Chemical approaches to discovery and study of sources and targets of hydrogen peroxide redox signaling through NADPH oxidase proteins

Annual Review of Biochemistry

Volumn 84, Issue , 2015, Pages 765-790

  Brewer, Thomas F ^a   Garcia, Francisco J ^c   Onak, Carl S ^a   Carroll, Kate S ^c   Chang, Christopher J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Bioorthogonal chemistry; Fluorescent probes; Molecular imaging; Oxidative stress; Posttranslational modifications; Reactive oxygen species

Indexed keywords

CYSTEINE DERIVATIVE; FLUORESCENT DYE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SULFENIC ACID DERIVATIVE; SULFINIC ACID DERIVATIVE;

CELLULAR DISTRIBUTION; CHEMICAL ANALYSIS; ELECTROPHILICITY; HUMAN; IMMUNOLOGICAL PROCEDURES; NONHUMAN; NUCLEOPHILICITY; OXIDATION; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; METABOLISM; OXIDATION REDUCTION REACTION;

MAMMALIA;

ANIMALS; HUMANS; HYDROGEN PEROXIDE; NADPH OXIDASE; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION; SULFENIC ACIDS;

EID: 84930707903     PISSN: 00664154     EISSN: 15454509     Source Type: Book Series    
DOI: 10.1146/annurev-biochem-060614-034018     Document Type: Review

References (152)

1. Thénard LJ. 1818. Observations sur des combinaisons nouvelles entre l'oxigène et divers acides. Ann. Chim. Phys. 8:306-13
2. Loew O. 1900. A new enzyme of general occurrence in organisms. Science 11:701-2
3. Chance B, Oshino N. 1971. Kinetics and mechanisms of catalase in peroxisomes of the mitochondrial fraction. Biochem. J. 122:225-33
4. Chance B, Sies H, Boveris A. 1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:527-605
5. Babior BM, Kipnes RS, Curnutte JT. 1973. Biological defense mechanisms-production by leukocytes of superoxide, a potential bactericidal agent. J. Clin. Investig. 52:741-44
6. Rossi F, Zatti M. 1964. Biochemical aspects of phagocytosis in poly-morphonuclear leucocytes. NADH and NADPH oxidation by the granules of resting and phagocytizing cells. Cell. Mol. Life Sci. 20:21-23
7. Radeke HH, Meier B, Topley N, Flöge J, Habermehl GG, Resch K. 1990. Interleukin 1α and tumor necrosis factor αinduce oxygen radical production in mesangial cells. Kidney Int. 37:767-75
8. Sundaresan M, Yu Z-X, Ferrans VJ, Irani K, Finkel T. 1995. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270:296-99
9. Suh Y-A, Arnold RS, Lassegue B, Shi J, Xu X, et al. 1999. Cell transformation by the superoxidegenerating oxidase Mox1. Nature 401:79-82
10. Bedard K, Krause K-H. 2007. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:245-313
11. O'Neill JS, Reddy AB. 2011. Circadian clocks in human red blood cells. Nature 469:498-503
12. O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F, et al. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469:554-58
13. Kim J-S, Huang TY, Bokoch GM. 2009. Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol. Biol. Cell 20:2650-60
14. Gianni D, Taulet N, DerMardirossian C, Bokoch GM. 2010. c-Src-mediated phosphorylation ofNoxA1 and Tks4 induces the reactive oxygen species (ROS)-dependent formation of functional invadopodia in human colon cancer cells. Mol. Biol. Cell 21:4287-98
15. Niethammer P, Grabher C, Look AT, Mitchison TJ. 2009. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:996-99
16. Dickinson BC, Peltier J, Stone D, Schaffer DV, Chang CJ. 2011. Nox2 redox signalingmaintains essential cell populations in the brain. Nat. Chem. Biol. 7:106-12
17. D'Autreaux B, Toledano MB. 2007. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8:813-24
18. Stone JR, Yang S. 2006. Hydrogen peroxide: a signaling messenger. Antioxid. Redox Signal. 8:243-70
19. Wood ZA, Poole LB, Karplus PA. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650-53
20. Araki K, Inaba K. 2012. Structure, mechanism, and evolution of Ero1 family enzymes. Antioxid. Redox Signal. 16:790-99
21. Dawkes HC, Phillips SEV. 2001. Copper amine oxidase: cunning cofactor and controversial copper. Curr. Opin. Struct. Biol. 11:666-73
22. Kim J-JP, Miura R. 2004. Acyl-CoA dehydrogenases and acyl-CoA oxidases. Eur. J. Biochem. 271:483-93
23. Halliwell B, Gutteridge JMC. 1999. Free Radicals in Biology and Medicine. Oxford, UK: Oxford Univ. Press
24. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, et al. 2006. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3:281-86
25. Markvicheva KN, Bilan DS, Mishina NM, Gorokhovatsky AY, Vinokurov LM, et al. 2011. A genetically encoded sensor for H2O2 with expanded dynamic range. Bioorg. Med. Chem. 19:1079-84
26. Bilan DS, Pase L, Joosen L, Gorokhovatsky AY, Ermakova YG, et al. 2012. HyPer-3: a genetically encoded H2O2 probe with improved performance for ratiometric and fluorescence lifetime imaging. Am. Chem. Soc. Chem. Biol. 8:535-42
27. Dwyer DJ, Belenky PA, Yang JH, MacDonald IC, Martell JD, et al. 2014. Antiobiotics induce redoxrelated physiological alterations as part of their lethality. PNAS 111:e2100-9
28. Zhang X, Huang Y, Gu A, Wang G, Fang B, Wu H. 2012. Hydrogen peroxide sensor based on carbon nanotubes/β-Ni(OH)2 nanocomposites. Chin. J. Chem. 30:501-6
29. Lippert AR, Keshari KR, Kurhanewicz J, Chang CJ. 2011. A hydrogen peroxide-responsive hyperpolarized 13C MRI contrast agent. J. Am. Chem. Soc. 133:3776-79
30. Olson ES, Orozco J, Wu Z, Malone CD, Yi B, et al. 2013. Toward in vivo detection of hydrogen peroxide with ultrasound molecular imaging. Biomaterials 34:8918-24
31. Cochemé HM, Quin C, McQuaker SJ, Cabreiro F, Logan A, et al. 2011. Measurement of H2O2 within living Drosophila during aging using a ratiometricmass spectrometry probe targeted to themitochondrial matrix. Cell Metab. 13:340-50
32. Lee D, Khaja S, Velasquez-Castano JC, Dasari M, Sun C, et al. 2007. In vivo imaging of hydrogen peroxide with chemiluminescent nanoparticles. Nat. Mater. 6:765-69
33. Van de Bittner GC, Dubikovskaya EA, Bertozzi CR, Chang CJ. 2010. In vivo imaging of hydrogen peroxide production in a murine tumor model with a chemoselective bioluminescent reporter. PNAS 107:21316-21
34. Van de Bittner GC, Bertozzi CR, Chang CJ. 2013. Strategy for dual-analyte luciferin imaging: in vivo bioluminescence detection of hydrogen peroxide and caspase activity in a murine model of acute inflammation. J. Am. Chem. Soc. 135:1783-95
35. Cathcart R, Schwiers E, Ames BN. 1983. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem. 134:111-16
36. Chen X, Zhong Z, Xu Z, Chen L, Wang Y. 2010. 2′, 7′, -Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: forty years of application and controversy. Free Radic. Res. 44:587-604
37. Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP. 1997. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem. 253:162-68
38. Kuivila HG, Wiles RA. 1955. Electrophilic displacement reactions. VII. Catalysis by chelating agents in the reaction between hydrogen peroxide and benzeneboronic acid. J. Am. Chem. Soc. 77:4830-34
39. Kuivila HG, Armour AG. 1957. Electrophilic displacement reactions. IX. Effects of substituents on rates of reactions between hydrogen peroxide and benzeneboronic acid. J. Am. Chem. Soc. 79:5659-62
40. Chang MC, Pralle A, Isacoff EY, Chang CJ. 2004. A selective, cell-permeable optical probe for hydrogen peroxide in living cells. J. Am. Chem. Soc. 126:15392-93
41. Lippert AR, Van de Bittner GC, Chang CJ. 2011. Boronate oxidation as a bioorthogonal reaction approach for studying the chemistry of hydrogen peroxide in living systems. Acc. Chem. Res. 44:793-804
42. Jencks WP, Carriuolo J. 1960. Reactivity of nucleophilic reagents toward esters. J. Am. Chem. Soc. 82:1778-86
43. Dickinson BC, Huynh C, Chang CJ. 2010. A palette of fluorescent probes with varying emission colors for imaging hydrogen peroxide signaling in living cells. J. Am. Chem. Soc. 132:5906-15
44. Sikora A, Zielonka J, Lopez M, Joseph J, Kalyanaraman B. 2009. Direct oxidation of boronates by peroxynitrite: mechanism and implications in fluorescence imaging of peroxynitrite. Free Radic. Biol. Med. 47:1401-7
45. Zielonka J, Sikora A, Hardy M, Joseph J, Dranka BP, Kalyanaraman B. 2012. Boronate probes as diagnostic tools for real time monitoring of peroxynitrite and hydroperoxides. Chem. Res. Toxicol. 25:1793-99
46. Sun X, Xu Q, Kim G, Flower SE, Lowe JP, et al. 2014. A water-soluble boronate-based fluorescent probe for the selective detection of peroxynitrite and imaging in living cells. Chem. Sci. 5:3368-73
47. Charkoudian LK, Pham DM, Franz KJ. 2006. A pro-chelator triggered by hydrogen peroxide inhibits iron-promoted hydroxyl radical formation. J. Am. Chem. Soc. 128:12424-25
48. Wei Y, Guo M. 2007. Hydrogen peroxide triggered prochelator activation, subsequent metal chelation, and attenuation of the Fenton reaction. Angew. Chem. Int. Ed. 46:4722-25
49. Major Jourden JL, Cohen SM. 2010. Hydrogen peroxide activated matrix metalloproteinase inhibitors: a prodrug approach. Angew. Chem. Int. Ed. 49:6795-97
50. Urano Y, Kamiya M, Kanda K, Ueno T, Hirose K, Nagano T. 2005. Evolution of fluorescein as a platform for finely tunable fluorescence probes. J. Am. Chem. Soc. 127:4888-94
51. Miller EW, Tulyathan O, Isacoff EY, Chang CJ. 2007. Molecular imaging of hydrogen peroxide produced for cell signaling. Nat. Chem. Biol. 3:263-67
52. Setsukinai K-I, Urano Y, Kakinuma K, Majima HJ, Nagano T. 2003. Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278:3170-75
53. Tsien RY. 1981. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290:527-28
54. Rojek A, Praetorius J, Frøkiaer J, Nielsen S, Fenton RA. 2008. Acurrent view of themammalian aquaglyceroporins. Annu. Rev. Physiol. 70:301-27
55. Miller EW, Dickinson BC, Chang CJ. 2010. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. PNAS 107:15681-86
56. Kwon J, Lee S-R, Yang K-S, Ahn Y, Kim YJ, et al. 2004. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. PNAS 101:16419-24
57. Peltier J, O'Neill A, Schaffer DV. 2007. PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev. Neurobiol. 67:1348-61
58. Basu S, Rajakaruna S, Dickinson BC, Chang CJ, Menko AS. 2014. Endogenous hydrogen peroxide production in the epithelium of the developing embryonic lens. Mol. Vis. 20:458-67
59. Sakai J, Li J, Subramanian KK, Mondal S, Bajrami B, et al. 2012. Reactive oxygen species-induced actin glutathionylation controls actin dynamics in neutrophils. Immunity 37:1037-49
60. Yang M, Haase AD, Huang F-K, Coulis G, Rivera KD, et al. 2014. Dephosphorylation of tyrosine 393 in argonaute 2 by protein tyrosine phosphatase 1B regulates gene silencing in oncogenic RAS-induced senescence. Mol. Cell 55:782-90
61. Dickinson BC, Chang CJ. 2008. A targetable fluorescent probe for imaging hydrogen peroxide in the mitochondria of living cells. J. Am. Chem. Soc. 130:9638-39
62. Ross MF, Kelso GF, Blaikie FH, James AM, Cochemé HM, et al. 2005. Lipophilic triphenylphosphonium cations as tools in mitochondrial bioenergetics and free radical biology. Biochemistry 70:222-30
63. Ohsaki Y, O'Connor P, Mori T, Ryan RP, Dickinson BC, et al. 2011. Increase of sodium delivery stimulates the mitochondrial respiratory chain H2O2 production in rat renal medullary thick ascending limb. Am. J. Physiol. Ren. Physiol. 302:95-102
64. Dickinson BC, Tang Y, Chang Z, Chang CJ. 2011. A nuclear-localized fluorescent hydrogen peroxide probe for monitoring sirtuin-mediated oxidative stress responses in vivo. Chem. Biol. 18:943-48
65. Juillerat A, Gronemeyer T, Keppler A, Gendreizig S, Pick H, et al. 2003. Directed evolution of O6- alkylguanine-DNA alkyltransferase for efficient labeling of fusion proteins with small molecules in vivo. Chem. Biol. 10:313-17
66. Srikun D, Albers AE, Nam CI, Iavarone AT, Chang CJ. 2010. Organelle-targetable fluorescent probes for imaging hydrogen peroxide in living cells via SNAP-tag protein labeling. J. Am. Chem. Soc. 132:4455-65
67. Lo Conte M, Carroll KS. 2013. The redox biochemistry of protein sulfenylation and sulfinylation. J. Biol. Chem. 288:26480-88
68. Winterbourn CC, Hampton MB. 2008. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45:549-61
69. Salsbury FR Jr, Knutson ST, Poole LB, Fetrow JS. 2008. Functional site profiling and electrostatic analysis of cysteines modifiable to cysteine sulfenic acid. Protein Sci. 17:299-312
70. Carballal S, Alvarez B, Turell L, Botti H, Freeman BA, Radi R. 2007. Sulfenic acid in human serum albumin. Amino Acids 32:543-51
71. Reddie KG, Seo YH, Muse WB III, Leonard SE, Carroll KS. 2008. A chemical approach for detecting sulfenic acid-modified proteins in living cells. Mol. Biosyst. 4:521-31
72. Lee JW, Soonsanga S, Helmann JD. 2007. A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. PNAS 104:8743-48
73. 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
74. vanMontfort RL, Congreve M, Tisi D, Carr R, Jhoti H. 2003. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:773-77
75. Yang J, Groen A, Lemeer S, Jans A, Slijper M, et al. 2007. Reversible oxidation of the membrane distal domain of receptor PTPαis mediated by a cyclic sulfenamide. Biochemistry 46:709-19
76. Hugo M, Turell L, Manta B, Botti H, Monteiro G, et al. 2009. Thiol and sulfenic acid oxidation of AhpE, the one-cysteine peroxiredoxin from Mycobacterium tuberculosis: kinetics, acidity constants, and conformational dynamics. Biochemistry 48:9416-26
77. Sohn J, Rudolph J. 2003. Catalytic and chemical competence of regulation of Cdc25 phosphatase by oxidation/reduction. Biochemistry 42:10060-70
78. Turell L, Botti H, Carballal S, Ferrer-Sueta G, Souza JM, et al. 2008. Reactivity of sulfenic acid in human serum albumin. Biochemistry 47:358-67
79. Berndt C, Lillig CH, Holmgren A. 2007. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 292:1227-36
80. Finkel T. 2011. Signal transduction by reactive oxygen species. J. Cell Biol. 194:7-15
81. Paulsen CE, Carroll KS. 2013. Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem. Rev. 113:4633-79
82. Paulsen CE, Carroll KS. 2010. Orchestrating redox signaling networks through regulatory cysteine switches. Am. Chem. Soc. Chem. Biol. 5:47-62
83. Holmstrom KM, Finkel T. 2014. Cellular mechanisms and physiological consequences of redoxdependent signalling. Nat. Rev. Mol. Cell Biol. 15:411-21
84. Schieber M, Chandel NS. 2014. ROS function in redox signaling and oxidative stress. Curr. Biol. 24:R453-62
85. Marino SM, Li Y, Fomenko DE, Agisheva N, Cerny RL, Gladyshev VN. 2010. Characterization of surface-exposed reactive cysteine residues in Saccharomyces cerevisiae. Biochemistry 49:7709-21
86. Boivin B, Tonks NK. 2010. Analysis of the redox regulation of protein tyrosine phosphatase superfamily members utilizing a cysteinyl-labeling assay. Methods Enzymol. 474:35-50
87. Sethuraman M, McComb ME, Huang H, Huang S, Heibeck T, et al. 2004. Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures. J. Proteome Res. 3:1228-33
88. Sethuraman M, Clavreul N, Huang H, McComb ME, Costello CE, Cohen RA. 2007. Quantification of oxidative posttranslational modifications of cysteine thiols of p21ras associated with redox modulation of activity using isotope-coded affinity tags and mass spectrometry. Free Radic. Biol. Med. 42:823-29
89. Benitez LV, Allison WS. 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. 249:6234-43
90. Poole LB, Zeng BB, Knaggs SA, Yakubu M, King SB. 2005. Synthesis of chemical probes tomap sulfenic acid modifications on proteins. Bioconjug. Chem. 16:1624-28
91. Martinez-Acedo P, Gupta V, Carroll KS. 2014. Proteomic analysis of peptides tagged with dimedone and related probes. J. Mass Spectrom. 49:257-65
92. Leonard SE, Carroll KS. 2011. Chemical 'omics' approaches for understanding protein cysteine oxidation in biology. Curr. Opin. Chem. Biol. 15:88-102
93. Poole LB, Klomsiri C, Knaggs SA, Furdui CM, Nelson KJ, et al. 2007. Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. Bioconjug. Chem. 18:2004-17
94. Charles RL, Schröder E, May G, Free P, Gaffney PR, et al. 2007. Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol. Cell. Proteomics 6:1473-84
95. Oshikawa J, Urao N, Kim HW, Kaplan N, Razvi M, et al. 2010. Extracellular SOD-derived H2O2 promotes VEGF signaling in caveolae/lipid rafts and post-ischemic angiogenesis in mice. PLOS ONE 5:e10189
96. Kaplan N, Urao N, Furuta E, Kim SJ, Razvi M, et al. 2011. Localized cysteine sulfenic acid formation by vascular endothelial growth factor: role in endothelial cell migration and angiogenesis. Free Radic. Res. 45:1124-35
97. Michalek RD, Nelson KJ, Holbrook BC, Yi JS, Stridiron D, et al. 2007. The requirement of reversible cysteine sulfenic acid formation for T cell activation and function. J. Immunol. 179:6456-67
98. Wani R, Qian J, Yin L, Bechtold E, King SB, et al. 2011. Isoform-specific regulation of Akt by PDGFinduced reactive oxygen species. PNAS 108:10550-55
99. Klomsiri C, Rogers LC, Soito L, McCauley AK, King SB, et al. 2014. Endosomal H2O2 production leads to localized cysteine sulfenic acid formation on proteins during lysophosphatidic acid-mediated cell signaling. Free Radic. Biol. Med. 71:49-60
100. Qian J, Klomsiri C, Wright MW, King SB, Tsang AW, et al. 2011. Simple synthesis of 1, 3- cyclopentanedione derived probes for labeling sulfenic acid proteins. Chem. Commun. 47:9203-5
101. Qian J, Wani R, Klomsiri C, Poole LB, Tsang AW, Furdui CM. 2012. A simple and effective strategy for labeling cysteine sulfenic acid in proteins by utilization of β-ketoesters as cleavable probes. Chem. Commun. 48:4091-93
102. Cohen MS, Hadjivassiliou H, Taunton J. 2007. A clickable inhibitor reveals context-dependent autoactivation of p90 RSK. Nat. Chem. Biol. 3:156-60
103. Seo YH, Carroll KS. 2009. Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies. PNAS 106:16163-68
104. Hang HC, Loureiro J, Spooner E, van der Velden AW, Kim YM, et al. 2006. Mechanism-based probe for the analysis of cathepsin cysteine proteases in living cells. Am. Chem. Soc. Chem. Biol. 1:713-23
105. Speers AE, Cravatt BF. 2004. Profiling enzyme activities in vivo using click chemistry methods. Chem. Biol. 11:535-46
106. Go YM, Jones DP. 2008. Redox compartmentalization in eukaryotic cells. Biochim. Biophys. Acta 1780:1273-90
107. Leonard SE, Garcia FJ, Goodsell DS, Carroll KS. 2011. Redox-based probes for protein tyrosine phosphatases. Angew. Chem. 50:4423-27
108. Seo YH, Carroll KS. 2009. Facile synthesis and biological evaluation of a cell-permeable probe to detect redox-regulated proteins. Bioorg. Med. Chem. Lett. 19:356-59
109. Patterson DM, Nazarova LA, Prescher JA. 2014. Finding the right (bioorthogonal) chemistry. Am. Chem. Soc. Chem. Biol. 9:592-605
110. Truong TH, Carroll KS. 2012. Bioorthogonal chemical reporters for analyzing protein sulfenylation in cells. Curr. Protoc. Chem. Biol. 4:101-22
111. Paulsen CE, Carroll KS. 2009. Chemical dissection of an essential redox switch in yeast. Chem. Biol. 16:217-25
112. Depuydt M, Leonard SE, Vertommen D, Denoncin K, Morsomme P, et al. 2009. A periplasmic reducing system protects single cysteine residues from oxidation. Science 326:1109-11
113. Gupta V, Carroll KS. 2014. Sulfenic acid chemistry, detection and cellular lifetime. Biochim. Biophys. Acta 1840:847-75
114. Leonard SE, Reddie KG, Carroll KS. 2009. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. Am. Chem. Soc. Chem. Biol. 4:783-99
115. Charron G, Zhang MM, Yount JS, Wilson J, Raghavan AS, et al. 2009. Robust fluorescent detection of protein fatty-acylation with chemical reporters. J. Am. Chem. Soc. 131:4967-75
116. Paulsen CE, Truong TH, Garcia FJ, Homann A, Gupta V, et al. 2012. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat. Chem. Biol. 8:57-64
117. Maller C, Schröder E, Eaton P. 2011. Glyceraldehyde 3-phosphate dehydrogenase is unlikely tomediate hydrogen peroxide signaling: studies with a novel anti-dimedone sulfenic acid antibody. Antioxid. Redox Signal. 14:49-60
118. Seo YH, Carroll KS. 2011. Quantification of protein sulfenic acid modifications using isotope-coded dimedone and iododimedone. Angew. Chem. 50:1342-45
119. Truong TH, Garcia FJ, Seo YH, Carroll KS. 2011. Isotope-coded chemical reporter and acid-cleavable affinity reagents for monitoring protein sulfenic acids. Bioorg. Med. Chem. Lett. 21:5015-20
120. Zhu X, Tanaka F, Lerner RA, Barbas CF 3rd, Wilson IA. 2009. Direct observation of an enamine intermediate in amine catalysis. J. Am. Chem. Soc. 131:18206-7
121. Yang J, Gupta V, Carroll KS, Liebler DC. 2014. Site-specific mapping and quantification of protein S-sulphenylation in cells. Nat. Commun. 5:4776
122. Tanner JJ, Parsons ZD, Cummings AH, Zhou H, Gates KS. 2011. Redox regulation of protein tyrosine phosphatases: structural and chemical aspects. Antioxid. Redox Signal. 15:77-97
123. Karisch R, Neel BG. 2013. Methods to monitor classical protein tyrosine phosphatase oxidation. FEBS J. 280:459-75
124. Garcia FJ, Carroll KS. 2014. Redox-based probes as tools to monitor oxidized protein tyrosine phosphatases in living cells. Eur. J. Med. Chem. 88:28-33
125. Persson C, Sjöblom T, Groen A, Kappert K, Engström U, et al. 2004. Preferential oxidation of the second phosphatase domain of receptor-like PTP-α revealed by an antibody against oxidized protein tyrosine phosphatases. PNAS 101:1886-91
126. Karisch R, Fernandez M, Taylor P, Virtanen C, St-Germain JR, et al. 2011. Global proteomic assessment of the classical protein tyrosine phosphatome and "redoxome". Cell 146:826-40
127. Haque A, Andersen JN, Salmeen A, Barford D, Tonks NK. 2011. Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147:185-98
128. Truong TH, Carroll KS. 2012. Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 51:9954-65
129. Truong TH, Carroll KS. 2013. Redox regulation of protein kinases. Crit. Rev. Biochem.Mol. Biol. 48:332-56
130. Schwartz PA, Kuzmic P, Solowiej J, Bergqvist S, Bolanos B, et al. 2014. Covalent EGFR inhibitor analysis reveals importance of reversible interactions to potency and mechanisms of drug resistance. PNAS 111:173-78
131. 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
132. 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
133. Fuangthong M, Helmann JD. 2002. The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. PNAS 99:6690-95
134. Griffiths SW, King J, Cooney CL. 2002. The reactivity and oxidation pathway of cysteine 232 in recombinant human α1-antitrypsin. J. Biol. Chem. 277:25486-92
135. Poole TH, Reisz JA, Zhao W, Poole LB, Furdui CM, King SB. 2014. Strained cycloalkynes as new protein sulfenic acid traps. J. Am. Chem. Soc. 136:6167-70
136. van Geel R, Pruijn GJ, van Delft FL, Boelens WC. 2012. Preventing thiol-yne addition improves the specificity of strain-promoted azide-alkyne cycloaddition. Bioconjug. Chem. 23:392-98
137. Beatty KE, Fisk JD, Smart BP, Lu YY, Szychowski J, et al. 2010. Live-cell imaging of cellular proteins by a strain-promoted azide-alkyne cycloaddition. ChemBioChem 11:2092-95
138. Lo Conte M, Staderini S, Marra A, Sanchez-Navarro M, Davis BG, Dondoni A. 2011. Multi-molecule reaction of serum albumin can occur through thiol-yne coupling. Chem. Commun. 47:11086-88
139. Kim EJ, Kang DW, Leucke HF, Bond MR, Ghosh S, et al. 2013. Optimizing the selectivity of DIFObased reagents for intracellular bioorthogonal applications. Carbohydr. Res. 377:18-27
140. Liu CT, Benkovic SJ. 2013. Capturing a sulfenic acid with arylboronic acids and benzoxaborole. J. Am. Chem. Soc. 135:14544-47
141. Jonsson TJ, Johnson LC, Lowther WT. 2008. Structure of the sulphiredoxin-peroxiredoxin complex reveals an essential repair embrace. Nature 451:98-101
142. Murakami T, Nojiri M, Nakayama H, Odaka M, Yohda M, et al. 2000. Post-translational modification is essential for catalytic activity of nitrile hydratase. Protein Sci. 9:1024-30
143. Fu X, Kassim SY, Parks WC, Heinecke JW. 2001. Hypochlorous acid oxygenates the cysteine switch domain of pro-matrilysin (MMP-7).Amechanism formatrixmetalloproteinase activation and atherosclerotic plaque rupture by myeloperoxidase. J. Biol. Chem. 276:41279-87
144. Blackinton J, Lakshminarasimhan M, Thomas KJ, Ahmad R, Greggio E, et al. 2009. Formation of a stabilized cysteine sulfinic acid is critical for the mitochondrial function of the parkinsonism protein DJ-1. J. Biol. Chem. 284:6476-85
145. Witze ES, Old WM, Resing KA, Ahn NG. 2007. Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 4:798-806
146. Woo HA, Kang SW, Kim HK, Yang KS, Chae HZ, Rhee SG. 2003. Reversible oxidation of the active site cysteine of peroxiredoxins to cysteine sulfinic acid. Immunoblot detection with antibodies specific for the hyperoxidized cysteine-containing sequence. J. Biol. Chem. 278:47361-64
147. Hamann M, Zhang T, Hendrich S, Thomas JA. 2002. Quantitation of protein sulfinic and sulfonic acid, irreversibly oxidized protein cysteine sites in cellular proteins. Methods Enzymol. 348:146-56
148. Lo Conte M, Carroll KS. 2012. Chemoselective ligation of sulfinic acids with aryl-nitroso compounds. Angew. Chem. 51:6502-5
149. Fujiwara N, Nakano M, Kato S, Yoshihara D, Ookawara T, et al. 2007. Oxidativemodification to cysteine sulfonic acid of Cys111 in human copper-zinc superoxide dismutase. J. Biol. Chem. 282:35933-44
150. Tasaki T, Kwon YT. 2007. The mammalian N-end rule pathway: new insights into its components and physiological roles. Trends Biochem. Sci. 32:520-28
151. Lim JC, Choi HI, Park YS, Nam HW, Woo HA, et al. 2008. Irreversible oxidation of the active-site cysteine of peroxiredoxin to cysteine sulfonic acid for enhanced molecular chaperone activity. J. Biol. Chem. 283:28873-80
152. Chang YC, Huang CN, Lin CH, Chang HC, Wu CC. 2010. Mapping protein cysteine sulfonic acid modifications with specific enrichment and mass spectrometry: an integrated approach to explore the cysteine oxidation. Proteomics 10:2961-71