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On the Mechanism of Renaturation of Proteins Containing Disulfide Bonds

  • Hiroshi Taniuchi
  • A. Seetharama Acharya
  • Generoso Andria
  • Diana S. Parker
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 86A)

Abstract

The renaturation of bovine pancreatic ribonuclease A and hen egg white lysozyme from their reduced forms involves two statistical processes, pairing of half-cystine residues by oxidation and rearrangement of disulfide bonds by enzyme or thiol catalyzed sulfhydryl-disulfide interchange. The stability against sulfhydryl-disulfide interchange of the native or nativelike conformation thus attained, which could be a form containing three native disulfide bonds and one open disulfide bond, causes the system to accumulate the renatured enzyme. Thus, the native-like conformation is associated with the lowest free energy only in the late phase of folding.

Keywords

Disulfide Bond Conformational Energy Lower Free Energy Gibbs Standard Free Energy Folding Rate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Anfinsen, C.B. (1955). Studies on the structural basis of ribo-nuclease activity. Biochim. Biophys. Acta, 17, 141–142.PubMedCrossRefGoogle Scholar
  2. Anfinsen, C.B. (1956). The limited digestion of ribonuclease with pepsin. J. Biol. Chem., 221, 405–412.PubMedGoogle Scholar
  3. Anfinsen, C.B. (1967). The formation of the tertiary structure of proteins. Harvey Lectures, 61, 95–116.PubMedGoogle Scholar
  4. Anfinsen, C.B. and Scheraga, H.A. (1975). Experimental and theoretical aspects of protein folding. Advan Prot. Chem., 29, 205–300.CrossRefGoogle Scholar
  5. Andria, G. and Taniuchi, H. (1971). Renaturation of randomly oxidized des-(119-124)-ribonuclease by disulfide interchange in the presence of the fragment, 105-124. Fed Proc, 30, 1288. The full account is in preparation.Google Scholar
  6. Acharya, S.A. and Taniuchi, H. (1976a). A study of renaturation of reduced hen egg white lysozyme: enzymically active intermediates formed during oxidation of the reduced protein. J. Biol. Chem., in press.Google Scholar
  7. Acharya, S.A. and Taniuchi, H. (1976b). The manuscript is in preparation.Google Scholar
  8. Arnone, A., Bier, C.J., Cotton, F.A., Day, V.W., Hazen, E.E., Jr., Richardson, D.C., Richardson, J.S. and, in part, A. Yonath (1971). A high resolution structure of an inhibitor complex of the extracellular nuclease of Staphylococcus aureus. I. Experimental procedures and chain tracing. J. Biol. Chem., 246, 2302–2316.PubMedGoogle Scholar
  9. Blake, C.C.F., Koenig, D.F., Mair, G.A., North, A.C.T., Phillips, D.C. and Sarma, V.R. (1965). Structure of hen egg white lysozyme. A three-dimensional Fourier synthesis at 2 A resolution. Nature, 22, 757–761.CrossRefGoogle Scholar
  10. Bohnert, J.L. and Taniuchi, H. (1972). The examination of the presence of amide groups in glutamic acid and aspartic acid residues of staphylococcal nuclease (Foggi strain). J. Biol. Chem., 247, 4557–4560.PubMedGoogle Scholar
  11. Canfield, R.E. and Liu, A.K. (1965). The disulfide bonds of egg white lysozyme (Muramidase). J. Biol. Chem., 240, 1997–2002.Google Scholar
  12. Cone, J.L., Cusumano, C.L., Taniuchi, H. and Anfinsen, C.B. (1971). Staphylococcal nuclease (Foggi strain). II. The amino acid sequence. J. Biol. Chem., 246, 3103–3110.PubMedGoogle Scholar
  13. Creighton, T.E. (1974). The single-disulfide intermediates in the refolding of reduced pancreatic trypsin inhibitor. J. Mol. Biol. 87., 603–624.PubMedCrossRefGoogle Scholar
  14. Cuatrecasas, P., Fuchs, S., and Anfinsen, C.B. (1967). The binding of nucleotides and calcium to the extracellular nuclease of Staphylococcus aureus: studies by gel filtration. J. Biol. Chem., 242, 3063–3067.PubMedGoogle Scholar
  15. Epstein, C.J., Goldberger, R.F. and Anfinsen, C.B. (1963). Genetic control of tertiary protein structure: studies with model systems. Cold Spring Harbor Symposia on Quant. Biol., 28, 439–449.CrossRefGoogle Scholar
  16. Epstein, H.F., Schechter, A.N., Chen, R.F. and Anfinsen, C.B. (1971). Folding of staphylococcal nuclease: kinetic studies of two processes in acid denaturation. J. Mol. Biol., 60, 499–508.PubMedCrossRefGoogle Scholar
  17. Givol, D., Goldberger, R.F. and Anfinsen, C.B. (1964). Oxidation and disulfide interchange in the reactivation of reduced ribonuclease. J. Biol. Chem., 239, 3114–3116.Google Scholar
  18. Gutte, B., Lin, M.C., Caldi, D.G. and Merrifield, R.B. (1972). Reactivation of des(119-, 120-, or 121-124) ribonuclease A by mixture with synthetic COOH-terminal peptides of varying lengths, J. Biol. Chem., 247, 4763–4767.PubMedGoogle Scholar
  19. Harrington, W.F. and Sela, M. (1959). A comparison of the physical chemical properties of oxidized and reduced alkylated ribonuclease. Biochim. Biophys. Acta, 31, 427–434.PubMedCrossRefGoogle Scholar
  20. Hantgan, R.R., Hammes, G.G. and Scheraga, H.A. (1974). Pathways of folding of reduced bovine pancreatic ribonuclease. Biochemistry, 13, 3421–3431.PubMedCrossRefGoogle Scholar
  21. Habor, E. and Anfinsen, C.B. (1961). Regeneration of enzymic activity by air oxidation of reduced subtilisin-modified ribonuclease. J. Biol. Chem., 236, 422–424.Google Scholar
  22. Hopfield, J.J. (1973). Relation between structure, co-operativity and spectra in a model of hemoglobin action. J. Mol. Biol., 77, 207–222.PubMedCrossRefGoogle Scholar
  23. Karplus, M. and Weaver, D.L. (1976). Protein-folding dynamics. Nature, 260, 404–406.PubMedCrossRefGoogle Scholar
  24. Kartha, G., Bello, J. and Harker, D. (1967). Tertiary structure of ribonuclease. Nature, 213, 862–865.PubMedCrossRefGoogle Scholar
  25. Kato, I. and Anfinsen, C.B. (1969). On the stabilization of ribonuclease S-protein by ribonuclease S-peptide. J. Biol. Chem. 244, 1004–1007.PubMedGoogle Scholar
  26. Koshland, D.E. (1970). The molecular basis for enzyme regulation. “The Enzymes” P.D. Boyer, ed., Academic Press, New York, Vol. 1, pp. 341–396.Google Scholar
  27. Light, A., Taniuchi, H. and Chen, R.F. (1974). A kinetic study of the complementation of fragments of staphylococcal nuclease. J. Biol. Chem., 249, 2285–2293.PubMedGoogle Scholar
  28. Lin, M.C. (1970). The structural roles of amino acid residues near the carboxyl terminus of bovine pancreatic ribonuclease A. J. Biol. Chem., 245, 6726–6731.PubMedGoogle Scholar
  29. Markus, G., Barnard, E.A., Castellani, B.A. and Saunders, D. (1968). Ligand-induced conformational changes in ribonuclease. J. Biol. Chem., 243, 4070–4076.PubMedGoogle Scholar
  30. Ottesen, M. and Stracher, A. (1960). Deuterium exchange of subtilisin-modified ribonuclease and pepsin-inactivated ribonuclease. Compt.-rend. Lab. Carlsberg. Ser. Chim., 31, 457–467.Google Scholar
  31. Parikh, I., Corley, L., and Anfinsen, C.B. (1971). Semisynthetic analogues of an enzymically active complex formed between two overlapping fragments of staphylococcal nuclease. J. Biol. Chem., 246, 7392–7397.PubMedGoogle Scholar
  32. Parker, D.S., Davis, A. and Taniuchi, H. (1975). Determination of the difference in energy between two alternative enzymically active structures formed by two overlapping fragments of staphylococcal nuclease. Fed. Proc. 34, 597.Google Scholar
  33. Phillips, D.C. (1967). The hen egg-white lysozyme molecule. Proc. Nat. Acad. Sci. U.S.A., 57, 484–495.CrossRefGoogle Scholar
  34. Richards, P.M. and Vithayathil, P.J. (1959). The preparation of the subtilisin-modified ribonuclease and the separation of the peptide and protein components. J. Biol. Chem., 234, 1459–1465.PubMedGoogle Scholar
  35. Richards, F.M. and Wyckoff, H.W. (1971). Bovine pancreatic ribonuclease. “The Enzymes”, P.D. Boyer, ed., Academic Press, New York, Vol. 4, pp. 647–806.Google Scholar
  36. Ristow, S.S. and Wetlaufer, D.B. (1973). Evidence for nucleation in the folding of reduced hen egg lysozyme. Biochem. Biophys. Research Commun., 39, 544–550.CrossRefGoogle Scholar
  37. Rose, G.D., Winters, R.H. and Wetlaufer, D.B. (1976) A testable model for protein folding. FEBS Letters, 63, 10–16.PubMedCrossRefGoogle Scholar
  38. Sela, M. and Anfinsen, C.B. (1957). Some spectrophotometric and Polarimetric experiments with ribonuclease. Biochim. Biophys. Acta, 24, 229–235.PubMedCrossRefGoogle Scholar
  39. Tanford, C. (1968). Protein denaturation. Advan. Protein. Chem., 23, 122–282.Google Scholar
  40. Taniuchi, H. and Anfinsen, C.B. (1968). Steps in the formation of active derivatives of staphylococcal nuclease during trypsin digestion. J. Biol. Chem., 243, 4778–4786.PubMedGoogle Scholar
  41. Taniuchi, H. (1970). Formation of randomly paired disulfide bonds in des-(121–124)-ribonuclease after reduction and reoxidation. J. Biol. Chem., 245, 5459–5468.PubMedGoogle Scholar
  42. Taniuchi, H. and Anfinsen, C.B. (1971). Simultaneous formation of two alternative enzymically active structures by complementation of two overlapping fragments of staphylococcal nuclease. J. Biol. Chem., 246, 2291–2301.PubMedGoogle Scholar
  43. Taniuchi, H., Davies, D.R. and Anfinsen, C.B. (1972). A comparison of the X-ray diffraction patterns of crystals of reconstituted Nuclease-T and of native staphylococcal nuclease. J. Biol. Chem., 247, 3362–3364.PubMedGoogle Scholar
  44. Taniuchi, H. and Bohnert, J.L. (1973). Regulation of the complementation of two overlapping fragments of stpahylococcal nuclease. Fed. Proc., 32, 458.Google Scholar
  45. Taniuchi, H. (1973). The dynamic equilibrium of folding and unfolding of Nuclease-T’. J. Biol. Chem., 248, 5164–5174.PubMedGoogle Scholar
  46. Taniuchi, H. and Bohnert, J.L. (1975). The mechanism of stabilization of the structure of Nuclease-T’ by binding of ligands. J. Biol. Chem., 250, 2388–2394.PubMedGoogle Scholar
  47. Taniuchi, H., Parker, D.S. and Bohnert, J.L. (1976). A study of equilibration of the system involving two alternative, enzymically active complementing structures simultaneously formed from two overlapping fragments of staphylococcal nuclease. J. Biol. Chem., in press.Google Scholar
  48. Venetianer, P., and Straub, F.B. (1964). The mechanism of action of the ribonuclease-reactivating enzyme. Biochim. Biophys. Acta, 89, 189–190.PubMedGoogle Scholar
  49. Watson, J.D. (1976). “Molecular Biology of the Gene.” 3rd Edition, W.A. Benjamin, Inc., New York.Google Scholar
  50. Wyckoff, H.W., Hardman, K.D., Allewell, N.M., Inagami, T., Johnson, L.N. and Richards, F.M. (1967). The structure of ribonuclease-S at 3.5 A resolution. J. Biol. Chem., 242, 3984–3988.PubMedGoogle Scholar
  51. Wyman, J., Jr. (1964). Linked functions and reciprocal effects in hemoglobin: a second look. Advan. Prot. Chem., 19, 224–286.Google Scholar

Copyright information

© Plenum Press, New York 1977

Authors and Affiliations

  • Hiroshi Taniuchi
    • 1
  • A. Seetharama Acharya
    • 1
  • Generoso Andria
    • 1
  • Diana S. Parker
    • 1
  1. 1.Laboratory of Chemical BiologyNational Institute of Arthritis, Metabolism, and Digestive Diseases, National Institutes of HealthBethesdaUSA

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