Biological chemistry and functionality of protein sulfenic acids and related thiol modifications

Free Radical Research

Volumn 50, Issue 2, 2016, Pages 172-194

  Devarie Baez, Nelmi O ^a   Lopez, Elsa I Silva ^a   Furdui, Cristina M ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Chemistry; reactive oxygen species; redox status; sulfenic acid; thiols

Indexed keywords

5' METHYLTHIOADENOSINE PHOSPHORYLASE; ABELSON KINASE; ACYLGLYCEROL LIPASE; ADAPTOR PROTEIN; AMINO ACID TRANSFER RNA LIGASE; CATHEPSIN K; COPPER ZINC SUPEROXIDE DISMUTASE; DEUBIQUITINASE; DIHYDROLIPOAMIDE DEHYDROGENASE; DJ 1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; JANUS KINASE 2; METHIONINE ADENOSYLTRANSFERASE; METHIONINE SULFOXIDE REDUCTASE; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN SH2; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; RECOVERIN; SULFENIC ACID DERIVATIVE; THIOL; VASCULOTROPIN RECEPTOR 2; XANTHINE DEHYDROGENASE; XANTHINE OXIDASE; CYSTEINE; THIOL DERIVATIVE;

ANALYTIC METHOD; ARTICLE; EPIGENETICS; HUMAN; MICROENVIRONMENT; NONHUMAN; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION; SYNTHESIS; ANIMAL; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; CYSTEINE; EPIGENOMICS; HUMANS; OXIDATION-REDUCTION; PROTEINS; SIGNAL TRANSDUCTION; SULFENIC ACIDS; SULFHYDRYL COMPOUNDS;

EID: 84955462575     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2015.1090571     Document Type: Article

References (229)

1. Ferrer-Sueta G, Manta B, Botti H, Radi R, Trujillo M, Denicola A. Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem Res Toxicol 2011;24:434-450.
2. Meng FG, Zhang ZY. Redox regulation of protein tyrosine phosphatase activity by hydroxyl radical. Biochim Biophys Acta 2013;1834:464-469.
3. Carballal S, Radi R, Kirk MC, Barnes S, Freeman BA, Alvarez B. Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite. Biochemistry 2003;42:9906-9914.
4. Nagy P, Ashby MT. Reactive sulfur species: kinetics and mechanisms of the oxidation of cysteine by hypohalous acid to give cysteine sulfenic acid. J Am Chem Soc 2007;129:14082-14091.
5. Barrett TJ, Pattison DI, Leonard SE, Carroll KS, Davies MJ, Hawkins CL. Inactivation of thiol-dependent enzymes by hypothiocyanous acid: role of sulfenyl thiocyanate and sulfenic acid intermediates. Free Radic Biol Med 2012;52:1075-1085.
6. Heinecke J, Ford PC. Formation of cysteine sulfenic acid by oxygen atom transfer from nitrite. J Am Chem Soc 2010;132:9240-9243.
7. Heinecke JL, Khin C, Pereira JC, Suarez SA, Iretskii AV, Doctorovich F, et al. Nitrite reduction mediated by heme models. Routes to NO and HNO? J Am Chem Soc 2013;135:4007-4017.
8. Nagy P, Lemma K, Ashby MT. Reactive sulfur species: kinetics and mechanisms of the reaction of cysteine thiosulfinate ester with cysteine to give cysteine sulfenic acid. J Org Chem 2007;72:8838-8846.
9. Keceli G, Toscano JP. Reactivity of C-terminal cysteines with HNO. Biochemistry 2014;53:3689-3698.
10. Zhukova L, Zhukov I, Bal W, Wyslouch-Cieszynska A. Redox modifications of the C-terminal cysteine residue cause structural changes in S100A1 and S100B proteins. Biochim Biophys Acta 2004;1742:191-201.
11. Goto K, Tokitoh N, Okazaki R. Synthesis of a stable arenesulfenic acid bearing a bowl-shaped macrobicyclic cyclophane skeleton. Angew Chem Int Ed Engl 1995;34:1124-1126.
12. Saiki T, Goto K, Tokitoh N, Okazaki R. Synthesis and structure of a bridged calix[6]arene with a sulfenic acid functionality in the cavity. J Org Chem 1996;61:2924-2925.
13. Nakamura N. A stable sulfenic acid, 9-triptycenesulfenic acid: its isolation and characterization. J Am Chem Soc 1983;105:7172-7173.
14. Ishihara M, Abe N, Sase S, Goto K. Synthesis, structure, and reactivities of a stable primary-alkyl-substituted sulfenic acid. Chem Lett 2015;44:615-617.
15. Li XB, Xu ZF, Liu LJ, Liu JT. Synthesis and identification of solution-stable sulfenic acids: perfluoroalkanesulfenic acids. Eur J Org Chem 2014;2014:1182-1188.
16. Freeman F, Adesina IT, La JL, Lee JY, Poplawski AA. Conformers of cysteine and cysteine sulfenic acid and mechanisms of the reaction of cysteine sulfenic acid with 5,5-dimethyl-1,3-cyclohexanedione (dimedone). J Phys Chem B 2013;117:16000-16012.
17. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, et al. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 2003;423:769-773.
18. Sarma BK, Mugesh G. Redox regulation of protein tyrosine phosphatase 1B (PTP1B): a biomimetic study on the unexpected formation of a sulfenyl amide intermediate. J Am Chem Soc 2007;129:8872-8881.
19. van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 2003;423:773-777.
20. Sivaramakrishnan S, Keerthi K, Gates KS. A chemical model for redox regulation of protein tyrosine phosphatase 1B (PTP1B) activity. J Am Chem Soc 2005;127:10830-10831.
21. Poole LB, Ellis HR. Identification of cysteine sulfenic acid in AhpC of alkyl hydroperoxide reductase. Methods Enzymol 2002;348:122-36.
22. Furdui CM, Poole LB. Chemical approaches to detect and analyze protein sulfenic acids. Mass Spectrom Rev 2014;33126-146.
23. Reisz JA, Bechtold E, King SB, Poole LB, Furdui CM. Thiol-blocking electrophiles interfere with labeling and detection of protein sulfenic acids. FEBS J 2013;280:6150-6161.
24. Qian J, Klomsiri C, Wright MW, King SB, Tsang AW, Poole LB, Furdui CM. Simple synthesis of 1,3-cyclopentanedione derived probes for labeling sulfenic acid proteins. Chem Commun (Camb) 2011;47:9203-9205.
25. Jonsson TJ, Tsang AW, Lowther WT, Furdui CM. Identification of intact protein thiosulfinate intermediate in the reduction of cysteine sulfinic acid in peroxiredoxin by human sulfiredoxin. J Biol Chem 2008;283:22890-22894.
26. Haynes AC, Qian J, Reisz JA, Furdui CM, Lowther WT. Molecular basis for the resistance of human mitochondrial 2-Cys peroxiredoxin 3 to hyperoxidation. J Biol Chem 2013;288:29714-29723.
27. Poole TH, Reisz JA, Zhao W, Poole LB, Furdui CM, King SB. Strained cycloalkynes as new protein sulfenic acid traps. J Am Chem Soc 2014;136:6167-6170.
28. Qian J, Wani R, Klomsiri C, Poole LB, Tsang AW, Furdui CM. A simple and effective strategy for labeling cysteine sulfenic acid in proteins by utilization of beta-ketoesters as cleavable probes. Chem Commun (Camb) 2012;48:4091-4093.
29. 13C NMR analysis of the cysteine-sulfenic acid redox center of enterococcal NADH peroxidase. Biochemistry 1997;36:8611-8618.
30. Baez NO, Reisz JA, Furdui CM. Mass spectrometry in studies of protein thiol chemistry and signaling: opportunities and caveats. Free Radic Biol Med 2015;80:191-211.
31. Davis FA, Billmers RL. Chemistry of sulfenic acids. 4. The first direct evidence for the involvement of sulfenic acids in the oxidation of thiols. J Am Chem Soc 1981;103:7016-7018.
32. Ellis HR, Poole LB. 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 1997;36:15013-15018.
33. Benitez LV, Allison WS. 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 1974;249:6234-6243.
34. Poole LB, Zeng BB, Knaggs SA, Yakubu M, King SB. Synthesis of chemical probes to map sulfenic acid modifications on proteins. Bioconjug Chem 2005;16:1624-1628.
35. Nelson KJ, Klomsiri C, Codreanu SG, Soito L, Liebler DC, Rogers LC, et al. Use of dimedone-based chemical probes for sulfenic acid detection methods to visualize and identify labeled proteins. Methods Enzymol 2010;473:95-115.
36. Poole LB, Klomsiri C, Knaggs SA, Furdui CM, Nelson KJ, Thomas MJ, et al. Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. Bioconjug Chem 2007;18:2004-2017.
37. Klomsiri C, Nelson KJ, Bechtold E, Soito L, Johnson LC, Lowther WT, et al. Use of dimedone-based chemical probes for sulfenic acid detection evaluation of conditions affecting probe incorporation into redox-sensitive proteins. Methods Enzymol 2010;473:77-94.
38. Bansal N, Mims J, Kuremsky JG, Olex AL, Zhao W, Yin L, et al. Broad phenotypic changes associated with gain of radiation resistance in head and neck squamous cell cancer. Antioxid Redox Signal 2014;21:221-236.
39. Leonard SE, Reddie KG, Carroll KS. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. ACS Chem Biol 2009;4783-799.
40. Seo YH, Carroll KS. Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies. Proc Natl Acad Sci U S A 2009;106:16163-16168.
41. Charles RL, Schroder E, May G, Free P, Gaffney PR, Wait R, et al. Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol Cell Proteomics 2007;6:1473-1484.
42. Truong TH, Garcia FJ, Seo YH, Carroll KS. Isotope-coded chemical reporter and acid-cleavable affinity reagents for monitoring protein sulfenic acids. Bioorg Med Chem Lett 2011;21:5015-5020.
43. Seo YH, Carroll KS. Quantification of protein sulfenic acid modifications using isotope-coded dimedone and iododimedone. Angew Chem Int Ed Engl 2011;50:1342-1345.
44. Yang J, Gupta V, Carroll KS, Liebler DC. Site-specific mapping and quantification of protein S-sulphenylation in cells. Nat Commun 2014;5:4776.
45. Yang J, Gupta V, Tallman KA, Porter NA, Carroll KS, Liebler DC. Global, in situ, site-specific analysis of protein Ssulfenylation. Nat Protoc 2015;10:1022-1037.
46. Liu CT, Benkovic SJ. Capturing a sulfenic acid with arylboronic acids and benzoxaborole. J Am Chem Soc 2013;135:14544-14547.
47. Galardon E, Padovani D. Reactivity of persulfides toward strained bicyclo[6.1.0]nonyne derivatives: relevance to chemical tagging of proteins. Bioconjug Chem 2015;26:1013-1016.
48. Katsuyama M, Fan C, Arakawa N, Nishinaka T, Miyagishi M, Taira K, Yabe-Nishimura C. Essential role of ATF-1 in induction of NOX1, a catalytic subunit of NADPH oxidase: involvement of mitochondrial respiratory chain. Biochem J 2005;386:255-261.
49. Lee SB, Bae IH, Bae YS, Um HD. Link between mitochondria and NADPH oxidase 1 isozyme for the sustained production of reactive oxygen species and cell death. J Biol Chem 2006;281:36228-36235.
50. Hall A, Karplus PA, Poole LB. Typical 2-Cys peroxiredoxins-structures, mechanisms and functions. FEBS J 2009;276:2469-2477.
51. Wood ZA, Poole LB, Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 2003;300:650-653.
52. Jang HH, Kim SY, Park SK, Jeon HS, Lee YM, Jung JH, et al. Phosphorylation and concomitant structural changes in human 2-Cys peroxiredoxin isotype I differentially regulate its peroxidase and molecular chaperone functions. FEBS Lett 2006;580:351-355.
53. Chae HZ, Oubrahim H, Park JW, Rhee SG, Chock PB. Protein glutathionylation in the regulation of peroxiredoxins: a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators. Antioxid Redox Signal 2012;16:506-523.
54. 2 accumulation for cell signaling. Cell 2010;140:517-528.
55. Chang TS, Jeong W, Choi SY, Yu S, Kang SW, Rhee SG. Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J Biol Chem 2002;277:25370-25376.
56. Sheng Y, Abreu IA, Cabelli DE, Maroney MJ, Miller AF, Teixeira M, Valentine JS. Superoxide dismutases and superoxide reductases. Chem Rev 2014;114:3854-3918.
57. Fukai T, Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 2011;15:1583-1606.
58. Wilcox KC, Zhou L, Jordon JK, Huang Y, Yu Y, Redler RL, et al. Modifications of superoxide dismutase (SOD1) in human erythrocytes: a possible role in amyotrophic lateral sclerosis. J Biol Chem 2009;284:13940-13947.
59. Redler RL, Wilcox KC, Proctor EA, Fee L, Caplow M, Dokholyan NV. Glutathionylation at Cys-111 induces dissociation of wild type and FALS mutant SOD1 dimers. Biochemistry 2011;50:7057-7066.
60. Leinartaite L, Johansson AS. Disulfide scrambling in superoxide dismutase 1 reduces its cytotoxic effect in cultured cells and promotes protein aggregation. PLoS One 2013;8:e78060.
61. Fujiwara N, Nakano M, Kato S, Yoshihara D, Ookawara T, Eguchi H, et al. Oxidative modification to cysteine sulfonic acid of Cys111 in human copper-zinc superoxide dismutase. J Biol Chem 2007;282:35933-35944.
62. Cozzolino M, Amori I, Pesaresi MG, Ferri A, Nencini M, Carri MT. Cysteine 111 affects aggregation and cytotoxicity of mutant Cu,Zn-superoxide dismutase associated with familial amyotrophic lateral sclerosis. J Biol Chem 2008;283:866-874.
63. Boschi-Muller S, Olry A, Antoine M, Branlant G. The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 2005;1703:231-238.
64. Boschi-Muller S, Azza S, Sanglier-Cianferani S, Talfournier F, Van Dorsselear A, Branlant G. A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J Biol Chem 2000;275:35908-35913.
65. Lowther WT, Brot N, Weissbach H, Honek JF, Matthews BW. Thiol-disulfide exchange is involved in the catalytic mechanism of peptide methionine sulfoxide reductase. Proc Natl Acad Sci U S A 2000;97:6463-6468.
66. Srivastava S, Watowich SJ, Petrash JM, Srivastava SK, Bhatnagar A. Structural and kinetic determinants of aldehyde reduction by aldose reductase. Biochemistry 1999;38:42-54.
67. Ramana KV, Dixit BL, Srivastava S, Balendiran GK, Srivastava SK, Bhatnagar A. Selective recognition of glutathiolated aldehydes by aldose reductase. Biochemistry 2000;39:12172-12180.
68. Kaiserova K, Srivastava S, Hoetker JD, Awe SO, Tang XL, Cai J, Bhatnagar A. Redox activation of aldose reductase in the ischemic heart. J Biol Chem 2006;281:15110-15120.
69. Kaiserova K, Tang XL, Srivastava S, Bhatnagar A. Role of nitric oxide in regulating aldose reductase activation in the ischemic heart. J Biol Chem 2008;283:9101-9112.
70. Wetzelberger K, Baba SP, Thirunavukkarasu M, Ho YS, Maulik N, Barski OA, et al. Postischemic deactivation of cardiac aldose reductase: role of glutathione Stransferase P and glutaredoxin in regeneration of reduced thiols from sulfenic acids. J Biol Chem 2010;285:26135-26148.
71. Kuwabara Y, Nishino T, Okamoto K, Matsumura T, Eger BT, Pai EF. Unique amino acids cluster for switching from the dehydrogenase to oxidase form of xanthine oxidoreductase. Proc Natl Acad Sci USA 2003;100:8170-8175.
72. Nishino T, Okamoto K, Eger BT, Pai EF. Mammalian xanthine oxidoreductase - mechanism of transition from xanthine dehydrogenase to xanthine oxidase. FEBS J 2008;275:3278-3289.
73. Robinson DR, Wu YM, Lin SF. The protein tyrosine kinase family of the human genome. Oncogene 2000;19:5548-5557.
74. Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010;141:1117-1134.
75. Chen Q, Olashaw N, Wu J. Participation of reactive oxygen species in the lysophosphatidic acid-stimulated mitogenactivated protein kinase kinase activation pathway. J Biol Chem 1995;270:28499-28502.
76. 2 for plateletderived growth factor signal transduction. Science 1995;270:296-299.
77. 2 production leads to localized cysteine sulfenic acid formation on proteins during lysophosphatidic acid-mediated cell signaling. Free Radic Biol Med 2014;71:49-60.
78. Oakley FD, Abbott D, Li Q, Engelhardt JF. Signaling components of redox active endosomes: the redoxosomes. Antioxid Redox Signal 2009;11:1313-1333.
79. Spencer NY, Engelhardt JF. The basic biology of redoxosomes in cytokine-mediated signal transduction and implications for disease-specific therapies. Biochemistry 2014;53:1551-1564.
80. Truong TH, Carroll KS. Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 2012;51:9954-9965.
81. Kato M, Iwashita T, Takeda K, Akhand AA, Liu W, Yoshihara M, et al. Ultraviolet light induces redox reaction-mediated dimerization and superactivation of oncogenic Ret tyrosine kinases. Mol Biol Cell 2000;11:93-101.
82. Lee SR, Kwon KS, Kim SR, Rhee SG. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem 1998;273:15366-15372.
83. Barrett WC, DeGnore JP, Konig S, Fales HM, Keng YF, Zhang ZY, et al. Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 1999;38:6699-6705.
84. Saito S, Frank GD, Mifune M, Ohba M, Utsunomiya H, Motley ED, et al. Ligand-independent trans-activation of the platelet-derived growth factor receptor by reactive oxygen species requires protein kinase C-d and c-Src. J Biol Chem 2002;277:44695-44700.
85. 2 signaling. Nat Chem Biol 2015;11:64-70.
86. Ushio-Fukai M. Vascular signaling through G proteincoupled receptors: new concepts. Curr Opin Nephrol Hypertens 2009;18:153-159.
87. Sun L, Ye RD. Role of G protein-coupled receptors in inflammation. Acta Pharmacol Sin 2012;33:342-350.
88. Svineng G, Ravuri C, Rikardsen O, Huseby NE, Winberg JO. The role of reactive oxygen species in integrin and matrix metalloproteinase expression and function. Connect Tissue Res 2008;49:197-202.
89. Kozai D, Ogawa N, Mori Y. Redox regulation of transient receptor potential channels. Antioxid Redox Signal 2014;21:971-986.
90. Paulsen CE, Truong TH, Garcia FJ, Homann A, Gupta V, Leonard SE, Carroll KS. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol 2011;8:57-64.
91. Lemmon MA, Schlessinger J, Ferguson KM. The EGFR family: not so prototypical receptor tyrosine kinases. Cold Spring Harb Perspect Biol 2014;6:a020768.
92. Ogiso H, Ishitani R, Nureki O, Fukai S, Yamanaka M, Kim JH, et al. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 2002;110:775-787.
93. Schwartz PA, Kuzmic P, Solowiej J, Bergqvist S, Bolanos B, Almaden C, et al. Covalent EGFR inhibitor analysis reveals importance of reversible interactions to potency and mechanisms of drug resistance. Proc Natl Acad Sci U S A 2014;111:173-178.
94. Kaplan N, Urao N, Furuta E, Kim SJ, Razvi M, Nakamura Y, et al. Localized cysteine sulfenic acid formation by vascular endothelial growth factor: role in endothelial cell migration and angiogenesis. Free Radic Res 2011;45:1124-1135.
95. Kemble DJ, Sun G. Direct and specific inactivation of protein tyrosine kinases in the Src and FGFR families by reversible cysteine oxidation. Proc Natl Acad Sci U S A 2009;106:5070-5075.
96. Meng TC, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Molecular Cell 2002;9:387-399.
97. Denu JM, Tanner KG. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 1998;37:5633-5642.
98. Ostman A, Frijhoff J, Sandin A, Bohmer FD. Regulation of protein tyrosine phosphatases by reversible oxidation. J Biochem 2011;150:345-356.
99. 3POOH). J Am Chem Soc 2007;129:5320-5321.
100. 3POOH). Bioorg Med Chem Lett 2009;19:218-221.
101. Jeon TJ, Chien PN, Chun HJ, Ryu SE. Structure of the catalytic domain of protein tyrosine phosphatase sigma in the sulfenic acid form. Mol Cells 2013;36:55-61.
102. Michalek RD, Nelson KJ, Holbrook BC, Yi JS, Stridiron D, Daniel LW, et al. The requirement of reversible cysteine sulfenic acid formation for T cell activation and function. J Immunol 2007;179:6456-6467.
103. Crump KE, Juneau DG, Poole LB, Haas KM, Grayson JM. The reversible formation of cysteine sulfenic acid promotes B-cell activation and proliferation. Eur J Immunol 2012;42:2152-2164.
104. Chen CY, Willard D, Rudolph J. Redox regulation of SH2-domain-containing protein tyrosine phosphatases by two backdoor cysteines. Biochemistry 2009;48:1399-1409.
105. Tang H, Hao Q, Rutherford SA, Low B, Zhao ZJ. Inactivation of SRC family tyrosine kinases by reactive oxygen species in vivo. J Biol Chem 2005;280:23918-23925.
106. Giannoni E, Buricchi F, Raugei G, Ramponi G, Chiarugi P. Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchoragedependent cell growth. Mol Cell Biol 2005;25:6391-6403.
107. Akhand AA, Pu M, Senga T, Kato M, Suzuki H, Miyata T, et al. Nitric oxide controls Src kinase activity through a sulfhydryl group modification-mediated Tyr-527-independent and Tyr-416-linked mechanism. J Biol Chem 1999;274:25821-25826.
108. Minetti M, Mallozzi C, Di Stasi AM. Peroxynitrite activates kinases of the Src family and upregulates tyrosine phosphorylation signaling. Free Radic Biol Med 2002;33:744-754.
109. Wood ST, Long DL, Reisz JA, Yammani RR, Burke EA, Klomsiri C, et al. Cysteine-mediated redox regulation of cell signaling in chondrocytes stimulated with fibronectin fragments. Arthritis Rheumatol 2015.
110. Shaul Y. c-Abl: activation and nuclear targets. Cell Death Differ 2000;7:10-16.
111. Cao C, Leng Y, Kufe D. Catalase activity is regulated by c-Abl and Arg in the oxidative stress response. J Biol Chem 2003;278:29667-29675.
112. Wang X, Zeng L, Wang J, Chau JF, Lai KP, Jia D, et al. A positive role for c-Abl in Atm and Atr activation in DNA damage response. Cell Death Differ 2011;18:5-15.
113. Sun X, Majumder P, Shioya H, Wu F, Kumar S, Weichselbaum R, et al. Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species. J Biol Chem 2000;275:17237-17240.
114. Leonberg AK, Chai YC. The functional role of cysteine residues for c-Abl kinase activity. Mol Cell Biochem 2007;304:207-212.
115. Mamoon NM, Smith JK, Chatti K, Lee S, Kundrapu K, Duhe RJ. Multiple cysteine residues are implicated in Janus kinase 2-mediated catalysis. Biochemistry 2007;46:14810-14818.
116. Smith JK, Patil CN, Patlolla S, Gunter BW, Booz GW, Duhe RJ. Identification of a redox-sensitive switch within the JAK2 catalytic domain. Free Radic Biol Med 2012;52:1101-1110.
117. Gonzalez E, McGraw TE. The Akt kinases: isoform specificity in metabolism and cancer. Cell Cycle 2009;8:2502-2508.
118. Gonzalez E, McGraw TE. Insulin-modulated Akt subcellular localization determines Akt isoform-specific signaling. Proc Natl Acad Sci USA 2009;106:7004-7009.
119. Dummler B, Hemmings BA. Physiological roles of PKB/Akt isoforms in development and disease. Biochem Soc Trans 2007;35:231-235.
120. Wani R, Qian J, Yin L, Bechtold E, King SB, Poole LB, et al. Isoform-specific regulation of Akt by PDGF-induced reactive oxygen species. Proc Natl Acad Sci USA 2011;108:10550-10555.
121. Brozinick Jr JT, Roberts BR, Dohm GL. Defective signaling through Akt-2 and Akt-3 but not Akt-1 in insulinresistant human skeletal muscle: potential role in insulin resistance. Diabetes 2003;52:935-941.
122. Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB, et al. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKBb). Science 2001;292:1728-1731.
123. Garofalo RS, Orena SJ, Rafidi K, Torchia AJ, Stock JL, Hildebrandt AL, et al. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKBb. J Clin Invest 2003;112:197-208.
124. George S, Rochford JJ, Wolfrum C, Gray SL, Schinner S, Wilson JC, et al. A family with severe insulin resistance and diabetes due to a mutation in AKT2. Science 2004;304:1325-1328.
125. Ardite E, Barbera JA, Roca J, Fernandez-Checa JC. Glutathione depletion impairs myogenic differentiation of murine skeletal muscle C2C12 cells through sustained NF-κB activation. Am J Pathol 2004;165:719-728.
126. Hansen JM, Klass M, Harris C, Csete M. A reducing redox environment promotes C2C12 myogenesis: implications for regeneration in aged muscle. Cell Biol Int 2007;31:546-553.
127. Clark AR, Toker A. Signalling specificity in the Akt pathway in breast cancer. Biochem Soc Trans 2014;42:1349-1355.
128. Iwakura Y, Nakae S, Saijo S, Ishigame H. The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol Rev 2008;226:57-79.
129. Nolin JD, Tully JE, Hoffman SM, Guala AS, van der Velden JL, Poynter ME, et al. The glutaredoxin/S-glutathionylation axis regulates interleukin-17A-induced proinflammatory responses in lung epithelial cells in association with S-glutathionylation of nuclear factor kB family proteins. Free Radic Biol Med 2014;73:143-153.
130. Gupta S. Molecular signaling in death receptor and mitochondrial pathways of apoptosis (Review). Int J Oncol 2003;22:15-20.
131. Luanpitpong S, Chanvorachote P, Stehlik C, Tse W, Callery PS, Wang L, Rojanasakul Y. Regulation of apoptosis by Bcl-2 cysteine oxidation in human lung epithelial cells. Mol Biol Cell 2013;24:858-869.
132. Canet-Aviles RM, Wilson MA, Miller DW, Ahmad R, McLendon C, Bandyopadhyay S, et al. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteinesulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci USA 2004;101:9103-9108.
133. Kato I, Maita H, Takahashi-Niki K, Saito Y, Noguchi N, Iguchi-Ariga SM, Ariga H. Oxidized DJ-1 inhibits p53 by sequestering p53 from promoters in a DNA-binding affinity-dependent manner. Mol Cell Biol 2013;33:340-359.
134. Kinumi T, Kimata J, Taira T, Ariga H, Niki E. Cysteine-106 of DJ-1 is the most sensitive cysteine residue to hydrogen peroxide-mediated oxidation in vivo in human umbilical vein endothelial cells. Biochem Biophys Res Commun 2004;317:722-728.
135. Takahashi-Niki K, Niki T, Taira T, Iguchi-Ariga SM, Ariga H. Reduced anti-oxidative stress activities of DJ-1 mutants found in Parkinson's disease patients. Biochem Biophys Res Commun 2004;320:389-397.
136. Williams-Ashman HG, Seidenfeld J, Galletti P. Trends in the biochemical pharmacology of 5′-deoxy-5′-methylthioadenosine. Biochem Pharmacol 1982;31:277-288.
137. Fernandez-Irigoyen J, Santamaria M, Sanchez-Quiles V, Latasa MU, Santamaria E, Munoz J, et al. Redox regulation of methylthioadenosine phosphorylase in liver cells: molecular mechanism and functional implications. Biochem J 2008;411:457-465.
138. Nagahara N, Sawada N. The mercaptopyruvate pathway in cysteine catabolism: a physiologic role and related disease of the multifunctional 3-mercaptopyruvate sulfurtransferase. Curr Med Chem 2006;13: 1219-1230.
139. Nagahara N, Katayama A. Post-translational regulation of mercaptopyruvate sulfurtransferase via a low redox potential cysteine-sulfenate in the maintenance of redox homeostasis. J Biol Chem 2005;280:34569-34576.
140. Conway ME, Yennawar N, Wallin R, Poole LB, Hutson SM. Human mitochondrial branched chain aminotransferase: structural basis for substrate specificity and role of redox active cysteines. Biochim Biophys Acta 2003;1647:61-65.
141. Conway ME, Poole LB, Hutson SM. Roles for cysteine residues in the regulatory CXXC motif of human mitochondrial branched chain aminotransferase enzyme. Biochemistry 2004;43:7356-7364.
142. Conway ME, Yennawar N, Wallin R, Poole LB, Hutson SM. Identification of a peroxide-sensitive redox switch at the CXXC motif in the human mitochondrial branched chain aminotransferase. Biochemistry 2002;41:9070-9078.
143. Markham GD, Pajares MA. Structure-function relationships in methionine adenosyltransferases. Cell Mol Life Sci 2009;66:636-648.
144. Sanchez-Gongora E, Ruiz F, Mingorance J, An W, Corrales FJ, Mato JM. Interaction of liver methionine adenosyltransferase with hydroxyl radical. FASEB J 1997;11:1013-1019.
145. Morettin A, Baldwin RM, Cote J. Arginine methyltransferases as novel therapeutic targets for breast cancer. Mutagenesis 2015;30:177-189.
146. Cha B, Jho EH. Protein arginine methyltransferases (PRMTs) as therapeutic targets. Expert Opin Ther Targets 2012;16:651-664.
147. Kuhn P, Xu W. Protein arginine methyltransferases: nuclear receptor coregulators and beyond. Prog Mol Biol Transl Sci 2009;87:299-342.
148. Sydow K, Munzel T. ADMA and oxidative stress. Atheroscler Suppl 2003;4:41-51.
149. Cooke JP. ADMA: its role in vascular disease. Vasc Med 2005;10Suppl1:S11-S17.
150. Morales Y, Nitzel DV, Price OM, Gui S, Li J, Qu J, Hevel JM. Redox control of protein arginine methyltransferase 1 (PRMT1) activity. J Biol Chem 2015;290:14915-14926.
151. Anastasiou D, Poulogiannis G, Asara JM, Boxer MB, Jiang JK, Shen M, et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011;334:1278-1283.
152. Junod AF, Clement A, Jornot L, Petersen H. Differential effects of hyperoxia and hydrogen peroxide on thymidine kinase and adenosine kinase activities of cultured endothelial cells. Biochim Biophys Acta 1985;847:20-24.
153. Sun R, Eriksson S, Wang L. Oxidative stress induced Sglutathionylation and proteolytic degradation of mitochondrial thymidine kinase 2. J Biol Chem 2012;287:24304-24312.
154. Sankaranarayanan R, Moras D. The fidelity of the translation of the genetic code. Acta Biochim Pol 2001;48:323-335.
155. Ling J, Soll D. Severe oxidative stress induces protein mistranslation through impairment of an aminoacyltRNA synthetase editing site. Proc Natl Acad Sci USA 2010;107:4028-4033.
156. Cura V, Moras D, Kern D. Sequence analysis and modular organization of threonyl-tRNA synthetase from Thermus thermophilus and its interrelation with threonyl-tRNA synthetases of other origins. Eur J Biochem 2000;267:379-393.
157. Cruzen ME, Arfin SM. Nucleotide and deduced amino acid sequence of human threonyl-tRNA synthetase reveals extensive homology to the Escherichia coli and yeast enzymes. J Biol Chem 1991;266:9919-9923.
158. Wu J, Fan Y, Ling J. Mechanism of oxidant-induced mistranslation by threonyl-tRNA synthetase. Nucleic Acids Res 2014;42:6523-6531.
159. Alonso E, Cervera J, Garcia-Espana A, Bendala E, Rubio V. Oxidative inactivation of carbamoyl phosphate synthetase (ammonia). Mechanism and sites of oxidation, degradation of the oxidized enzyme, and inactivation by glycerol, EDTA, and thiol protecting agents. J Biol Chem 1992;267:4524-4532.
160. Hart EJ, Powers-Lee SG. Role of Cys-1327 and Cys-1337 in redox sensitivity and allosteric monitoring in human carbamoyl phosphate synthetase. J Biol Chem 2009;284:5977-5985.
161. Lu KP, Zhou XZ. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 2007;8:904-916.
162. Keeney JT, Swomley AM, Harris JL, Fiorini A, Mitov MI, Perluigi M, et al. Cell cycle proteins in brain in mild cognitive impairment: insights into progression to Alzheimer disease. Neurotox Res 2012;22:220-230.
163. Innes BT, Sowole MA, Gyenis L, Dubinsky M, Konermann L, Litchfield DW, et al. Peroxide-mediated oxidation and inhibition of the peptidyl-prolyl isomerase Pin1. Biochim Biophys Acta 2015;1852:905-912.
164. Chen CH, Li W, Sultana R, You MH, Kondo A, Shahpasand K, et al. Pin1 cysteine-113 oxidation inhibits its catalytic activity and cellular function in Alzheimer's disease. Neurobiol Dis 2015;76:13-23.
165. Heideker J, Wertz IE. DUBs, the regulation of cell identity and disease. Biochem J 2015;465:1-26.
166. Enesa K, Evans P. The biology of A20-like molecules. Adv Exp Med Biol 2014;809:33-48.
167. Verstrepen L, Carpentier I, Beyaert R. The biology of A20-binding inhibitors of NF-κB activation (ABINs). Adv Exp Med Biol 2014;809:13-31.
168. Kulathu Y, Garcia FJ, Mevissen TE, Busch M, Arnaudo N, Carroll KS, et al. Regulation of A20 and other OTU deubiquitinases by reversible oxidation. Nat Commun 2013;4:1569.
169. Cotto-Rios XM, Bekes M, Chapman J, Ueberheide B, Huang TT. Deubiquitinases as a signaling target of oxidative stress. Cell Rep 2012;2:1475-1484.
170. Godat E, Herve-Grvepinet V, Veillard F, Lecaille F, Belghazi M, Bromme D, Lalmanach G. Regulation of cathepsin K activity by hydrogen peroxide. Biol Chem 2008;389:1123-1126.
171. Lalmanach G, Diot E, Godat E, Lecaille F, Herve-Grepinet V. Cysteine cathepsins and caspases in silicosis. Biol Chem 2006;387:863-870.
172. Huang Z, Pinto JT, Deng H, Richie JP, Inhibition of caspase-3 activity and activation by protein glutathionylation. Biochem Pharmacol 2008;75:2234-2244.
173. Zech B, Wilm M, van Eldik R, Brune B. Mass spectrometric analysis of nitric oxide-modified caspase-3. J Biol Chem 1999;274:20931-20936.
174. Xu Z, Lam LS, Lam LH, Chau SF, Ng TB, Au SW. Molecular basis of the redox regulation of SUMO proteases: a protective mechanism of intermolecular disulfide linkage against irreversible sulfhydryl oxidation. FASEB J 2008;22:127-137.
175. Dinh TP, Freund TF, Piomelli D. A role for monoglyceride lipase in 2-arachidonoylglycerol inactivation. Chem Phys Lipids 2002;121:149-158.
176. King AR, Dotsey EY, Lodola A, Jung KM, Ghomian A, Qiu Y, et al. Discovery of potent and reversible monoacylglycerol lipase inhibitors. Chem Biol 2009;16:1045-1052.
177. King AR, Lodola A, Carmi C, Fu J, Mor M, Piomelli D. A critical cysteine residue in monoacylglycerol lipase is targeted by a new class of isothiazolinone-based enzyme inhibitors. Br J Pharmacol 2009;157:974-983.
178. Labar G, Bauvois C, Borel F, Ferrer JL, Wouters J, Lambert DM. Crystal structure of the human monoacylglycerol lipase, a key actor in endocannabinoid signaling. Chembiochem 2010;11:218-227.
179. Dotsey EY, Jung KM, Basit A, Wei D, Daglian J, Vacondio F, et al. Peroxide-dependent MGL sulfenylation regulates 2-AG-mediated endocannabinoid signaling in brain neurons. Chem Biol 2015;22:619-628.
180. Harms N, Ras J, Reijnders WN, van Spanning RJ, Stouthamer AH. S-Formylglutathione hydrolase of Paracoccus denitrificans is homologous to human esterase D: a universal pathway for formaldehyde detoxification? J Bacteriol 1996;178:6296-6299.
181. Lee WH, Wheatley W, Benedict WF, Huang CM, Lee EY. Purification, biochemical characterization, and biological function of human esterase D. Proc Natl Acad Sci USA 1986;83:6790-6794.
182. Legler PM, Kumaran D, Swaminathan S, Studier FW, Millard CB. Structural characterization and reversal of the natural organophosphate resistance of a D-type esterase, Saccharomyces cerevisiae S-formylglutathione hydrolase. Biochemistry 2008;47:9592-9601.
183. Legler PM, Leary DH, Hervey WJt, Millard CB. A role for His-160 in peroxide inhibition of S. cerevisiae Sformylglutathione hydrolase: evidence for an oxidation sensitive motif. Arch Biochem Biophys 2012;528:7-20.
184. Patel MS, Vettakkorumakankav NN, Liu TC. Dihydrolipoamide dehydrogenase: activity assays. Methods Enzymol 1995;252:186-195.
185. Yan LJ, Sumien N, Thangthaeng N, Forster MJ. Reversible inactivation of dihydrolipoamide dehydrogenase by mitochondrial hydrogen peroxide. Free Radic Res 2013;47:123-133.
186. Hildebrandt T, Knuesting J, Berndt C, Morgan B, Scheibe R. Cytosolic thiol switches regulating basic cellular functions: GAPDH as an information hub? Biol Chem 2015;396:523-537.
187. Maller C, Schroder E, Eaton P. Glyceraldehyde 3-phosphate dehydrogenase is unlikely to mediate hydrogen peroxide signaling: studies with a novel anti-dimedone sulfenic acid antibody. Antioxid Redox Signal 2011;14:49-60.
188. Jenkins JL, Tanner JJ. High-resolution structure of human D-glyceraldehyde-3-phosphate dehydrogenase. Acta Crystallogr D Biol Crystallogr 2006;62:290-301.
189. Cowan-Jacob SW, Kaufmann M, Anselmo AN, Stark W, Grutter MG. Structure of rabbit-muscle glyceraldehyde-3-phosphate dehydrogenase. Acta Crystallogr D Biol Crystallogr 2003;59:2218-2227.
190. Schuppe-Koistinen I, Moldeus P, Bergman T, Cotgreave IA. S-Thiolation of human endothelial cell glyceraldehyde-3-phosphate dehydrogenase after hydrogen peroxide treatment. Eur J Biochem 1994;221:1033-1037.
191. Grant CM, Quinn KA, Dawes IW. Differential protein Sthiolation of glyceraldehyde-3-phosphate dehydrogenase isoenzymes influences sensitivity to oxidative stress. Mol Cell Biol 1999;19:2650-2656.
192. Cotgreave IA, Gerdes R, Schuppe-Koistinen I, Lind C. Sglutathionylation of glyceraldehyde-3-phosphate dehydrogenase: role of thiol oxidation and catalysis by glutaredoxin. Methods Enzymol 2002;348:175-182.
193. 2 sensitivity of GAPDH to facilitate metabolic adaptation. Nat Chem Biol 2015;11:156-163.
194. Lim S, Dizhoor AM, Ames JB. Structural diversity of neuronal calcium sensor proteins and insights for activation of retinal guanylyl cyclase by GCAP1. Front Mol Neurosci 2014;7:19.
195. Permyakov SE, Nazipova AA, Denesyuk AI, Bakunts AG, Zinchenko DV, Lipkin VM, et al. Recoverin as a redox-sensitive protein. J Proteome Res 2007;6:1855-1863.
196. Permyakov SE, Zernii EY, Knyazeva EL, Denesyuk AI, Nazipova AA, Kolpakova TV, et al. Oxidation mimicking substitution of conservative cysteine in recoverin suppresses its membrane association. Amino Acids 2012;42:1435-1442.
197. 2+ to recoverin. J Biol Chem 2013;288:36160-36167.
198. 2S and NO cooperatively regulate vascular tone by activating a neuroendocrine HNO-TRPA1-CGRP signalling pathway. Nat Commun 2014;5:4381.
199. Andersson DA, Filipovic MR, Gentry C, Eberhardt M, Vastani N, Leffler A, et al. Streptozotocin stimulates TRPA1 directly: involvement of peroxynitrite. J Biol Chem 2015;290:15185-15196.
200. Christakos S, Barletta F, Huening M, Dhawan P, Liu Y, Porta A, Peng X. Vitamin D target proteins: function and regulation. J Cell Biochem 2003;88:238-244.
201. 2+ sensor. J Biol Chem 2002;277:16662-16672.
202. 28K from human brain. Biochemistry 2002;41:6185-6192.
203. 28k are structurally and functionally important. Biochemistry 2005;44:684-693.
204. Vanbelle C, Halgand F, Cedervall T, Thulin E, Akerfeldt KS, Laprevote O, Linse S. Deamidation and disulfide bridge formation in human calbindin D28k with effects on calcium binding. Protein Sci 2005;14:968-979.
205. 28K gene transfer via Herpes Simplex Virus amplicon vector decreases hippocampal damage in vivo following neurotoxic insults. J Neurochem 1999;73:1200-1205.
206. 28k is expressed in osteoblastic cells and suppresses their apoptosis by inhibiting caspase-3 activity. J Biol Chem 2000;275:26328-26332.
207. Svoboda LK, Reddie KG, Zhang L, Vesely ED, Williams ES, Schumacher SM, et al. Redox-sensitive sulfenic acid modification regulates surface expression of the cardiovascular voltage-gated potassium channel Kv1.5. Circ Res 2012;111:842-853.
208. ATP channel gating by S-glutathionylation. J Biol Chem 2011;286:9298-9307.
209. Jerng HH, Pfaffinger PJ. S-Glutathionylation of an auxiliary subunit confers redox sensitivity to Kv4 channel inactivation. PLoS One 2014;9:e93315.
210. Jin X, Yu L, Wu Y, Zhang S, Shi Z, Chen X, et al. SGlutathionylation underscores the modulation of the heteromeric Kir4.1-Kir5.1 channel in oxidative stress. J Physiol 2012;590:5335-5348.
211. Hitchler MJ, Domann FE. Redox regulation of the epigenetic landscape in cancer: a role for metabolic reprogramming in remodeling the epigenome. Free Radic Biol Med 2012;53:2178-2187.
212. Li M, Wilson DM, 3rd. Human apurinic/apyrimidinic endonuclease 1. Antioxid Redox Signal 2014;20:678-707.
213. Kelley MR, Georgiadis MM, Fishel ML. APE1/Ref-1 role in redox signaling: translational applications of targeting the redox function of the DNA repair/redox protein APE1/Ref-1. Curr Mol Pharmacol 2012;5:36-53.
214. Kim YJ, Kim D, Illuzzi JL, Delaplane S, Su D, Bernier M, et al. S-Glutathionylation of cysteine 99 in the APE1 protein impairs abasic endonuclease activity. J Mol Biol 2011;414:313-326.
215. Luo M, Zhang J, He H, Su D, Chen Q, Gross ML, et al. Characterization of the redox activity and disulfide bond formation in apurinic/apyrimidinic endonuclease. Biochemistry 2012;51:695-705.
216. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, Miyamoto S. Rel/NF-κB/IkB family: intimate tales of association and dissociation. Genes Dev 1995;9:2723-2735.
217. Perkins ND, Schmid RM, Duckett CS, Leung K, Rice NR, Nabel GJ. Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc Natl Acad Sci U S A 1992;89:1529-1533.
218. Matthews JR, Botting CH, Panico M, Morris HR, Hay RT. Inhibition of NF-κB DNA binding by nitric oxide. Nucleic Acids Res 1996;24:2236-2242.
219. Klatt P, Pineda Molina E, Perez-Sala D, Lamas S. Novel application of S-nitrosoglutathione-Sepharose to identify proteins that are potential targets for S-nitrosoglutathione-induced mixed-disulphide formation. Biochem J 2000;349:567-578.
220. Pineda-Molina E, Klatt P, Vazquez J, Marina A, Garcia de Lacoba M, Perez-Sala D, Lamas S. Glutathionylation of the p50 subunit of NF-κB: a mechanism for redoxinduced inhibition of DNA binding. Biochemistry 2001;40:14134-14142.
221. Wu Q, Ni X. ROS-mediated DNA methylation pattern alterations in carcinogenesis. Curr Drug Targets 2015;16:13-19.
222. Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK, et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the Ecadherin promoter. Gastroenterol 2008;135:2128-2140, 2140 e1-8.
223. Szumiel I. Ionizing radiation-induced oxidative stress, epigenetic changes and genomic instability: the pivotal role of mitochondria. Int J Radiat Biol 2015;91:1-12.
224. Wang KY, Chen CC, Shen CK. Active DNA demethylation of the vertebrate genomes by DNA methyltransferases: deaminase, dehydroxymethylase or demethylase? Epigenomics 2014;6:353-363.
225. Chen CC, Wang KY, Shen CK. The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 2012;287:33116-33121.
226. Wojdyla K, Williamson J, Roepstorff P, Rogowska-Wrzesinska A. The SNO/SOH TMT strategy for combinatorial analysis of reversible cysteine oxidations. J Proteomics 2015;113:415-434.
227. Wang YT, Piyankarage SC, Williams DL, Thatcher GR. Proteomic profiling of nitrosative stress: protein Soxidation accompanies S-nitrosylation. ACS Chem Biol 2014;9:821-830.
228. Guo J, Gaffrey MJ, Su D, Liu T, Camp DG, Smith RD, Qian WJ. Resin-assisted enrichment of thiols as a general strategy for proteomic profiling of cysteine-based reversible modifications. Nat Protoc 2014;9:64-75.
229. Defelipe LA, Lanzarotti E, Gauto D, Marti MA, Turjanski AG. Protein topology determines cysteine oxidation fate: the case of sulfenyl amide formation among protein families. PLoS Comput Biol 2015;11:e1004051.