Cysteine sulfenic acid as an intermediate in disulfide bond formation and nonenzymatic protein folding

Biochemistry

Volumn 49, Issue 35, 2010, Pages 7748-7755

  Rehder, Douglas S ^a   Borges, Chad R ^a  

^a Arizona State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDS; PROTEIN FOLDING; SOLUTIONS; TRACE ELEMENTS;

AQUEOUS SOLUTIONS; COPPER (II); CYSTEINE RESIDUES; DISULFIDE BOND FORMATION; ENZYME FUNCTIONS; IN-VITRO; NONENZYMATIC PROTEIN; OXIDATIVE REFOLDING; OXIDIZING REAGENTS; PROTEIN MODIFICATIONS; REDOX SIGNALING; SULFENIC ACIDS; TRACE METAL;

MOLECULAR OXYGEN;

CYSTEINE SULFENIC ACID; OXYGEN; SULFENIC ACID DERIVATIVE; TRACE METAL; UNCLASSIFIED DRUG; CYSTEINE; CYSTEINESULFENIC ACID; DISULFIDE; PEPTIDE;

AQUEOUS SOLUTION; ARTICLE; DIMERIZATION; DISULFIDE BOND; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROCESSING; ANALOGS AND DERIVATIVES; CHEMISTRY; MASS SPECTROMETRY; METABOLISM;

CYSTEINE; DIMERIZATION; DISULFIDES; OXIDATIVE STRESS; PEPTIDES; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SULFENIC ACIDS;

EID: 77956140082     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1008694     Document Type: Article

References (48)

1. White, F. H., Jr. and Anfinsen, C. B. (1959) Some relationships of structure to function in ribonuclease Ann. N.Y. Acad. Sci. 81, 515-523
2. Anfinsen, C. B. and Haber, E. (1961) Studies on the reduction and re-formation of protein disulfide bonds J. Biol. Chem. 236, 1361-1363
3. Anfinsen, C. B., Haber, E., Sela, M., and White, F. H., Jr. (1961) The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain Proc. Natl. Acad. Sci. U.S.A. 47, 1309-1314
4. White, F. H., Jr. (1961) Regeneration of native secondary and tertiary structures by air oxidation of reduced ribonuclease J. Biol. Chem. 236, 1353-1360
5. Haber, E. and Anfinsen, C. B. (1962) Side-chain interactions governing the pairing of half-cystine residues in ribonuclease J. Biol. Chem. 237, 1839-1844
6. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains Science 181, 223-230
7. Turell, L., Botti, H., Carballal, S., Ferrer-Sueta, G., Souza, J. M., Duran, R., Freeman, B. A., Radi, R., and Alvarez, B. (2008) Reactivity of sulfenic acid in human serum albumin Biochemistry 47, 358-367
8. Carballal, S., Radi, R., Kirk, M. C., Barnes, S., Freeman, B. A., and Alvarez, B. (2003) Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite Biochemistry 42, 9906-9914
9. Carballal, S., Alvarez, B., Turell, L., Botti, H., Freeman, B. A., and Radi, R. (2007) Sulfenic acid in human serum albumin Amino Acids 32, 543-551
10. Allison, W. S. (1976) Formation and reactions of sulfenic acids in proteins Acc. Chem. Res. 9, 293-299
11. Allison, W. S. and Connors, M. J. (1970) The activation and inactivation of the acyl phosphatase activity of glyceraldehyde-3-phosphate dehydrogenase Arch. Biochem. Biophys. 136, 383-391
12. You, K. S., Benitez, L. V., McConachie, W. A., and Allison, W. S. (1975) The conversion of glyceraldehyde-3-phosphate dehydrogenase to an acylphosphatase by trinitroglycerin and inactivation of this activity by azide and ascorbate Biochim. Biophys. Acta 384, 317-330
13. Lin, W. S., Armstrong, D. A., and Gaucher, G. M. (1975) Formation and repair of papain sulfenic acid Can. J. Biochem. 53, 298-307
14. Claiborne, A., Miller, H., Parsonage, D., and Ross, R. P. (1993) Protein-sulfenic acid stabilization and function in enzyme catalysis and gene regulation FASEB J. 7, 1483-1490
15. Claiborne, A., Yeh, J. I., Mallett, T. C., Luba, J., Crane, E. J., III, Charrier, V., and Parsonage, D. (1999) Protein-sulfenic acids: Diverse roles for an unlikely player in enzyme catalysis and redox regulation Biochemistry 38, 15407-15416
16. Poole, L. B., Karplus, P. A., and Claiborne, A. (2004) Protein sulfenic acids in redox signaling Annu. Rev. Pharmacol. Toxicol. 44, 325-347
17. Reynaert, N. L., van der Vliet, A., Guala, A. S., McGovern, T., Hristova, M., Pantano, C., Heintz, N. H., Heim, J., Ho, Y. S., Matthews, D. E., Wouters, E. F., and Janssen-Heininger, Y. M. (2006) Dynamic redox control of NF-κB through glutaredoxin-regulated S-glutathionylation of inhibitory κB kinase β Proc. Natl. Acad. Sci. U.S.A. 103, 13086-13091
18. Georgiou, G. (2002) How to flip the (redox) switch Cell 111, 607-610
19. Fuangthong, M. and Helmann, J. D. (2002) The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative Proc. Natl. Acad. Sci. U.S.A. 99, 6690-6695
20. Helmann, J. D. (2002) OxyR: A molecular code for redox sensing? Sci. STKE 2002, PE46
21. Poole, L. B. and Nelson, K. J. (2008) Discovering mechanisms of signaling-mediated cysteine oxidation Curr. Opin. Chem. Biol. 12, 18-24
22. Yeh, J. I., Claiborne, A., and Hol, W. G. (1996) Structure of the native cysteine-sulfenic acid redox center of enterococcal NADH peroxidase refined at 2.8 Å resolution Biochemistry 35, 9951-9957
23. Choi, H. J., Kang, S. W., Yang, C. H., Rhee, S. G., and Ryu, S. E. (1998) Crystal structure of a novel human peroxidase enzyme at 2.0 Å resolution Nat. Struct. Biol. 5, 400-406
24. Wood, Z. A., Schroder, E., Robin Harris, J., and Poole, L. B. (2003) Structure, mechanism and regulation of peroxiredoxins Trends Biochem. Sci. 28, 32-40
25. Seth, D. and Rudolph, J. (2006) Redox regulation of MAP kinase phosphatase 3 Biochemistry 45, 8476-8487
26. Becker, K., Savvides, S. N., Keese, M., Schirmer, R. H., and Karplus, P. A. (1998) Enzyme inactivation through sulfhydryl oxidation by physiologic NO-carriers Nat. Struct. Biol. 5, 267-271
27. Toennies, G. (1937) Oxidation of cysteine in non-aqueous media: The "sulfenic acid" as the primary oxidation product J. Biol. Chem. 122, 27-47
28. Claiborne, A., Mallett, T. C., Yeh, J. I., Luba, J., and Parsonage, D. (2001) Structural, redox, and mechanistic parameters for cysteine-sulfenic acid function in catalysis and regulation Adv. Protein Chem. 58, 215-276
29. Poole, L. B. and Ellis, H. R. (2002) Identification of cysteine sulfenic acid in AhpC of alkyl hydroperoxide reductase Methods Enzymol. 348, 122-136
30. Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T. C., Hinks, J. A., Tonks, N. K., and Barford, D. (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate Nature 423, 769-773
31. van Montfort, R. L., Congreve, M., Tisi, D., Carr, R., and Jhoti, H. (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B Nature 423, 773-777
32. Benitez, L. V. and Allison, W. S. (1974) The inactivation of the acyl phosphatase activity catalyzed by the sulfenic acid form of glyceraldehyde 3-phosphate dehydrogenase by dimedone and olefins J. Biol. Chem. 249, 6234-6243
33. Reddie, K. G. and Carroll, K. S. (2008) Expanding the functional diversity of proteins through cysteine oxidation Curr. Opin. Chem. Biol. 12, 746-754
34. Poole, L. B., Klomsiri, C., Knaggs, S. A., Furdui, C. M., Nelson, K. J., Thomas, M. J., Fetrow, J. S., Daniel, L. W., and King, S. B. (2007) Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins Bioconjugate Chem. 18, 2004-2017
35. Poole, L. B., Zeng, B. B., Knaggs, S. A., Yakubu, M., and King, S. B. (2005) Synthesis of chemical probes to map sulfenic acid modifications on proteins Bioconjugate Chem. 16, 1624-1628
36. Takanishi, C. L., Ma, L. H., and Wood, M. J. (2007) A genetically encoded probe for cysteine sulfenic acid protein modification in vivo Biochemistry 46, 14725-14732
37. Charles, R. L., Schroder, E., May, G., Free, P., Gaffney, P. R., Wait, R., Begum, S., Heads, R. J., and Eaton, P. (2007) Protein sulfenation as a redox sensor: Proteomics studies using a novel biotinylated dimedone analogue Mol. Cell. Proteomics 6, 1473-1484
38. Seo, Y. H. and Carroll, K. S. (2009) Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies Proc. Natl. Acad. Sci. U.S.A. 106, 16163-16168
39. Leonard, S. E., Reddie, K. G., and Carroll, K. S. (2009) Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells ACS Chem. Biol. 4, 783-799
40. Conway, M. E., Poole, L. B., and Hutson, S. M. (2004) Roles for cysteine residues in the regulatory CXXC motif of human mitochondrial branched chain aminotransferase enzyme Biochemistry 43, 7356-7364
41. Regazzoni, L., Panusa, A., Yeum, K. J., Carini, M., and Aldini, G. (2009) Hemoglobin glutathionylation can occur through cysteine sulfenic acid intermediate: Electrospray ionization LTQ-Orbitrap hybrid mass spectrometry studies J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 877, 3456-3461
42. Saurin, A. T., Neubert, H., Brennan, J. P., and Eaton, P. (2004) Widespread sulfenic acid formation in tissues in response to hydrogen peroxide Proc. Natl. Acad. Sci. U.S.A. 101, 17982-17987
43. Ramadan, D., Rancy, P. C., Nagarkar, R. P., Schneider, J. P., and Thorpe, C. (2009) Arsenic(III) species inhibit oxidative protein folding in vitro Biochemistry 48, 424-432
44. Carballal, S., Alvarez, B., Turell, L., Botti, H., Freeman, B. A., and Radi, R. (2007) Sulfenic acid in human serum albumin Amino Acids 32, 543-551
45. Johansson, M. and Lundberg, M. (2007) Glutathionylation of β-actin via a cysteinyl sulfenic acid intermediary BMC Biochem. 8, 26
46. Nagy, P., Lemma, K., and Ashby, M. T. (2007) Reactive sulfur species: Kinetics and mechanisms of the reaction of cysteine thiosulfinate ester with cysteine to give cysteine sulfenic acid J. Org. Chem. 72, 8838-8846
47. Creighton, T. E. (1977) Kinetics of refolding of reduced ribonuclease J. Mol. Biol. 113, 329-341
48. Creighton, T. E. (1979) Intermediates in the refolding of reduced ribonuclease A J. Mol. Biol. 129, 411-431