Disulfide bonds in protein folding studies: friends or foes?

• Autorzy: Dadlez M.
• Języki publikacji: EN

Abstrakty

EN

The studies on protein folding pathways utilizing disulfide bonds as reporter groups in several protein model systems arc reviewed. Implications for a general mechanism of protein folding are discussed. An updated folding path­way for bovine pancreatic trypsin inhibitor (BPTI) based on recent data is proposed.

Słowa kluczowe

EN

protein folding; trypsin inhibitor; disulphide bond; bovine pancreas

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 1997
• Tom: 44
• Numer: 3
• Opis fizyczny: p.433-452,fig.

Twórcy

autor

Dadlez M.

• Polish Academy of Sciences, A.Pawinskiego 5A, 02-106 Warsaw, Poland

Bibliografia

• 1. Gicrash, L.M. & King, J. (1990) Deciphering the second half of the genetic code; in Protein Folding. AAAS. Washington.
• 2. Levinthal, C. (1968) Are there pathways for protein folding?«/. Chem. Phys. 65, 44-45.
• 3. Anfinscn, C.B., Haber, E., Sela, M. & White. F.H. (1961) The kinctics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc. Natl. Acad. Sci. U.S.A. 47, 1309-1314.
• 4. Wetzel, R. (1996) For protein misassembly, it is the "r decade. Cell 86, 699-702.
• 5. Baldwin, R.L. (1995) The nature of protein folding pathways: The classical versus the new view. J. Biomol. NMR 5, 103-109.
• 6. Baldwin, R.L. (1996) Why is protein folding so fast? Proc. Natl. Acad. Sci. U.S.A. 93, 2627-2628.
• 7. Weissman, J.S. (1995) All roads lead to Rome? The multiple pathways of protein folding. Chem. Biol. 2, 255-260.
• 8. Mucke, M. & Schmid, X.F. (1994) Intact disul­fide bonds decelerate the folding of ribonu- clease Tl. J. Mol. Biol. 239, 713-725.
• 9. Sosnick, T.R., Mayne, L., Miller, R. & Eng­lander, S.W. (1994) The barriers in protein folding. Nature Struct. Biol. 1, 149-155.
• 10. Creighton, T.E. (1984) Disulfide bond forma­tion in proteins. Methods Enzymol. 107, 305-318.
• 11. Creighton, T.E. (1986) Disulfide bonds as probes of protein folding pathways. Methods Enzymol. 131,83-106.
• 12. Hwang, C., Sinskey, A.J. & Ix)dish. H.F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502.
• 13. Weissman, J.S. & Kim. P.S. (1991) Reexami­nation of the folding of BPTI: Predominance of native intermediates. Science 253, 1386- -1393.
• 14. Marston, F.A.O. (1986) The purification of eukaryotic polypeptides synthesized in Es­cherichia coli. Biochem. J. 240, 1-12.
• 15. Eyles, S.J.. Radford, S.E., Robinson, C.V. & Dobson, C.M. (1994) Kinetic consequences of the removal of a disulfide bridge on the folding of hen lysozyme. Biochemistry 33, 13038- 13048.
• 16. Tang, J.-G. & Tsou, C.-L. (1990) The insulin A and B chains contain structural information for the formation of the native molecule. Bio­chem. J. 268, 423-455.
• 17. Miller, J.A., Owers Narhi, L., Hua, Q.X., Roscnfeld, R., Arakawa, T., Rohde, M., Prestrelski, S., I^auren, S., Stoney, KS., Tsai, L. & Weiss, M.A. (1993) Oxidative refolding of insulin-like growth factor 1 yields two prod­ucts of similar thermodynamic stability: A bifurcating protein-folding pathway. Bio­chemistry 32, 5203-5213.
• 18. Goto, Y. & Hamaguchi, K. (1981) Formation of the intrachain disulfide bond in the con­stant fragment of the immunoglobulin light chain. J. Mol. Biol. 146, 321-340.
• 19. Chatrenet, B. & Chang, J.-Y. (1993) The di­sulfide folding pathway of hirudin elucidated by stop/go folding experiments. J. Biol. Chem. 268,20988 20996.
• 20. Chang, J.-Y., Schindler, P., Ramsaier, U. & Lai, P.-II. (1995) The disulfide folding path­way of human epidermal growth factor. J. Biol. Chem. 270, 9207-9216.
• 21. Chang, J.-Y., Canals, F., Schindler, P., Querol, K. & Aviles, F.X. (1994) The disulfide folding pathway of potato carboxypeptidase inhibitor. J. Biol. Chem. 269, 22087-22094.
• 22. Chang, J.-Y. (1996) The disulfide folding pathway of tick anticoagulant peptide (TAP) a Kunitz-type inhibitor structurally homolo­gous to BPTI. Biochemistry 35, 11702-11709.
• 23. Price-Carter, M., Gray, W.R. & Goldenberg. D.P. (1996) Folding of oconotoxins. 1. Effi­cient disulfide coupled folding of mature se­quences in vitro. Biochemistry 35, 15537- -15546.
• 24. Takahashi, N. & Hiroso, M. (1992) Reversible denaturation of disulfide-reduced ovalbumin and its reoxidation generating the native cys­teine cross-link. J. Biol. Chem. 267, 11565- 11572.
• 25. Cardamone, M., Puri, N.K. & Brandon. M.R. (1995) Comparing the refolding and reoxida­tion of recombinant porcine growth hormone from urea denatured state and from Es­cherichia coli inclusion bodies. Biochemistry 34, 5773-5794.
• 26. Langley, K.E., Berg, T.F., Strickland, T.W., Fenton, D.M., Boone, T.C. & Wypych, J. (1987) Recombinant-DNA-derived bovine growth hormone from Escherichia coli. Eur. J. Biochem. 163,313-321.
• 27. Chau, M.-H. & Nelson, J.W. (1992) Coopera­tive disulfide bond formation in apamin. Bio­chemistry 31, 4445-4450.
• 28. Walker. K.W. & Gilbert, H. (1994) Effect of redox environment on the in vitro and in vivo folding of RTEM1 ^-lactamase and Es­cherichia coli alkaline phosphatase. J. Biol. Chem. 269, 28487-28493.
• 29. Freeh, C., Wunderlich, M., Glockshubcr, R. & Schmid, F.X. (1996) Competition between DsbA-mediated oxidation and conformational folding of RTEM1 (^-lactamase. Biochemistry 35, 11386-11395.
• 30. Clarke. J. & Fersht, A.R. (1993) Engineered disulfide bonds as probes of the folding path­way of barnase: Increasing the stability of proteins against the rate of denaturation. Bio­chemistry 32, 4322-4329.
• 31. Strausberg, S., Alexander, P., Wang, L., Gal­lagher, T., Gilliland, G. & Bryan, P. (1993) An engineered disulfide cross-link accelerates the refolding rate of calcium-free subtilisin by 850-fold. Biochemistry 32, 10371-10377.
• 32. Freedman, R.B. (1995) The formation of pro­tein disulphide bonds. Curr. Opin. Struct. Biol. 5, 85-91.
• 33. Creighton.T.E. & Charles, I.G.( 1987) Biosyn­thesis, processing, and evolution of bovine pancreatic trypsin inhibitor. Cold Spring Harbor Symp. Quant. Biol. LII, 511-519.
• 34. Creighton, T.E., Bagley, C.J., Cooper, L., Darby, N.J., Freedman, R.F., Kemmink, J. & Sheikh, A. (1993) On the biosynthesis of bo­vine pancreatic trypsin inhibitor (BPTI). J. Mol. Biol. 232, 1176-1196.
• 35. Freeh, C. & Schmid, F.X. (1995) DsbA-medi- ated disulfide bond formation and catalyzed prolyl isomerisation in oxidative protein fold­ing. J. Biol. Chem. 270, 5367-5374.
• 36. Bard well, J.C.A. & Beckwith, J. (1993) The bonds that tie: Catalyzed disulfide bond for­mation. Cell 74, 769-771.
• 37. Zapun, A. & Creighton, T.E. (1994) Effects of DsbA on the disulfide folding of BPTI and (X-lactalbumin. Biochemistry 33, 5202- 5211.
• 38. Fritz, II. & Wunderer, G. (1983) Biochemistry and applications of aprotinin, the kallikrein inhibitor from bovine organs. Arzneim. Forsch. /Drug Res. 33, 479-494.
• 39. Bode, W. & Huber, R. (1992) Natural protein proteinase inhibitors and their interaction with proteinases. Eur. J. Biochem. 204, 433- 451.
• 40. Eigenbrot, C., Randal. M. & Kossiakoff, A.A. (1992) Structural effects induced by mu­tagenesis affected by crystal packing factors: The structure of a 30-51 disulfide mutant of basic pancreatic trypsin inhibitor. Proteins Struct. Funct. Genet. 14, 75-87.
• 41. Deisenhofer, J. & Steigemann, W. (1975) Crystallographic refinement of the structure of bovine pancreatic trypsin inhibitor at 1.5 A resolution. Acta Crystallogr. B31, 238-250.
• 42. Wlodawer, A.. Walter, J., Huber, R. & Sjolin, L. (1984) Structure of bovine pancreatic tryp­sin inhibitor. Results of joint neutron and X-ray refinement of crystal form 11. J. Mol. Biol. 180, 301-329.
• 43. Wlodawer, A., Nachman. J., Gilliland. G.L., Gallagher, W. & Woodward, C. (1987) Struc­ture of form 111 crystals of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 198, 469-480.
• 44. Hynes, T.R., Randal, M., Kennedy, L.A., Eigenbrot, C. & Kossiakoff, A.A. (1990) X-ray crystal structure of the inhibitor domain of Alzheimer's amyloid |5-protein precursor. Bio­chemistry 29, 10018-10022.
• 45. Eigenbrot, C., Randal, M. & Kossiakoff, A.A. (1990) Structural effects induced by removal of a disulfide-bridge: The X-ray structure of the C30A/C51A mutant of basic pancreatic trypsin inhibitor at 1.6 A. Protein Eng. 3, 591-598.
• 46. Housset, D., Kim, K.-S., Fuchs, J., Woodward, C. & Wlodawer, A. (1991) Crystal structure of a Y35G mutant of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 220, 757-770.
• 47. Arnoux. B., Merigeau, K., Saluc^jian, P., Nor- ris, F., Norris, K., Bjorn. S., Olsen. O., Pe­tersen, L. & Ducruix, A. (1995) The 1.6 A structure of Kunitz-type domain from the 0(3 chain of human type VI collagen. J. Mol. Biol. 246, 609 -(517.
• 48. Wagner. G. & Wuthrich, K. (1982) Amide proton exchange and surface conformation of the basic pancreatic trypsin inhibitor in solu­tion. J. Mol. Biol. 160, 343-361.
• 49. van Mierlo, C.P.M., Darby, N.J., Neuhaus, D. & Creighton. T.E. (1991) (14-38, 30-51) dou­ble disulphide intermediate in folding of lx>- vine pancreatic trypsin inhibitor: A two di­mensional JH nuclear magnetic resonance study. J. Mol. Biol. 222, 353-371.
• 50. van Mierlo, C.P.M., Darby, N.J., Neuhaus, D. & Creighton, T.E. (1991 ) Two-dimensional 1II NMR study of the (5-55) single disulphide intermediate of bovine pancreatic trypsin in­hibitor. J. Mol. Biol. 222, 373-390.
• 51. van Mierlo, C.P.M., Darby, N.J. & Creighton, T.E. (1992) The partially folded conformation of the Cys30-Cys51 intermediate in the disul­phide folding pathway of bovine pancreatic trypsin inhibitor. Proc. Natl. Acad. Sci. U.S.A. 89, 6775-6779.
• 52. van Mierlo. C.P.M., Darby, N.J., Keeler, J., Neuhaus, D. & Creighton, T.E. (1993) Par­tially folded conformation of the (30-51) inter­mediate in the disulphide folding pathway of bovine pancreatic trypsin inhibitor. and 1SN resonance assignments and determina­tion of backbone dynamics from 15N relaxa­tion measurements. J. Mol. Biol. 229, 1125- -1146.
• 53. van Mierlo, C.P.M., Kemmink, J., Neuhaus, D., Darby, N.J. & Creighton, T.E. (1994) !H NMR analysis of the partly-folded non-native two-disulphide intermediates (30-51. 5-14) and (30-51, 5-38) in the folding pathway of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 235, 1044-1061.
• 54. Berndt, K.D., Guntert, P., Orbons. L P. & Wuthrich, K. (1992) Determination of a high quality nuclear magnetic resonance solution structure of the bovine pancreatic trypsin in­hibitor and comparison with three crystal structures. J. Mol. Biol. 227, 757-775.
• 55. Zweckstetter, M., Czisch, M.. Mayer, U., Chu, M.-L., Zinth, W., Timpl, R. & Holak, T.A. (1995) Structure and multiple conformations of the Kunitz-type domain from human type VI collagen «3(VI) chain in solution. Structure 4, 195-209.
• 56. Moses, E. & Hinz, II.-J. (1983) Basic pancre­atic trypsin inhibitor has unusual thermody­namic stability parameters.«/. Mol. Biol. 170, 765-776.
• 57. Makhatadze. G.I., Kim, K.-S., Woodward, C. & Privalov, P.L. (1993) Thermodynamics of BPTI folding. Protein Sci. 2, 2028-2036.
• 58. Richardson, J.S. ( 1985) Schematic drawings of protein structures. Methods. Enzymol. 115, 359 380.
• 59. Creighton. T.E. & Goldenberg, D.P. (1984) Kinetic role of the meta-stable native like two disulfide species in the folding transition of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 179,497-526.
• 60. Creighton, T.E. (1978) Experimental studies of protein folding and unfolding. Prog. Bio- phys. Mol. Biol. 33, 231-297.
• 61. Creighton, T.E. (1974) Renaturation of the reduced bovine pancreatic trypsin inhibitor. J. Mol. Biol. 87, 563-577.
• 62. Creighton, T.E. (1977) Conformational re­strictions on the pathway of folding and un­folding of BPTI. J. Mol. Biol. 113, 275-293.
• 63. Weissman, J.S. & Kim, P.S. (1992) Kinetic role of nonnative species in the folding of bovine pancreatic trypsin inhibitor. Proc. Natl. Acad. Sci. U.S.A. 89, 9900-9904.
• 64. Weissman, J.S. & Kim, P.S. (1992) The pro region of BPTI facilitates folding. Cell 71, 841-851.
• 65. Weissman, J.S. & Kim, P.S. (1993) Efficient catalysis of disulfide rearrangements by pro­tein disulfide isomerase. Nature 365, 185-188.
• 66. Weissman, J.S. & Kim, P.S. (1995) A kinetic explanation for the rearrangement pathway of BPTI folding. Nature Struct. Biol. 2, 1123-1130.
• 67. Dadlez, M. & Kim, P.S. (1995) A third native one-disulphide intermediate in the folding of bovine pancreatic trypsin inhibitor. Nature Struct. Biol. 2, 674-679.
• 68. Dadlez, M. & Kim, P.S. (1996) Rapid forma­tion of the native 14-38 disulfide bond in the early stages of BPTI folding. Biochem istry 35, 16153-16164.
• 69. Dadlez, M. (1997) Hydrophobic interactions accclcrate early stages of the folding of BPTI. Biochemistry 36, 2788 2797.
• 70. Creighton, T.E. (1992) The disulfide folding pathway of BPTI. Science 256, 111-112.
• 71. Weissman, J.S. & Kim, P.S. (1992) The disul­fide folding pathway of BPTI. Science 256, 112-114.
• 72. Goldenberg, D.P. (1992) Native and non-na­tive intermediates in the BPTI folding path­way. Trends Biochem. Sci. 17, 257 261.
• 73. Hoffman, M. (1991) Straightening out the protein folding puzzle. Science 253, 1357- -1358.
• 74. Crcighton, T.E. ( 1979) Electrophoretic analy­sis of the unfolding of proteins by urea. J. Mol. Biol. 129. 235-264.
• 75. Darby, N.J., Morin. P.E., Talbo, G. & Crei- ghton, T.E. (1995) Refolding of bovine pancre­atic trypsin inhibitor via non-native disul- phide intermediates. J. Mol. Biol. 249, 463—477.
• 76. Darby, N.J. & Creighton, T.E. (1993) Dissect­ing the disulphide-coupled folding pathway of bovine pancreatic trypsin inhibitor. Forming the first disulfide bonds in analogues of the reduced protein. J. Mol. Biol. 232, 873-896.
• 77. Creighton, T.E. (1988) On the relevance of non-random polypeptide conformations for protein folding. Biophys. Chenu 31, 155-162.
• 78. Goldenberg, D.P. & Zhang, J. (1993) Small effects of amino acid replecements on the reduced and unfolded state of pancreatic tryp­sin inhibitor. Proteins: Struct. Fund. Genet. 6, 259-266. (1980) Kosen, P.A., Creighton. T.E. & Blout, E.R. (1980) Ultraviolet difference spectroscopy of intermediates trapped in unfolding and re­folding of bovine pancreatic trypsin inhibitor. Biochemistry 19, 4936-4944. (1981) Kosen, P.A., Creighton, T.E. & Blout, E.R. (1981) Circular dichroism spectroscopy of bo­vine pancreatic trypsin inhibitor and five al­tered conformational states. Relationship of conformation and the refolding pathway of the trypsin inhibitor. Biochemistry 20, 5744-5754.
• 81. Creighton, T.E. (1975) Reactivities of the cys­teine residues of the reduced pancreatic tryp­sin inhibitor. J. Mol. Biol. 96, 777-782.
• 82. Roder, II. (1981 ) Ph.D. Thesis No. 6932, ETH Zurich.
• 83. Kemmink, J. & Creighton, T.E. (1993) Local conformations of peptides representing the entire sequence of bovine pancreatic trypsin inhibitor and their roles in folding. J. Mol. Biol. 234, 861-878.
• 84. Kemmink, J., van Mierlo, C.P.M., Scheek. R.M. & Creighton, T.E. (1993) Local structure due to an aromatic-amide interaction ob­served by ^-nuclear magnetic resonance spectroscopy in peptide related to the N-ter- minus of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 230, 312-322.
• 85. Lumb, K.J. & Kim, P.S. (1994) Formation of a hydrophobic cluster in denatured bovine pancreatic trypsin inhibitor. J. Mol. Biol. 236, 412-420.
• 86. Pan, H., Barbar, E., Barany, G. & Woodward, C. (1995) Extensive non-random structure in reduced and unfolded bovine pancreatic tryp­sin inhibitor. Biochemistry 34, 13974-13981.
• 87. Amir, D. & Haas, E. (1988) Reduced bovine pancreatic trypsin inhibitor has a compact structure. Biochemistry 27, 8889-8893.
• 88. Amir, D., Krausz, S. & Haas. E. (1992) Detec­tion of local structures in reduced unfolded bovine pancreatic trypsin inhibitor. Proteins: Struct. Funet. Genet. 13, 162-173.
• 89. Gottfried. D.S. & Haas, E. (1992) Nonlocal interactions stabilize compact folding inter­mediates in reduced unfolded bovine pancre­atic trypsin inhibitor. Biochemistry 31, 12353-12362.
• 90. Ittah, V. & Haas, E. (1995) Nonlocal interac­tions stabilize long range loops in the initial folding intermediates of reduced bovine pan­creatic trypsin inhibitor. Biochemistry 34, 4493-4506.
• 91. Ferrer, M., Barany, G. & Woodward. C. (1995) Partially folded, molten globule and molten coil states of bovine pancreatic trypsin inhibi­tor. Nature Struct. Biol. 2. 211-217.
• 92. Krokoszynska, I., Dadlez, M. & Otlewski. J. (1997) Early folding intermediates of BPTI folding bind to trypsin. J. Mol. Biol, (in press).
• 93. Barbar, E., Barany, G. & Woodward, C. (1995) Dynamic structure of a highly ordered p-sheet molten globule: Multiple conforma­tions with a stable core. Biochemistry 34, 11423-11434.
• 94.States, D.J., Creighton, T.E., Dobson, C.M. & Karplus, M. (1987) Conformations ofinter- mediates in the folding of the pancreatic trypsin inhibitor. J. Mol. Biol. 195, 731-739.
• 95.Oas, T.G. & Kim, P.S. ( 1988) A peptide model of a protein folding intermediate. Nature 336, 42—48.
• 96.Staley, J.P. & Kim, P.S. (1990) Role of a subdomain in the folding of bovine pancreatic trypsin inhibitor. Nature 344, 685-688.
• 97.Staley, J.P. & Kim, P.S. (1992) Complete folding of bovine pancreatic trypsin inhibitor with only a single disulfide bond. Proc. Natl. Acad. Sci. U.S.A. 89, 1519-1523.
• 98.Staley, J.P. & Kim, P.S. (1994) Formation of a native-like subdomain in a partially-folded intermediate of bovine pancreatic trypsin in­hibitor. Protein Sci. 10, 1822-1832.
• 99.Darby, N.J., van Mierlo, C.P.M., Scott, G.H.E., Neuhaus, D. & Creighton, T.E. (1992) Kinetic roles and conformational properties of the non-native two-disulfide in­termediates in the refolding of BPTI. J. Mol. Biol. 22, 905-911.
• 100. States, D.J., Dobson, C.M., Karplus, M. & Creighton, T.E. (1984) A new two-disulfide intermediate in the refolding of reduced BPTI. J. Mol. Biol. 174, 411-418.
• 101. Schulman, B.A. & Kim, P.S. ( 1994) Hydrogen exchange in BPTI variants that do not share a common disulfide bond. Protein Sci. 3, 2226-2232.
• 102.Stassinopulou, C.I., Wagner, G. & Wuthrich, K. (1984) Two dimensional lH NMR of two chemically modified analogs of the basic pan­creatic trypsin inhibitor. Eur. J. Biochem. 145, 423-430.
• 103. Goldenberg, D.P. (1988) Kinetic analysis of the folding and unfolding of a mutant form of bovine pancreatic trypsin inhibitor lacking the cysteine 14 and cysteine 38 thiols. Bio­chemistry 27, 2481-2489.
• 104. Zhang, J.-X. & Goldenberg, D.P. (1993) Amino acid replacement that eliminates ki­netic traps in the folding pathway of BPTI. Biochemistry 32, 14075-14081.
• 105.Ostermeier, M. & Georgiou, G. (1994) The folding of BPTI in the Escherichia coli peri­plasm. J. Biol. Chem. 269, 21072-221077.
• 106. Heincmann, U. & Sacnger, W. (1982) Spe­cific protein-nucleic acid recognition in ri- bonuclease Tl-2'guanylic acid complex. Na­ture 299, 27-31.
• 107.0obatake, M., Takahashi, S. & Ooi, T. (1979) Conformational stability of ribonuclease Tl. I. Thermal denaturation and effects of salts. J. Biochem. 86, 55-63.
• 108. Kiefhaber, T., Quaas, R., Hahn, U. & Schmid, F.X. (1990) Folding of ribonuclease Tl. 1. Existence of multiple unfolded states created by proline isomerization. Biochemistry 29, 3053-3060.
• 109. Kiefhaber, T., Quaas, R., Hahn, U. & Schmid, F.X. (1990) Folding of ribonuclease Tl. 2. Kinetic models for the folding and unfolding reactions. Biochemistry 29, 3061-3070.
• 110. Kiefhaber, T., Schmid, F.X., Willaert, K., Engelborghs, Y. & Chaffotte, A. (1992) Struc­ture of rapidly formed intermediate in RNase Tl folding. Protein Sci. 1, 1162-1172.
• 111. Mullins, L.S., Pace, C.N. & Rauschel, F.M. (1993) Investigation of ribonuclease Tl fold­ing intermediates by H/D amide exchange — 2D NMR spectroscopy. Biochemistry 32, 6152-6156.
• 112. Fischer, G., Wittman-Liebold, B., Lang, K, Kiefhaber, T. & Schmid, F.X. (1989) Cyclo- philin and peptidyl-prolyl-ci'.s//rarc.s-isom- erase are probably identical proteins. Nature 337, 476-478.
• 113.Schoenbrunner, E.R., Mayer, S., Tropshung, M., Fischer, G., Takahashi, N. & Schmid, F.X. (1991) Catalysis of protein folding by cyclophilins from different species is highly conserved. J. Biol. Chem. 266, 3630-3637.
• 114. Kiefhaber, T., Grunert, H.P., Hahn, U. & Schmid, F.X. (1992) Folding of RNase Tl is decelerated by a specific tertiary contact in a folding intermediate. Proteins: Struct. Funct. Genet. 12, 171-179.
• 115. Kiefhaber, T., Grunert, H.-P., Hahn, U. & Schmid, F.X. (1990) Replacement of a cis proline simplifies the mechanism of ribonu­clease Tl folding. Biochemistry 29, 6475- -6480.
• 116. Mayr, L. & Schmid, F.X. (1993) Kinetic models for unfolding and refolding of ribonu- clease T1 with substitution of cis-proline 39 with alanine. J. Mol. Biol. 231, 913-926.
• 117. Mayr, L., Willibold, D., Roesch, P. & Schmid, F.X. (1995) Generation of a non-prolyl cis peptide bond in ribonuclease Tl. J. Mol. Biol. 240, 288-293.
• 118. Pace, N. & Creighton, T.E. (1986) The disul- phide folding pathway of ribonuclease Tl. J. Mol. Biol. 188, 477—486.
• 119. Mayr, L. & Schmid, F.X. (1994) Role of the Cys2-Cysl() disulfide bond for the structure, stability, and folding kinetics of ribonuclease Tl. Protein Sci. 3, 227-239.
• 120. Pace, N., Grimsley, G.R., Thomson, J. A & Barnett, B.J. (1988) Conformational stability and activity of RNase Tl with zero, one and two intact disulfide bonds. J. Biol. Chem. 263, 11820-11825.
• 121. Mucke, M. & Schmid. F.X. (1992) Enzymatic catalysis of prolyl isomerization in an unfold­ing protein. Biochemistry 31, 7848-7854.
• 122. Mucke, M. & Schmid, F.X. (1994) Folding of ribonuclease Tl in the absence of the disul­fide bonds. Biochemistry 33, 14608-14619.
• 123. Ruoppolo, M. & Freedman, R.B. (1995) Re­folding by disulfide isomerization: the mixed disulfide between ribonuclease Tl and glu­tathione as a model refolding substrate. Bio­chemistry 34, 9380-9388.
• 124. Freeh, C. & Schmid, F.X. (1995) Influence of protein conformation on disulfide bond for­mation in the oxidative folding of ribonu­clease Tl. J. Mol. Biol. 251, 135—149.
• 125. Wlodawer, A., Svensson, L.A., Sjolin, L. & Gilliland. G.L. (1988) Structure of phos­phate-free ribonuclease A refined at 1.26 A. Biochemistry 27, 2705-2713.
• 126. Anfinsen, C.B. (1973) Principles that govern the folding of protein chains. Science 181, 223-230.
• 127. Cook, K.H., Schmid, F.X. & Baldwin, R.L. (1979) Role of proline isomerization in fold­ing of ribonuclease A Proc. Natl. Acad. Sci. U.S.A. 76, 6157-6161.
• 128.Schultz, D.A., Schmid, F.X. & Baldwin, R.L. (1982) Cis proline mutants of ribonuclease A.1I. Elimination of the slow folding forms by mutation. Protein Sci. I, 917-924.
• 129. 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.
• 130. Hantgan, R.R., Hammes, G.G. & Scheraga, H.A. (1974) Pathways of folding of reduced bovine pancreatic ribonuclease. Biochemis­try 13, 3421-3431.
• 131. Rothwarf, D.M. & Scheraga, H.A. (1993) Re­generation of bovine pancreatic ribonu­clease. Biochemistry 32, 2671-2703.
• 132. Creighton, T.E. (1979) Intermediates in the refolding of reduced ribonuclease A. J. Mol. Biol. 129,411-431.
• 133. Wearne, S.J. & Creighton, T.E. (1988) Fur­ther experimental studies of the disulfide folding transition of ribonuclease A. Proteins: Struct. Fund. Genet. 4, 251-261.
• 134. Konishi, Y., Ooi, T. & Scheraga, H.A. (1982) Regeneration of ribonuclease A from reduced protein. Rate-limiting steps. Bu>chemistry 21, 4734-4740.
• 135. Konishi, Y., Ooi, T. & Scheraga, H.A. (1982) Regeneration of ribonuclease A from reduced protein. Energetic analysis. Biochemistry 21, 4741-4748.
• 136. Konishi, Y., Ooi, T. & Scheraga, H.A. (1982) Regeneration of RNase A from the reduced protein: Models of regeneration pathways. Proc. Natl. Acad. Sci. U.S.A. 79, 5734-5738.
• 137. Konishi, Y., Ooi, T. & Scheraga, H.A. (1981) Regeneration of ribonuclease A from reduced protein. Isolation and identification of inter­mediates and equilibrium treatment. Bio­chemistry 20, 3945-3955.
• 138. Konishi, Y. & Scheraga, H.A. (1980) Regen­eration of ribonuclease A from reduced pro­tein. Conformational analysis of the inter­mediates by NMR spectroscopy. Biochemis­try 19, 1316-1322.
• 139. Creighton, T.E. (1988) Toward a better un­derstanding of protein folding pathways. Proc. Natl. Acad. Sci. U.S.A. 85, 5082-5086.
• 140.Scheraga, H.A., Konishi, Y., Rothwarf, D.M. & Hui, P.W. (1987) Toward a better under­standing of the folding of ribonuclease A. Proc. Natl. Acad. Sci. U.S.A 84, 5740-5744.
• 141. Rothwarf, D.M. & Scheraga, H.A. (1991) Re­generation and reduction of native bovine pancreatic ribonuclease A with oxidized and reduced DTT. J. Am. Chem. Soc. 113, 6293- -6295.
• 142. Telluri, S., Rothwarf, D.M. & Scheraga, H.A. (1994) Structural characterization of a three disulfide intermediate of ribonuclease A in­volved both in the folding and unfolding pathway. Biochemistry 33, 10437-10449.
• 143.Buckler, D.R., Haas, E. & Scheraga, H.A. (1995) 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 34,15965-15978.
• 144. Beals, J.M., Haas, E., Krausz, S. & Scheraga, H.A. (1991) Conformational studies of a pep­tide corresponding to a region of the C-termi- nus of ribonuclease A. Biochemistry 30, 7680-7692.
• 145.Sosnick, T.R. & Trewhclla, J. (1992) Dena­tured states of ribonuclease A have compact dimensions and residual secondary struc­ture. Biochemistry 31, 8329-8335.
• 146. Wright, P.E., Dyson, H.J. & Lerner, A.R. (1988) Conformation of peptide fragments of proteins in aqueous solution: Implications for initiation of protein folding. Biochemistry 27, 7167-7175.
• 147. Acharya, K.R., Stuart. D.I., Walker, N.P.C., Lewis, M. & Philips, DC. (1989) Refined structure of baboon a-lactalbumin at 1.7 A resolution. J. Mol. Biol. 208, 99-127.
• 148. Acharya, K.R., Ren, J., Stuart, D.I., Philips, D.C. & Fcnna, R E. (1991) Crystal structure of human a-lactalbumin at 1.7 A resolution. J. Mol. Biol. 221, 571-581.
• 149. Vanaman, T.C., Brew, K. & Hill, R.L. (1970) The disulfide bonds of bovine a-lactalbumin. J. Biol. Chem. 245, 4583-4590.
• 150. Kuwajima, K., Nitta, K., Yoneyama, M. & Sugai, S. (1976) Three-state denaturation of a-lactalbumin by guanidine hydrochloride. J. Mol. Biol. 106, 359-373.
• 151. Dolgikh, D.A., Gilmanshin, R.I., Brazhnikov, E. V., Bychkova, V.E., Semisotnov, G.V., Ven- yaminov, S.Y. & Ptitsyn, O.B. (1981) a-Lac- toglobulin: compact state with fluctuating tertiary structure? FEBS Lett. 136,311-315.
• 152. Xie, D., Bhakuni, V. & Freire, E. (1991) Calorimetric determination of the energetics of the molten globule intermediate in protein folding: apo a-lactoglobulin. Biochemistry 30, 10673-10678.
• 153. Ewbank, J.J. & Creighton, T.E. (1993) Path­way of disulphide-coupled unfolding and re­folding of bovine a-lactalbumin. Biochemis­try 32, 3677-3693.
• 154. Ewbank, J.J. & Creighton, T.E. (1993) Struc­tural characterization of the disulfide folding intermediate of bovine a-lactalbumin. Bio­chemistry 32, 3694-3707.
• 155. Ewbank, J.J. & Creighton, T.E. (1991) The molten globule protein conformation probed by disulphide bonds. Nature 350, 518-520.
• 156. Peng, Z.Y. & Kim, P.S. (1994) A protein dissection study of a molten globule. Bio­chemistry 33, 2136-2141.
• 157. Wu, C.L., Peng, Z.Y. & Kim, P.S. (1995) Bipartite structure of the a-lactalbumin mol­ten globule. Nature Struct. Biol. 2, 281-286.
• 158. Peng, Z.Y., Wu, C.L. & Kim, P.S. (1995) Local structural preferences in the a-lactalbumin molten globule. Biochemistry 34,3248-3252.
• 159. Kuwajima, K. (1989) The molten globule as a clue for understanding the folding and cooperativity of globular protein structure. Proteins: Struct. Fund. Genet. 6, 87-103.
• 160. Ptitsyn, O.B. (1992) in Protein Folding (Creighton, T.E., ed.) pp. 243-300, W.H. Freeman & Co., New York.
• 161. de Young, L.R., Burton, L.E., Liu, J., Powell, M.F., Schmelzer, C.H. & Skelton, N.J. (1996) RhNGF slow unfolding is not due to proline isomerization: Possibility of a cysteine knot loop-threading mechanism. Protein Sci. 5, 1554-1566.
• 162. Owers Narhi, L., Hua, Q.-X., Arakawa, T., Fox, G.M., Tsai, L., Rosenfeld, R., Hoist, P., Miller, J.A. & Weiss. M.A. (1993) Role of native disulfide bonds in the structure and activity of insulin-like growth factor 1: Ge­netic models of protein folding intermedi­ates. Biochemistry 32, 5214-5221.
• 163. Price-Carter, M., Gray, W.R. & Goldenberg, D.P. (1996) Folding of a>-conotoxins. 2. Influ­ence of precursor sequences and protein di­sulfide isomerase. Biochemistry 35, 15547- -15557.
• 164.Kim, J.S. & Raines, R.T. (1994) A misfolded but active dimer of bovine seminal ribonu- clease. Eur. J. Biochem. 224, 109-114.
• 165.O'Shea, E.K., Rutkowski, R., Stafford, W.F. & Kim, P.S. (1989) Preferential heterodimer formation by isolated leucine zippers from fos and jun. Science 245, 646-648.