Protein sulfenic acids in redox signaling

Annual Review of Pharmacology and Toxicology

Volumn 44, Issue , 2004, Pages 325-347

  Poole, Leslie B ^a   Karplus, P Andrew ^b   Claiborne, Al ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Cell signaling; Cysteine; Oxidation; Redox center; Sulfinic acid

Indexed keywords

CYSTEINE; DISULFIDE; ENZYME; PROTEIN DERIVATIVE; PROTEIN SULFENIC ACID DERIVATIVE; SULFENAMIDE DERIVATIVE; SULFENIC ACID DERIVATIVE; SULFINIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

HUMAN; NITROSATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

GLUTATHIONE REDUCTASE; HUMANS; METHIONINE; OXIDATION-REDUCTION; PEROXIDASES; PEROXIDES; PROTEIN CONFORMATION; PROTEINS; SIGNAL TRANSDUCTION; SULFENIC ACIDS; TRANSCRIPTION, GENETIC;

EID: 1342281240     PISSN: 03621642     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.pharmtox.44.101802.121735     Document Type: Review

References (106)

1. Christman MF, Morgan RW, Jacobson FS, Ames BN. 1985. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41:753-62
2. Paget MSB, Buttner MJ. 2003. Thiol-based regulatory switches. Annu. Rev. Genet. 37:91-121
3. 2 stimulon in Saccharomyces cerevisiae. J. Biol. Chem. 273:22480-89
4. Rhee SG, Bae YS, Lee S-R, Kwon J. 2000. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Science's STKE. www.stke.org/cgi/contentfull/OC_sigtrans;2000/53/pel
5. Finkel T. 2000. Redox-dependent signal transduction. FEBS Lett. 476:52-54
6. Stamler JS, Hausladen A. 1998. Oxidative modifications in nitrosative stress. Nat. Struct. Biol. 5:247-49
7. Wood ZA, Schröder E, Harris JR, Poole LB. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28:32-40
8. Wood ZA, Poole LB, Karplus PA. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650-53
9. 2 receptor and redox-transducer in gene activation. Cell 111: 471-81
10. Kice JL. 1980. Mechanisms and reactivity in reactions of organic oxyacids of sulfur and their anhydrides. Adv. Phys. Org. Chem. 17:65-181
11. Hogg DR. 1990. Chemistry of sulphenic acids and esters. In The Chemistry of Sulphenic Acids and Their Derivatives, ed. S Patai, pp. 361-402. New York: Wiley
12. Claiborne A, Mallett TC, Yeh JI, Luba J, Parsonage D. 2001. Structural, redox, and mechanistic parameters for cysteine-sulfenic acid function in catalysis and regulation. Adv. Protein Chem. 58:215-76
13. Allison WS. 1976. Formation and reactions of sulfenic acids in proteins. Acc. Chem. Res. 9:293-99
14. Claiborne A, Yeh JI, Mallett TC, Luba J, Crane EJ III, et al. 1999. Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry 38:15407-16
15. Ellis HR, Poole LB. 1997. Novel application of 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole to identify cysteine sulfenic acid in the AhpC component of alkyl hydroperoxide reductase. Biochemistry 36:15013-18
16. Bryk R, Griffin P, Nathan C. 2000. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211-15
17. Raftery MJ, Yang Z, Valenzuela SM, Geczy CL. 2001. Novel intra- and inter-molecular sulfinamide bonds in S100A8 produced by hypochlorite oxidation. J. Biol. Chem. 276:33393-401
18. Winterbourn CC, Metodiewa D. 1999. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic. Biol. Med. 27:322-28
19. Denu JM, Tanner KG. 1998. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37:5633-42
20. Baker LMS, Poole LB. 2003. Catalytic mechanism of thiol peroxidase from Escherichia coli: sulfenic acid formation and overoxidation of essential Cys61. J. Biol. Chem. 278:9203-11
21. Hofmann B, Hecht H-J, Flohé L. 2002. Peroxiredoxins. Biol. Chem. 383:347-64
22. Crane EJ III, Parsonage D, Poole LB, Claiborne A. 1995. Analysis of the kinetic mechanism of enterococcal NADH peroxidase reveals catalytic roles for NADH complexes with both oxidized and two-electron-reduced enzyme forms. Biochemistry 34:14114-24
23. Åslund F, Zheng M, Beckwith J, Storz G. 1999. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. USA 96:6161-65
24. Gu ZZ, Kaul M, Yan BX, Kridel SJ, Cui JK, et al. 2002. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297:1186-90
25. Ishii T, Sunami O, Nakajima H, Nishio H, Takeuchi T, Hata F. 1999. Critical role of sulfenic acid formation of thiols in the inactivation of glyceraldehyde-3-phosphate dehydrogenase by nitric oxide. Biochem. Pharmacol. 58:133-43
26. Percival MD, Ouellet M, Campagnolo C, Claveau D, Li C. 1999. Inhibition of cathepsin K by nitric oxide donors: evidence for the formation of mixed disulfides and a sulfenic acid. Biochemistry 38:13574-83
27. Hogg PJ. 2003. Disulfide bonds as switches for protein function. Trends Biochem. Sci. 28:210-14
28. Giles GI, Tasker KM, Jacob C. 2001. Hypothesis: the role of reactive sulfur species in oxidative stress. Free Radic. Biol. Med. 31:1279-83
29. Dickinson DA, Forman HJ. 2002. Glutathione in defense and signaling: lessons from a small thiol. Ann. NY Acad. Sci. 973:488-504
30. Klatt P, Lamas S. 2000. Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem. 267:4928-44
31. Thomas JA, Poland B, Honzatko R. 1995. Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch. Biochem. Biophys. 319:1-9
32. Finlayson AJ, MacKenzie SL, Finley FW. 1979. Reaction of alanine-3-sulfinic acid with 2-mercaptoethanol. Can. J. Chem. 57:2073-77
33. Woo HA, Chae HZ, Hwang SC, Yang K-S, Kang SW, et al. 2003. Reversible oxidation of the catalytic site cysteine of peroxiredoxins to cysteine sulfinic acid in mammalian cells. Science 300:653-56
34. Chevallet M, Wagner E, Luche S, Van Dorsselaer A, Leize-Wagner E, Rabilloud T. 2003. Regeneration of peroxiredoxins during recovery after oxidative stress: only some overoxidized peroxiredoxins can be reduced during recovery after oxidative stress. J. Biol. Chem. In press
35. Biteau B, Labarre J, Toledano M. 2003. ATP-dependent reduction of cysteine sulfinic acid by S. cerevisae sulfiredoxin. Nature 425:980-84
36. Denu J, Tanner KG. 2002. Redox regulation of protein tyrosin phosphatases by hydrogen peroxide: detecting sulfenic acid intermediates and examining reversible inactivation. Methods Enzymol. 348:297-305
37. 2. J. Biol. Chem. 273: 32554-60
38. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, et al. 2003. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423:769-73
39. Van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H. 2003. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:773-7
40. Williams CH Jr. 1992. Lipoamide dehydrogenase, glutathione reductase, thioredoxin reductase, and mercuric ion reductase - a family of flavoenzyme transhydrogenases. In Chemistry and Biochemistry of Flavoenzymes, ed. F Müller, 3:121-211. Boca Raton, FL: CRC Press
41. Crane EJ III, Ward DE, van der Oost J, She Q, Garrett R. 1999. Sequence analysis and overexpression of putative NADH oxidases from the hyperthermophilic arecheaons Sulfolobus solfataricus and Pyrococcus horikoshii. In Flavins and Flavoproteins 1999, ed. S Ghisla, P Kroneck, P Macheroux, H Sund, pp. 281-84. Berlin: Agency Sci. Publ.
42. Ward DE, Donnelly CJ, Mullendore ME, van der Oost J, de Vos WM, Crane EJ III. 2001. The NADH oxidase from Pyrococcus furiosus. Implications for the protection of anaerobic hyperthermophiles against oxidative stress. Eur. J. Biochem. 268:5816-23
43. 2-forming NADH oxidase with diaphorase (cytochrome) activity from Archaeoglobus fulgidus. J. Bacteriol. 183:7007-16
44. Karplus PA, Schulz GE. 1989. Substrate binding and catalysis by glutathione reductase as derived from refined enzyme: substrate crystal structures at 2 Å resolution. J. Mol. Biol. 210:163-80
45. Stehle T, Ahmed SA, Claiborne A, Schulz GE. 1991. Structure of NADH peroxidase from Streptococcus faecalis 10C1. J. Mol. Biol. 221:1325-55
46. Crane EJ III, Parsonage D, Claiborne A. 1996. The active-site histidine-10 of enterococcal NADH peroxidase is not essential for catalytic activity. Biochemistry 35:2380-87
47. Miller H, Claiborne A. 1991. Peroxide modification of monoalkylated glutathione reductase. Stabilization of an active-site cysteine-sulfenic acid. J. Biol. Chem. 266:19342-50
48. Becker K, Gui M, Schirmer RH. 1995. Inhibition of human glutathione reductase by S-nitrosoglutathione. Eur. J. Biochem. 234:472-78
49. Keese MA, Bose M, Mulsch A, Schirmer RH, Becker K. 1997. Dinitrosyl-dithiol-iron complexes, nitric oxide (NO) carriers in vivo, as potent inhibitors of human glutathione reductase and glutathione-S-transferase. Biochem. Pharmacol. 54:1307-13
50. Becker K, Savvides SN, Keese M, Schirmer RH, Karplus PA. 1998. Enzyme inactivation through sulfhydryl oxidation by physiologic NO-carriers. Nat. Struct. Biol. 5:267-71
51. Hogg N. 2002. The biochemistry and physiology of S-nitrosothiols. Annu. Rev. Pharmacol. Toxicol. 42:585-600
52. Miller H, Mande SS, Parsonage D, Sarfaty SH, Hol WG, Claiborne A. 1995. An L40C mutation converts the cysteine-sulfenic acid redox center in enterococcal NADH peroxidase to a disulfide. Biochemistry 34:5180-90
53. Link AJ, Robison K, Church GM. 1997. Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18:1259-313
54. Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG. 1994. Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc. Natl. Acad. Sci. USA 91:7017-21
55. Seaver LC, Imlay JA. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183:7173-81
56. Poole LB, Reynolds CM, Wood ZA, Karplus PA, Ellis HR, Calzi ML. 2000. AhpF and other NADH:peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. Eur. J. Biochem. 267:6126-33
57. Ellis HR, Poole LB. 1997. Roles for the two cysteine residues of AhpC in catalysis of peroxide reduction by alkyl hydroperoxide reductase from Salmonella typhimurium. Biochemistry 36:13349-56
58. Fuangthong M, Helmann JD. 2002. The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc. Natl. Acad. Sci. USA 99:6690-95
59. Kim SO, Merchant K, Nudelman R, Beyer WF, Keng T, et al. 2002. OxyR: a molecular code for redox-related signaling. Cell 109:383-96
60. Poole LB. 2003. Bacterial peroxiredoxins. In Signal Transduction by Reactive Oxygen and Nitrogen Species: Pathways and Chemical Principles, ed. M Torres, JM Fukuto, HJ Forman, pp. 80-101. Dordrecht, The Netherlands: Kluwer Acad.
61. Cha MK, Kim HK, Kim IH. 1995. Thioredoxin-linked 'thiol peroxidase' from periplasmic space of Escherichia coli. J. Biol. Chem. 270:28635-41
62. Jeong W, Cha MK, Kim IH. 2000. Thioredoxin-dependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)/alkyl hydroperoxide peroxidase C (AhpC) family. J. Biol. Chem. 275:2924-30
63. Moore TDE, Sparling PF. 1996. Interruption of the gpxA gene increases the sensitivity of Neisseria meningitidis to paraquat. J. Bacteriol. 178:4301-5
64. King KY, Horenstein JA, Caparon MG. 2000. Aerotolerance and peroxide resistance in peroxidase and PerR mutants of Streptococcus pyogenes. J. Bacteriol. 182:5290-99
65. Mongkolsuk S, Praituan W, Loprasert S, Fuangthong M, Chamnongpol S. 1998. Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J. Bacteriol. 180:2636-43
66. Atichartpongkul S, Loprasert S, Vattanaviboon P, Whangsuk W, Helmann JD, Mongkolsuk S. 2001. Bacterial Ohr and OsmC paralogues define two protein families with distinct functions and patterns of expression. Microbiology 147:1775-82
67. Lesniak J, Barton WA, Nikolov DB. 2002. Structural and functional characterization of Ohr, an organic hydroperoxide resistance protein from Pseudomonas aeruginosa. EMBO J. 21:6649-59
68. Renato J, Cussiol JR, Alves SV, Oliveira MA, Netto LES. 2003. Organic hydroperoxide resistance gene encodes a thiol-dependent peroxidase. J. Biol. Chem. 278:11570-78
69. Jin D-Y, Jeang K-T. 2000. Peroxiredoxins in cell signaling and HIV infection. In Antioxidant and Redox Regulation of Genes, ed. CK Sen, H Sies, PA Baeuerle, pp. 381-407. San Diego: Academic
70. Wen ST, Van Etten RA. 1997. The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev. 11:2456-67
71. Georgiou G, Masip L. 2003. An overoxidation journey with a return ticket. Science 300:592-94
72. Wood ZA, Poole LB, Hantgan RR, Karplus PA. 2002. Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 41:5493-504
73. Kitano K, Niimura Y, Nishiyama Y, Miki K. 1999. Stimulation of peroxidase activity by decamerization related to ionic strength: AhpC protein from Amphibacillus xylanus. J. Biochem 126:313-19
74. Chauhan R, Mande SC. 2001. Characterization of the Mycobacterium tuberculosis H37Rv alkyl hydroperoxidase AhpC points to the importance of ionic interactions in oligomerization and activity. Biochem. J. 354:209-15
75. König J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz KJ. 2003. Reaction mechanism of plant 2-Cys peroxiredoxin: role of the C-terminus and the quarternary structure. J. Biol. Chem. 278:24409-20
76. Chang TS, Jeong W, Choi SY, Yu S, Kang SW, Rhee SG. 2002. Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J. Biol. Chem. 277:25370-76
77. Schröder E, Willis AC, Ponting CP. 1998. Porcine natural-killer-enhancing factor-B: oligomerisation and identification as a calpain substrate in vitro. Biochim. Biophys. Acta 1383:279-91
78. Cha M-K, Yun C-H, Kim IH. 2000. Interaction of human thiol-specific antioxidant protein 1 with erythrocyte plasma membrane. Biochemistry 39:6944-50
79. Koo KH, Lee S, Jeong SY, Kim ET, Kim HJ, et al. 2002. Regulation of thioredoxin peroxidase activity by C-terminal truncation. Arch. Biochem. Biophys. 397:312-18
80. Mitsumoto A, Takanezawa Y, Okawa K, Iwamatsu A, Nakagawa Y. 2001. Variants of peroxiredoxins expression in response to hydroperoxide stress. Free Radic. Biol. Med. 30:625-35
81. Rabilloud T, Heller M, Gasnier F, Luche S, Rey C, et al. 2002. Proteomics analysis of cellular response to oxidative stress: evidence for in vivo over-oxidation of peroxiredoxins at their active site. J. Biol. Chem. 277:19396-401
82. Yang KS, Kang SW, Woo HA, Hwang SC, Chae HZ, et al. 2002. Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277:38029-36
83. Schröder E, Littlechild JA, Lebedev AA, Errington N, Vagin AA, Isupov MN. 2000. Crystal structure of decameric 2-Cys peroxiredoxin from human erythrocytes at 1.7 Å resolution. Structure 8:605-15
84. Alphey MS, Bond CS, Tetaud E, Fairlamb AH, Hunter WN. 2000. The structure of reduced tryparedoxin peroxidase reveals a decamer and insight into reactivity of 2Cys-peroxiredoxins. J. Mol. Biol. 300:903-16
85. Kang SW, Chae HZ, Seo MS, Kim K, Baines IC, Rhee SG. 1998. Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha. J. Biol. Chem. 273:6297-302
86. Moskovitz J, Rahman MA, Strassman J, Yancey SO, Kushner SR, et al. 1995. Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J. Bacteriol. 177:502-7
87. Boschi-Muller S, Azza S, Sanglier-Cianferani S, Talfournier F, Van Dorsselear A, Branlant G. 2000. A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J. Biol. Chem. 275:35908-13
88. Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW. 2002. The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat. Struct. Biol. 9:348-52
89. Weissbach H, Etienne F, Hoshi T, Heinemann SH, Lowther WT, et al. 2002. Peptide methionine sulfoxide reductase: structure, mechanism of action, and biological function. Arch. Biochem. Biophys. 397:172-78
90. Davis DA, Newcomb FM, Moskovitz J, Fales HM, Levine RL, Yarchoan R. 2002. Reversible oxidaiton of HIV-2 protease. Methods Enzymol. 348:249-59
91. Olry A, Boschi-Muller S, Marraud M, Sanglier-Cianferani S, Van Dorsselear A, Branlant G. 2002. Characterization of the methionine sulfoxide reductase activities of PILB, probably a virulence factor from Neisseria meningitidis. J. Biol. Chem. 277:12016-22
92. Vougier S, Mary J, Friguet B. 2003. Subcellular localisation of methionine sulphoxide reductase (MsrA): evidence for mitochondrial and cytosolic isoforms in rat liver cells. Biochem. J. 373:531-37
93. Pineda-Molina E, Klatt P, Vázquez J, Marina A, Garcia de Lacoba M, et al. 2001. Glutathionylation of the p50 subunit of NF-kappaB: a mechanism for redox-induced inhibition of DNA binding. Biochemistry 40:14134-42
94. Pineda-Molina E, Lamas S. 2002. S-glutathionylation of NF-kappaB subunit p50. Methods Enzymol. 359:268-79
95. Storz G, Tartaglia LA, Ames BN. 1990. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248:189-94
96. Kullik I, Toledano MB, Tartaglia LA, Storz G. 1995. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J. Bacteriol. 177:1275-84
97. Zheng M, Åslund F, Storz G. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718-21
98. Choi H, Kim S, Mukhopadhyay P, Cho S, Woo J, et al. 2001. Structural basis of the redox switch in the OxyR transcription factor. Cell 105:103-13
99. Helmann JD. 2002. OxyR: a molecular code for redox sensing? Science's STKE. www.stke.org/cgi/content/full/sigtra ns;2002/157/pe46
100. Georgiou G. 2002. How to flip the (redox) switch. Cell 111:607-10
101. Cooper CE, Patel RP, Brookes PS, Darley-Usmar VM. 2002. Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends Biochem. Sci. 27:489-92
102. Dickens C. 1859. A Tale of Two Cities. London: Chapman Hall
103. Mongkolsuk S, Helmann JD. 2002. Regulation of inducible peroxide stress responses. Mol. Microbiol. 45:9-15
104. Panmanee W, Vattanaviboon P, Eiamphungporn W, Whangsuk W, Sallabhan R, Mongkolsuk S. 2002. OhrR, a transcription repressor that senses and responds to changes in organic peroxide levels in Xanthomonas campestris pv. phaseoli. Mol. Microbiol. 45:1647-54
105. Inoue Y, Matsuda T, Sugiyama K, Izawa S, Kimura A. 1999. Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae. J. Biol. Chem. 274:27002-9
106. Flohé L. 1989. The selenoprotein glutathione peroxidase. In Glutathione. Chemical, Biochemical and Medical Aspects, Part A, pp. 643-731. New York: Wiley