.
11. Dill, K. A., and H. S. Chan. 1997. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4:10-19.
12. Dinner, A. R., and M. Karplus. 1999. Is protein unfolding the reverse of protein folding? A lattice simulation analysis. J. Mol. Biol. 292:403-419.
13. Plotkin, S. S., and J. N. Onuchic. 2000. Investigation of routes and funnels in protein folding by free energy functional methods. Proc. Natl. Acad. Sci. USA. 97:6509-6514.
14. Neira, J. L., and M. Rico. 1997. Folding studies on ribonuclease A, a model protein. Fold. Des. 2:R1-R11.
15. Ribo, M., J. Font, A. Benito, J. Torrent, R. Lange, and M. Vilanova. 2006. Pressure as a tool to study protein-unfolding/refolding processes: the case of ribonuclease A. Biochim. Biophys. Acta. 1764:461-469.
16. Wedemeyer, W. J., E. Welker, M. Narayan, and H. A. Scheraga. 2000. Disulfide bonds and protein folding. Biochemistry. 39:4207-4216.
17. Wlodawer, A., L. A. Svensson, L. Sjolin, and G. L. Gilliland. 1988. Structure of phosphate-free ribonuclease A refined at 1.26 A. Biochemistry. 27:2705-2717.
18. Wedemeyer, W. J., E. Welker, and H. A. Scheraga. 2002. Proline cistrans isomerization and protein folding. Biochemistry. 41:14637-14644.
19. Torrent, J., J. P. Connelly, M. G. Coll, M. Ribo, R. Lange, and M. Vilanova. 1999. Pressure versus heat-induced unfolding of ribonuclease A: the case of hydrophobic interactions within a chain-folding initiation site. Biochemistry. 38:15952-15961.
20. Matheson, R. R., and H. A. Sheraga. 1978. Method for predicting nucleation sites for protein folding based on hydrophobic contacts. Macromolecules. 11:819-829.
21. Navon, A., V. Ittah, J. H. Laity, H. A. Scheraga, E. Haas, and E. E. Gussakovsky. 2001. Local and long-range interactions in the thermal unfolding transition of bovine pancreatic ribonuclease A. Biochemistry. 40:93-104.
22. Torrent, J., P. Rubens, M. Ribo, K. Heremans, and M. Vilanova. 2001. Pressure versus temperature unfolding of ribonuclease A: an FTIR spectroscopic characterization of 10 variants at the carboxy-terminal site. Protein Sci. 10:725-734.
23. Dragan, A. I., S. A. Potekhin, A. Sivolob, M. Lu, and P. L. Privalov. 2004. Kinetics and thermodynamics of the unfolding and refolding of the three-stranded α-helical coiled coil, Lpp-56. Biochemistry. 43: 14891-14900.
24. Oliveberg, M., and P. G. Wolynes. 2005. The experimental survey of protein-folding energy landscapes. Q. Rev. Biophys. 38:245-288.
25. Jager, M., H. Nguyen, M. Dendle, M. Gruebele, and J. W. Kelly. 2007. Influence of hPin1 WW N-terminal domain boundaries on function, protein stability, and folding. Protein Sci. 16:1495-1501.
26. Ma, H., and M. Gruebele. 2005. Kinetics are probe-dependent during downhill folding of an engineered λ6-85 protein. Proc. Natl. Acad. Sci. USA. 102:2283-2287.
27. Naganathan, A. N., U. Doshi, A. Fung, M. Sadqi, and V. Munoz. 2006. Dynamics, energetics, and structure in protein folding. Biochemistry. 45:8466-8475.
28. Nguyen, H., M. Jager, J. W. Kelly, and M. Gruebele. 2005. Engineering a β-sheet protein toward the folding speed limit. J. Phys. Chem. B. 109:15182-15186.
29. Munoz, V. 2007. Conformational dynamics and ensembles in protein folding. Annu. Rev. Biophys. Biomol. Struct. 36:395-U2.
30. Zhu, Y., D. O. Alonso, K. Maki, C. Y. Huang, S. J. Lahr, V. Daggett, H. Roder, W. F. DeGrado, and F. Gai. 2003. Ultrafast folding of α3D: a de novo designed three-helix bundle protein. Proc. Natl. Acad. Sci. USA. 100:15486-15491.
31. Makhatadze, G. I., and P. L. Privalov. 1995. Energetics of protein structure. Adv. Protein Chem. 47:307-425.
32. Bhat, R., W. J. Wedemeyer, and H. A. Scheraga. 2003. Proline isomerization in bovine pancreatic ribonuclease A. 2. Folding conditions. Biochemistry. 42:5722-5728.
33. Dodge, R. W., and H. A. Scheraga. 1996. Folding and unfolding kinetics of the proline-to-alanine mutants of bovine pancreatic ribonuclease A. Biochemistry. 35:1548-1559.
34. Garel, J. R., B. T. Nall, and R. L. Baldwin. 1976. Guanidine-unfolded state of ribonuclease A contains both fast- and slow-refolding species. Proc. Natl. Acad. Sci. USA. 73:1853-1857.
35. Houry, W. A., D. M. Rothwarf, and H. A. Scheraga. 1994. A very fast phase in the refolding of disulfide-intact ribonuclease A: implications for the refolding and unfolding pathways. Biochemistry. 33:2516-2530.
36. Juminaga, D., W. J. Wedemeyer, R. Garduno-Juarez, M. A. McDonald, and H. A. Scheraga. 1997. Tyrosyl interactions in the folding and unfolding of bovine pancreatic ribonuclease A: a study of tyrosine-to-phenylalanine mutants. Biochemistry. 36:10131-10145.
37. Juminaga, D., W. J. Wedemeyer, and H. A. Scheraga. 1998. Proline isomerization in bovine pancreatic ribonuclease A. 1. Unfolding conditions. Biochemistry. 37:11614-11620.
38. Sendak, R. A., D. M. Rothwarf, W. J. Wedemeyer, W. A. Houry, and H. A. Scheraga. 1996. Kinetic and thermodynamic studies of the folding/unfolding of a tryptophan-containing mutant of ribonuclease A. Biochemistry. 35:12978-12992.
39. Udgaonkar, J. B., and R. L. Baldwin. 1995. Nature of the early folding intermediate of ribonuclease A. Biochemistry. 34:4088-4096.
40. Welker, E., K. Maki, M. C. Shastry, D. Juminaga, R. Bhat, H. A. Scheraga, and H. Roder. 2004. Ultrarapid mixing experiments shed new light on the characteristics of the initial conformational ensemble during the folding of ribonuclease A. Proc. Natl. Acad. Sci. USA. 101:17681-17686.
41. Kimura, T., S. Akiyama, T. Uzawa, K. Ishimori, I. Morishima, T. Fujisawa, and S. Takahashi. 2005. Specifically collapsed intermediate in the early stage of the folding of ribonuclease A. J. Mol. Biol. 350: 349-362.
42. Benz, F. W., and G. C. Roberts. 1975. Nucler magnetic resonance studies of the unfolding of pancreatic ribonuclease. J. Mol. Biol. 91: 345-365.
43. Chen, M. C., and R. C. Lord. 1976. Laser Raman spectroscopic studies of the thermal unfolding of ribonuclease A. Biochemistry. 15:1889-1897.
44. Denisov, V. P., and B. Halle. 1998. Thermal denaturation of ribonuclease A characterized by water 17O and 2H magnetic relaxation dispersion. Biochemistry. 37:9595-9604.
45. Labhardt, A. M. 1982. Secondary structure in ribonuclease. I. Equilibrium folding transitions seen by amide circular dichroism. J. Mol. Biol. 157:331-355.
46. Matthews, C. R., and D. G. Westmoreland. 1975. Nuclear magnetic resonance studies of residual structure in thermally unfolded ribonuclease A. Biochemistry. 14:4532-4538.
47. Seshadri, S., K. A. Oberg, and A. L. Fink. 1994. Thermally denatured ribonuclease A retains secondary structure as shown by FTIR. Biochemistry. 33:1351-1355.
48. Sosnick, T. R., and J. Trewhella. 1992. Denatured states of ribonuclease A have compact dimensions and residual secondary structure. Biochemistry. 31:8329-8335.
49. Houry, W. A., D. M. Rothwarf, and H. A. Scheraga. 1995. The nature of the initial step in the conformational folding of disulphide-intact ribonuclease A. Nat. Struct. Biol. 2:495-503.
50. Houry, W. A., D. M. Rothwarf, and H. A. Scheraga. 1996. Circular dichroism evidence for the presence of burst-phase intermediates on the conformational folding pathway of ribonuclease A. Biochemistry. 35:10125-10133.
51. Houry, W. A., and H. A. Scheraga. 1996. Structure of a hydrophobically collapsed intermediate on the conformational folding pathway of ribonuclease A probed by hydrogen-deuterium exchange. Biochemistry. 35:11734-11746.
52. Cook, K. H., F. X. Schmid, and R. L. Baldwin. 1979. Role of proline isomerization in folding of ribonuclease A at low temperatures. Proc. Natl. Acad. Sci. USA. 76:6157-6161.
53. Balbach, J., and F. X. Schmid. 2000. Proline isomerization and its catalysis in protein folding. In Mechanism of protein folding, 2nd ed. R. H. Pain, editor. Oxford University Press, New York. 212-249.
54. Scheraga, H. A., W. J. Wedemeyer, and E. Welker. 2001. Bovine pancreatic ribonuclease A: oxidative and conformational folding studies. Methods Enzymol. 341:189-221.
55. Choy, W. Y., Z. Zhou, Y. Bai, and L. E. Kay. 2005. An 15N NMR spin relaxation dispersion study of the folding of a pair of engineered mutants of apocytochrome b562. J. Am. Chem. Soc. 127:5066-5072.
56. Matagne, A., M. Jamin, E. W. Chung, C. V. Robinson, S. E. Radford, and C. M. Dobson. 2000. Thermal unfolding of an intermediate is associated with non-Arrhenius kinetics in the folding of hen lysozyme. J. Mol. Biol. 297:193-210.
57. Oliveberg, M., Y. J. Tan, and A. R. Fersht. 1995. Negative activation enthalpies in the kinetics of protein folding. Proc. Natl. Acad. Sci. USA. 92:8926-8929.
58. Bryngelson, J. D., J. N. Onuchic, N. D. Socci, and P. G. Wolynes. 1995. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins. 21:167-195.
59. Karplus, M., and A. Sali. 1995. Theoretical studies of protein folding and unfolding. Curr. Opin. Struct. Biol. 5:58-73.
60. Font, J., J. Torrent, M. Ribo, D. V. Laurents, C. Balny, M. Vilanova, and R. Lange. 2006. Pressure-jump-induced kinetics reveals a hydration dependent folding/unfolding mechanism of ribonuclease A. Biophys. J. 91:2264-2274.
61. Bray, R. C. 1961. Sudden freezing as a technique for the study of rapid reactions. Biochem. J. 81:189-193.
62. Cherepanov, A. V., and S. De Vries. 2004. Microsecond freezehyperquenching: development of a new ultrafast micro-mixing and sampling technology and application to enzyme catalysis. Biochim. Biophys. Acta. 1656:1-31.