Folding studies on ribonuclease A, a model protein

Folding and Design

Volumn 2, Issue 1, 1997, Pages

  Neira, José Luis ^a   Rico, Manuel ^b  

^a INSTITUTO DE ESTRUCTURA DE LA MATERIA   (Spain)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; PANCREATIC RIBONUCLEASE;

CHEMICAL MODEL; CHEMISTRY; KINETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW;

DISULFIDES; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEASE, PANCREATIC;

EID: 0030631923     PISSN: 13590278     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1359-0278(97)00001-1     Document Type: Review

References (70)

1. Fersht, A.R. (1993). Protein folding and stability: the pathway of folding of barnase. FEBS. Lett. 325, 5-16.
2. Matouschek, A. & Fersht, A.R. (1991). Protein engineering in analysis of protein folding pathways and stability. Methods Enzymol. 202, 81-112.
3. Baldwin, R.L. (1996). On-pathway versus off-pathway folding intermediates. Fold. & Des. 1, R1-R8; 1359-0278-001-R0001.
4. Englander, S.W. & Mayne, L. (1992). Protein folding studied using hydrogen-exchange labelling and two-dimensional NMR. Annu. Rev. Biophys. Biomol. Struct. 21, 243-265.
5. Baldwin, R.L (1993). Pulsed H/D exchange studies of folding intermediates. Curr. Opin. Struct. Biol. 3, 84-91.
6. Serrano, L (1994). Protein engineering and the dissection of protein folding pathways. Curr. Opin. Struct. Biol. 5, 107-111.
7. Fersht, A.R. (1994). Characterizing transition states in protein folding: an essential step in the puzzle. Curr. Opin. Struct. Biol. 5, 79-84.
8. Dobson, CM, Evans, P.A. & Radford, S.E. (1994). Understanding protein folding - the lysozyme story so far. Trends Biol. Sci. 19, 31-37.
9. Anfinsen, C.B. (1973). Principles that govern the folding of protein chain (Nobel Lecture). Science 181, 223-230.
10. Udgaonkar, J.B. & Baldwin, R.L. (1988). NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 335, 694-699.
11. Udgaonkar, J.B. & Baldwin, R.L. (1990). Early folding intermediate of ribonuclease A. Proc. Natl. Acad. Sci. USA 87, 8197-8201.
12. Laity, J.H., Shimotakahara, S. & Scheraga, H.A. (1993). Expression of wild-type and mutant bovine pancreatic ribonuclease A in Escherichia coli. Proc. Natl. Acad. Sci. USA 90, 615-619.
13. Wlodaver, A., Svenson, LA., Sjöin, L & Gilliland, G.L (1988). Structure of phosphate-free ribonuclease A refined at 1.26 A. Biochemistry 27,2705-2717.
14. Santoro, J., et al., & Rico, M. (1993). High-resolution three-dimensional structure of ribonuclease A in solution by nuclear magnetic resonance spectroscopy. J. Mol. Biol. 229, 722-734.
15. Wang, A., Robertson, A.D. & Bolen, D.W. (1995). Effects of naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemistry 34, 15096-15104.
16. Pace, C.N., Laurents, D.V. & Thomson, J.A. (1990). pH dependence of the urea and guanidinium hydro-chloride denaturation of ribonuclease A and ribonuclease T,. Biochemistry 29, 2564-2572.
17. Dyson, HJ. & Wright, P.E. (1993). Peptide conformation and protein folding. Curr. Opin. Struct. Biol. 3, 60-65.
18. Brown, J.E. & Klee, W.A. (1971). Helix-coil transition of the isolated amino terminus of ribonuclease. Biochemistry 10, 470-476.
19. Bierzynski, A., Kim, P.S. & Baldwin, R.L. (1982). A salt bridge stabilises the helix formed by isolated C-peptide of Rnase A. Proc. Natl. Acad. Sci. USA 79, 173-186.
20. 1H-NMR evidence of the folding of isolated ribonuclease S-peptide. FEBS Lett. 162, 314-319.
21. Zimm, B.H. & Bragg, W.K. (1959). Theory of the phase transition between helix and random-coils in polypeptide chains. J. Chem. Phys. 31,526-535.
22. Lifson, S. & Roig, A. (1961). On the theory of helix-coil transition on polypeptides. 7. Chem. Phys. 34, 1963-1974.
23. Sueki, M., Lee, S., Powers, S.P., Denton, J.B., Konishi, Y. & Scheraga, H.A. (1984). Helix-coil stability constants for the naturally occurring amino acids in water. 22. Histidine parameters from random poly(hydroxylbutyl)-glutamine-co-L-histidine Macromolecules 17, 148-155.
24. Kim, P.S. & Baldwin, R.L. (1984). A helix stop signal in the isolated Speptide of ribonuclease A. Nature 307, 329-334.
25. 10+ salt bridge in the folding of isolated ribonuclease A S-peptide. Biochim. Biophys. Res. Commun. 123, 757-763.
26. 10+ side-chain interaction in the C-peptide helix or ribonuclease A. Biophys. Chem. 37, 107-119.
27. 1H NMR data. Biopolymers 25, 1031-1053.
28. n+4 stabilising interaction in peptide a-helices. J. Mot. Struct. 142, 339-342.
29. Shoemaker, K.R., Kim, P.S., Brems, D.N., Marqusee, S., York, E.J., Chaiken, I.M., Stewart, J.M. & Baldwin, R.L (1985). Nature of the charged-group effect on the stability of the C-peptide helix. Proc. Natl. Acad. Sci. USA 82, 2349-2353.
30. Avbelj, F. & Moult, J. (1995). Determination of the conformation of folding initiation sites in proteins by computer simulation. Proteins 23, 129-141.
31. Jiménez, MA, Nieto, J.L., Herranz, J., Rico, M. & Santoro, J. (1987). 'H NMR and CD evidence of the folding of isolated ribonuclease 50-61 fragment. FEBS Lett. 221, 320-324.
32. Jiménez, M.A., Rico, M., Herranz, J., Santoro, J. & Nieto, J.L. (1988). 'H-NMR assignment and folding of the isolated ribonuclease 21-42 fragment. Eur. J. Biochem. 175, 101-109.
33. Matheson, R.R., Jr. & Scheraga, H.A. (1978). A method for predicting nucleation sites for protein folding based on hydrophobic contacts. Macromolecules 11,819-829.
34. Béais, J.M., Haas, E., Krausz, S. & Scheraga, H.A. (1991). Conformational studies of a peptide corresponding to a region of the C-terminus of ribonuclease A: implications on a potential chain-folding initiation site. Biochemistry 30, 7680-7692.
35. Jiménez, M.A., Rico, M., Herranz, J., Santoro, J. & Nieto, J.L. (1990). Solution structure of the isolated ribonuclease C-terminal 112-124 fragment. Biochem. Biophy. Acta 1038, 322-329.
36. Buckler, D.R., Haas, E. & Scheraga, H.A. (1995). Analysis of the structure of ribonuclease A in native and partially denatured states by timeresolved non-radiative dynamic excitation energy transfer between site-specific extrinsic probes. Biochemistry 34, 15965-15978.
37. Altmann, K.H. & Scheraga, H.A. (1990). Local structure in ribonuclease A. Effect of amino acid substitutions on the preferential formation of the native disulfide loop in synthetic peptides corresponding to residues Cys 58-Cys 72 of bovine pancreatic ribonuclease A. J. Am. Chem. Soc. 112, 4926-4931.
38. Talluri, S., Falcomer, C.M. & Scheraga, H.A. (1993). Energetic and structural basis for the preferential formation of the native disulfide loop involving Cys 65-Cys 72 in synthetic peptide fragments derived from the sequence of ribonuclease A. J. Am. Chem. Soc. 115, 3041-3047.
39. Milburn, PJ. & Scheraga. H.A. (1988). Local interactions favor the native 8-residue disulfide loop in the oxidation of a fragment corresponding to the sequence Ser 50-Met 79 derived from bovine pancreatic ribonuclease A. J. Protein. Chem. 7, 377-398.
40. Sosnick, T.R. & Trewhella, J. (1992). Denatured states of ribonuclease A have compact dimensions and residual secondary structure. Biochemistry 31, 8329-8335.
41. Englander, S.W. & Kallenbach, N.R. (1984). Hydrogen exchange and structural dynamics of proteins and nucleic acids. Quart. Rev. Biophys. 16, 521-655.
42. Rothwarf, D.M, Li, Y.J. & Scheraga, H.A. (1995). Regeneration of bovine pancreatic ribonuclease A. Determination of two independent folding pathways. Protein Sci. 4 (suppl 2), 237-245.
43. Anfinsen, C.B. & Harber, E. (1961). Studies of the reduction and reformation of protein disulfide bonds. J. Biol. Chem. 236, 1361-1363.
44. Ruoppolo, M., et al., & Morris, H.R. (1996). Identification of disulfide bonds in the refolding of bovine pancreatic RNase A. Fold. Des. 1, 381-390; 1359-0278-001-00381.
45. Rothwarf, D.M. & Scheraga, H.A. (1993). Regeneration of bovine pancreatic ribonuclease A. I. Steady-state distribution. Biochemistry 32, 2671-2679.
46. Xu, X., Rothwarf, D.M. & Scheraga, H.A. (1996). Nonrandom distribution of the one-disulfide intermediates in the regeneration of ribonuclease A. Biochemistry 35, 6406-6417.
47. Li, Y.J., Rothwarf, D.M. & Scheraga, H.A. (1995). Mechanism of reductive protein unfolding. Nat. Struct. Biol. 2, 489-494.
48. Talluri, S., Rothwarf, D.M. & Scheraga, H.A. (1994). Structural characterization of a three-disulfide intermediate of ribonuclease A involved in both the unfolding and folding pathways. Biochemistry 33, 10437-10449.
49. Roder, H. & Elöve, G. (1994). Early stages of protein folding. In Mechanisms of Protein Folding. (Pain, R.H., ed.), Oxford University Press, London.
50. Schmid, F.X. & Baldwin, R.L. (1979). The rate of inter conversion between the two unfolded forms of ribonuclease A does not depend on GdmCI concentration. J. Mol. Biol. 135, 199-215.
51. Kirn, P.S. & Baldwin, R.L. (1980). Structural intermediates trapped during the folding of ribonuclease A by amide proton exchange. Biochemistry 19, 6124-6129.
52. Udgaonkar, J.B. & Baldwin, R.L. (1995). Nature of the early folding intermediate of ribonuclease A. Biochemistry 34, 4088-4096.
53. Garel, J.R. & Baldwin, R.L. (1973). Both the fast and slow refolding reactions of ribonuclease A yield native enzyme. Proc. Natl. Acad. Sci. USA 70, 3347-3351.
54. Schmid, F.X. & Blaschek, H. (1981). A native-like intermediate on the ribonuclease A folding pathway. 2. Comparison of its properties to native ribonuclease A. Eur. J. Biochem. 114, 111-117.
55. Schmid, F.X. (1989). Kinetics of unfolding and refolding of singledomain proteins. In Protein Folding, pp. 197-242. (Creighton, T.E., ed.), Freeman, New York.
56. Kiefhaber, T. & Baldwin, R.L (1995). Kinetics and hydrogen bond breakage in the process of unfolding of ribonuclease A measured by pulsed hydrogen exchange. Proc. Natl. Acad. Sci. USA 92, 2657-2661.
57. Hvidt, A. & Nielsen, S.O. (1966). Hydrogen-exchange in proteins. Adv. Protein Chem. 21, 287-386.
58. Kiefhaber, T., Labhardt, A.M. & Baldwin, R.L. (1995). Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A. Nature 375, 513-515.
59. Shakhnovich, El. & Finkelstein, A.V. (1989). Theory of cooperative transitions in protein molecules. I. Why denaturation of globular protein is a first-order phase transition. Biopolymers 28, 1667-1680.
60. Brandts, J.F., Halvorson, H.R. & Brennan, M. (1975). Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry 14, 4953-4963.
61. Schultz, DA, Schmid, F.X. & Baldwin, R.L. (1992). C/s proline mutants of ribonuclease A. II. Elimination of the slow-folding by mutation. Protein Sci. 1, 917-924.
62. Houry, W.A., Rothwarf, D.M. & Scheraga, H.A. (1994). A very fast phase in the refolding of disulfide-intact ribonuclease A: implications for the refolding and unfolding pathways. Biochemistry 33, 2516-2530.
63. Houry, W.A. & & Scheraga, H.A. (1996). Nature of the unfolded state of ribonuclease A: effects of cis-trans X-Pro peptide bond isomerization. Biochemistry 35, 11719-11733.
64. Dodge, R.W. & Scheraga, H.A. (1996). Folding and unfolding kinetics of the proline-to-alanine mutants of bovine pancreatic ribonuclease A. Biochemistry 35, 1548-1559.
65. Mayr, L.M., Willbold, D., Rösch, P. & Schmid, F.X. (1994). Generation of a non-prolyl cis peptide bond in ribonuclease T,. J. Mol. Biol. 240, 288-293.
66. Houry, W.A., Rothwarf, D.M. & Scheraga, H.A. (1995). The nature of the initial step in the conformational folding of disulfide-intact ribonuclease. Nat. Struct. Biol. 2, 495-503.
67. Houry, W.A., Rothwarf, D.M. & Scheraga, H.A. (1996). Circular dichroism evidence of the presence of burst-phase intermediates on the conformational folding pathway of ribonuclease A. Biochemistry 35, 10125-10133.
68. Houry, W.A. & Scheraga, H.S. (1996). Structure of the hydrophobically collapsed intermediate on the conformational folding pathway of ribonuclease A probed by hydrogen-deuterium exchange. Biochemistry 35, 11734-11746.
69. Sendak, R.A., Rothwarf, D.M., Wedemeyer, WJ., Houry, W.A. & Scheraga, H.A. (1996). Kinetic and thermodynamic studies of the folding/unfolding of a tryptophan-containing mutant of ribonuclease A. Biochemistry 35,12978-12992.
70. Kraulis, P.J. (1991). Molscript: a program to produce both detailed and schematic plots for protein structures. J. Appl. Crystallogr. 24, 946-950.