1932

Abstract

Hydrogen peroxide (HO) is a prime member of the reactive oxygen species (ROS) family of molecules produced during normal cell function and in response to various stimuli, but if left unchecked, it can inflict oxidative damage on all types of biological macromolecules and lead to cell death. In this context, a major source of HO for redox signaling purposes is the NADPH oxidase (Nox) family of enzymes, which were classically studied for their roles in phagocytic immune response but have now been found to exist in virtually all mammalian cell types in various isoforms with distinct tissue and subcellular localizations. Downstream of this tightly regulated ROS generation, site-specific, reversible covalent modification of proteins, particularly oxidation of cysteine thiols to sulfenic acids, represents a prominent posttranslational modification akin to phosphorylation as an emerging molecular mechanism for transforming an oxidant signal into a dynamic biological response. We review two complementary types of chemical tools that enable () specific detection of HO generated at its sources and () mapping of sulfenic acid posttranslational modification targets that mediate its signaling functions, which can be used to study this important chemical signal in biological systems.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-060614-034018
2015-06-02
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/biochem/84/1/annurev-biochem-060614-034018.html?itemId=/content/journals/10.1146/annurev-biochem-060614-034018&mimeType=html&fmt=ahah

Literature Cited

  1. Thénard LJ. 1.  1818. Observations sur des combinaisons nouvelles entre l'oxigène et divers acides. Ann. Chim. Phys. 8:306–13 [Google Scholar]
  2. Loew O. 2.  1900. A new enzyme of general occurrence in organisms. Science 11:701–2 [Google Scholar]
  3. Chance B, Oshino N. 3.  1971. Kinetics and mechanisms of catalase in peroxisomes of the mitochondrial fraction. Biochem. J. 122:225–33 [Google Scholar]
  4. Chance B, Sies H, Boveris A. 4.  1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:527–605 [Google Scholar]
  5. Babior BM, Kipnes RS, Curnutte JT. 5.  1973. Biological defense mechanisms—production by leukocytes of superoxide, a potential bactericidal agent. J. Clin. Investig. 52:741–44 [Google Scholar]
  6. Rossi F, Zatti M. 6.  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 [Google Scholar]
  7. Radeke HH, Meier B, Topley N, Flöge J, Habermehl GG, Resch K. 7.  1990. Interleukin 1α and tumor necrosis factor α induce oxygen radical production in mesangial cells. Kidney Int. 37:767–75 [Google Scholar]
  8. Sundaresan M, Yu Z-X, Ferrans VJ, Irani K, Finkel T. 8.  1995. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270:296–99 [Google Scholar]
  9. Suh Y-A, Arnold RS, Lassegue B, Shi J, Xu X. 9.  et al. 1999. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401:79–82 [Google Scholar]
  10. Bedard K, Krause K-H. 10.  2007. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:245–313 [Google Scholar]
  11. O'Neill JS, Reddy AB. 11.  2011. Circadian clocks in human red blood cells. Nature 469:498–503 [Google Scholar]
  12. O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F. 12.  et al. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–58 [Google Scholar]
  13. Kim J-S, Huang TY, Bokoch GM. 13.  2009. Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol. Biol. Cell 20:2650–60 [Google Scholar]
  14. Gianni D, Taulet N, DerMardirossian C, Bokoch GM. 14.  2010. c-Src-mediated phosphorylation of NoxA1 and Tks4 induces the reactive oxygen species (ROS)–dependent formation of functional invadopodia in human colon cancer cells. Mol. Biol. Cell 21:4287–98 [Google Scholar]
  15. Niethammer P, Grabher C, Look AT, Mitchison TJ. 15.  2009. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:996–99 [Google Scholar]
  16. Dickinson BC, Peltier J, Stone D, Schaffer DV, Chang CJ. 16.  2011. Nox2 redox signaling maintains essential cell populations in the brain. Nat. Chem. Biol. 7:106–12 [Google Scholar]
  17. D'Autreaux B, Toledano MB. 17.  2007. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8:813–24 [Google Scholar]
  18. Stone JR, Yang S. 18.  2006. Hydrogen peroxide: a signaling messenger. Antioxid. Redox Signal. 8:243–70 [Google Scholar]
  19. Wood ZA, Poole LB, Karplus PA. 19.  2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650–53 [Google Scholar]
  20. Araki K, Inaba K. 20.  2012. Structure, mechanism, and evolution of Ero1 family enzymes. Antioxid. Redox Signal. 16:790–99 [Google Scholar]
  21. Dawkes HC, Phillips SEV. 21.  2001. Copper amine oxidase: cunning cofactor and controversial copper. Curr. Opin. Struct. Biol. 11:666–73 [Google Scholar]
  22. Kim J-JP, Miura R. 22.  2004. Acyl-CoA dehydrogenases and acyl-CoA oxidases. Eur. J. Biochem. 271:483–93 [Google Scholar]
  23. Halliwell B, Gutteridge JMC. 23.  1999. Free Radicals in Biology and Medicine Oxford, UK: Oxford Univ. Press [Google Scholar]
  24. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS. 24.  et al. 2006. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3:281–86 [Google Scholar]
  25. Markvicheva KN, Bilan DS, Mishina NM, Gorokhovatsky AY, Vinokurov LM. 25.  et al. 2011. A genetically encoded sensor for H2O2 with expanded dynamic range. Bioorg. Med. Chem. 19:1079–84 [Google Scholar]
  26. Bilan DS, Pase L, Joosen L, Gorokhovatsky AY, Ermakova YG. 26.  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 [Google Scholar]
  27. Dwyer DJ, Belenky PA, Yang JH, MacDonald IC, Martell JD. 27.  et al. 2014. Antiobiotics induce redox-related physiological alterations as part of their lethality. PNAS 111:e2100–9 [Google Scholar]
  28. Zhang X, Huang Y, Gu A, Wang G, Fang B, Wu H. 28.  2012. Hydrogen peroxide sensor based on carbon nanotubes/β-Ni(OH)2 nanocomposites. Chin. J. Chem. 30:501–6 [Google Scholar]
  29. Lippert AR, Keshari KR, Kurhanewicz J, Chang CJ. 29.  2011. A hydrogen peroxide–responsive hyperpolarized 13C MRI contrast agent. J. Am. Chem. Soc. 133:3776–79 [Google Scholar]
  30. Olson ES, Orozco J, Wu Z, Malone CD, Yi B. 30.  et al. 2013. Toward in vivo detection of hydrogen peroxide with ultrasound molecular imaging. Biomaterials 34:8918–24 [Google Scholar]
  31. Cochemé HM, Quin C, McQuaker SJ, Cabreiro F, Logan A. 31.  et al. 2011. Measurement of H2O2 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrix. Cell Metab. 13:340–50 [Google Scholar]
  32. Lee D, Khaja S, Velasquez-Castano JC, Dasari M, Sun C. 32.  et al. 2007. In vivo imaging of hydrogen peroxide with chemiluminescent nanoparticles. Nat. Mater. 6:765–69 [Google Scholar]
  33. Van de Bittner GC, Dubikovskaya EA, Bertozzi CR, Chang CJ. 33.  2010. In vivo imaging of hydrogen peroxide production in a murine tumor model with a chemoselective bioluminescent reporter. PNAS 107:21316–21 [Google Scholar]
  34. Van de Bittner GC, Bertozzi CR, Chang CJ. 34.  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 [Google Scholar]
  35. Cathcart R, Schwiers E, Ames BN. 35.  1983. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem. 134:111–16 [Google Scholar]
  36. Chen X, Zhong Z, Xu Z, Chen L, Wang Y. 36.  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 [Google Scholar]
  37. Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP. 37.  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 [Google Scholar]
  38. Kuivila HG, Wiles RA. 38.  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 [Google Scholar]
  39. Kuivila HG, Armour AG. 39.  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 [Google Scholar]
  40. Chang MC, Pralle A, Isacoff EY, Chang CJ. 40.  2004. A selective, cell-permeable optical probe for hydrogen peroxide in living cells. J. Am. Chem. Soc. 126:15392–93 [Google Scholar]
  41. Lippert AR, Van de Bittner GC, Chang CJ. 41.  2011. Boronate oxidation as a bioorthogonal reaction approach for studying the chemistry of hydrogen peroxide in living systems. Acc. Chem. Res. 44:793–804 [Google Scholar]
  42. Jencks WP, Carriuolo J. 42.  1960. Reactivity of nucleophilic reagents toward esters. J. Am. Chem. Soc. 82:1778–86 [Google Scholar]
  43. Dickinson BC, Huynh C, Chang CJ. 43.  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 [Google Scholar]
  44. Sikora A, Zielonka J, Lopez M, Joseph J, Kalyanaraman B. 44.  2009. Direct oxidation of boronates by peroxynitrite: mechanism and implications in fluorescence imaging of peroxynitrite. Free Radic. Biol. Med. 47:1401–7 [Google Scholar]
  45. Zielonka J, Sikora A, Hardy M, Joseph J, Dranka BP, Kalyanaraman B. 45.  2012. Boronate probes as diagnostic tools for real time monitoring of peroxynitrite and hydroperoxides. Chem. Res. Toxicol. 25:1793–99 [Google Scholar]
  46. Sun X, Xu Q, Kim G, Flower SE, Lowe JP. 46.  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 [Google Scholar]
  47. Charkoudian LK, Pham DM, Franz KJ. 47.  2006. A pro-chelator triggered by hydrogen peroxide inhibits iron-promoted hydroxyl radical formation. J. Am. Chem. Soc. 128:12424–25 [Google Scholar]
  48. Wei Y, Guo M. 48.  2007. Hydrogen peroxide triggered prochelator activation, subsequent metal chelation, and attenuation of the Fenton reaction. Angew. Chem. Int. Ed. 46:4722–25 [Google Scholar]
  49. Major Jourden JL, Cohen SM. 49.  2010. Hydrogen peroxide activated matrix metalloproteinase inhibitors: a prodrug approach. Angew. Chem. Int. Ed. 49:6795–97 [Google Scholar]
  50. Urano Y, Kamiya M, Kanda K, Ueno T, Hirose K, Nagano T. 50.  2005. Evolution of fluorescein as a platform for finely tunable fluorescence probes. J. Am. Chem. Soc. 127:4888–94 [Google Scholar]
  51. Miller EW, Tulyathan O, Isacoff EY, Chang CJ. 51.  2007. Molecular imaging of hydrogen peroxide produced for cell signaling. Nat. Chem. Biol. 3:263–67 [Google Scholar]
  52. Setsukinai K-I, Urano Y, Kakinuma K, Majima HJ, Nagano T. 52.  2003. Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278:3170–75 [Google Scholar]
  53. Tsien RY. 53.  1981. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290:527–28 [Google Scholar]
  54. Rojek A, Praetorius J, Frøkiaer J, Nielsen S, Fenton RA. 54.  2008. A current view of the mammalian aquaglyceroporins. Annu. Rev. Physiol. 70:301–27 [Google Scholar]
  55. Miller EW, Dickinson BC, Chang CJ. 55.  2010. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. PNAS 107:15681–86 [Google Scholar]
  56. Kwon J, Lee S-R, Yang K-S, Ahn Y, Kim YJ. 56.  et al. 2004. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. PNAS 101:16419–24 [Google Scholar]
  57. Peltier J, O'Neill A, Schaffer DV. 57.  2007. PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev. Neurobiol. 67:1348–61 [Google Scholar]
  58. Basu S, Rajakaruna S, Dickinson BC, Chang CJ, Menko AS. 58.  2014. Endogenous hydrogen peroxide production in the epithelium of the developing embryonic lens. Mol. Vis. 20:458–67 [Google Scholar]
  59. Sakai J, Li J, Subramanian KK, Mondal S, Bajrami B. 59.  et al. 2012. Reactive oxygen species–induced actin glutathionylation controls actin dynamics in neutrophils. Immunity 37:1037–49 [Google Scholar]
  60. Yang M, Haase AD, Huang F-K, Coulis G, Rivera KD. 60.  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 [Google Scholar]
  61. Dickinson BC, Chang CJ. 61.  2008. A targetable fluorescent probe for imaging hydrogen peroxide in the mitochondria of living cells. J. Am. Chem. Soc. 130:9638–39 [Google Scholar]
  62. Ross MF, Kelso GF, Blaikie FH, James AM, Cochemé HM. 62.  et al. 2005. Lipophilic triphenylphosphonium cations as tools in mitochondrial bioenergetics and free radical biology. Biochemistry 70:222–30 [Google Scholar]
  63. Ohsaki Y, O'Connor P, Mori T, Ryan RP, Dickinson BC. 63.  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 [Google Scholar]
  64. Dickinson BC, Tang Y, Chang Z, Chang CJ. 64.  2011. A nuclear-localized fluorescent hydrogen peroxide probe for monitoring sirtuin-mediated oxidative stress responses in vivo. Chem. Biol. 18:943–48 [Google Scholar]
  65. Juillerat A, Gronemeyer T, Keppler A, Gendreizig S, Pick H. 65.  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 [Google Scholar]
  66. Srikun D, Albers AE, Nam CI, Iavarone AT, Chang CJ. 66.  2010. Organelle-targetable fluorescent probes for imaging hydrogen peroxide in living cells via SNAP-tag protein labeling. J. Am. Chem. Soc. 132:4455–65 [Google Scholar]
  67. Lo Conte M, Carroll KS. 67.  2013. The redox biochemistry of protein sulfenylation and sulfinylation. J. Biol. Chem. 288:26480–88 [Google Scholar]
  68. Winterbourn CC, Hampton MB. 68.  2008. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45:549–61 [Google Scholar]
  69. Salsbury FR Jr, Knutson ST, Poole LB, Fetrow JS. 69.  2008. Functional site profiling and electrostatic analysis of cysteines modifiable to cysteine sulfenic acid. Protein Sci. 17:299–312 [Google Scholar]
  70. Carballal S, Alvarez B, Turell L, Botti H, Freeman BA, Radi R. 70.  2007. Sulfenic acid in human serum albumin. Amino Acids 32:543–51 [Google Scholar]
  71. Reddie KG, Seo YH, Muse WB III, Leonard SE, Carroll KS. 71.  2008. A chemical approach for detecting sulfenic acid–modified proteins in living cells. Mol. Biosyst. 4:521–31 [Google Scholar]
  72. Lee JW, Soonsanga S, Helmann JD. 72.  2007. A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. PNAS 104:8743–48 [Google Scholar]
  73. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA. 73.  et al. 2003. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423:769–73 [Google Scholar]
  74. van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H. 74.  2003. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:773–77 [Google Scholar]
  75. Yang J, Groen A, Lemeer S, Jans A, Slijper M. 75.  et al. 2007. Reversible oxidation of the membrane distal domain of receptor PTPα is mediated by a cyclic sulfenamide. Biochemistry 46:709–19 [Google Scholar]
  76. Hugo M, Turell L, Manta B, Botti H, Monteiro G. 76.  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 [Google Scholar]
  77. Sohn J, Rudolph J. 77.  2003. Catalytic and chemical competence of regulation of Cdc25 phosphatase by oxidation/reduction. Biochemistry 42:10060–70 [Google Scholar]
  78. Turell L, Botti H, Carballal S, Ferrer-Sueta G, Souza JM. 78.  et al. 2008. Reactivity of sulfenic acid in human serum albumin. Biochemistry 47:358–67 [Google Scholar]
  79. Berndt C, Lillig CH, Holmgren A. 79.  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 [Google Scholar]
  80. Finkel T. 80.  2011. Signal transduction by reactive oxygen species. J. Cell Biol. 194:7–15 [Google Scholar]
  81. Paulsen CE, Carroll KS. 81.  2013. Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem. Rev. 113:4633–79 [Google Scholar]
  82. Paulsen CE, Carroll KS. 82.  2010. Orchestrating redox signaling networks through regulatory cysteine switches. Am. Chem. Soc. Chem. Biol. 5:47–62 [Google Scholar]
  83. Holmstrom KM, Finkel T. 83.  2014. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 15:411–21 [Google Scholar]
  84. Schieber M, Chandel NS. 84.  2014. ROS function in redox signaling and oxidative stress. Curr. Biol. 24:R453–62 [Google Scholar]
  85. Marino SM, Li Y, Fomenko DE, Agisheva N, Cerny RL, Gladyshev VN. 85.  2010. Characterization of surface-exposed reactive cysteine residues in Saccharomyces cerevisiae. Biochemistry 49:7709–21 [Google Scholar]
  86. Boivin B, Tonks NK. 86.  2010. Analysis of the redox regulation of protein tyrosine phosphatase superfamily members utilizing a cysteinyl-labeling assay. Methods Enzymol. 474:35–50 [Google Scholar]
  87. Sethuraman M, McComb ME, Huang H, Huang S, Heibeck T. 87.  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 [Google Scholar]
  88. Sethuraman M, Clavreul N, Huang H, McComb ME, Costello CE, Cohen RA. 88.  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 [Google Scholar]
  89. Benitez LV, Allison WS. 89.  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 [Google Scholar]
  90. Poole LB, Zeng BB, Knaggs SA, Yakubu M, King SB. 90.  2005. Synthesis of chemical probes to map sulfenic acid modifications on proteins. Bioconjug. Chem. 16:1624–28 [Google Scholar]
  91. Martinez-Acedo P, Gupta V, Carroll KS. 91.  2014. Proteomic analysis of peptides tagged with dimedone and related probes. J. Mass Spectrom. 49:257–65 [Google Scholar]
  92. Leonard SE, Carroll KS. 92.  2011. Chemical ‘omics’ approaches for understanding protein cysteine oxidation in biology. Curr. Opin. Chem. Biol. 15:88–102 [Google Scholar]
  93. Poole LB, Klomsiri C, Knaggs SA, Furdui CM, Nelson KJ. 93.  et al. 2007. Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. Bioconjug. Chem. 18:2004–17 [Google Scholar]
  94. Charles RL, Schröder E, May G, Free P, Gaffney PR. 94.  et al. 2007. Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol. Cell. Proteomics 6:1473–84 [Google Scholar]
  95. Oshikawa J, Urao N, Kim HW, Kaplan N, Razvi M. 95.  et al. 2010. Extracellular SOD-derived H2O2 promotes VEGF signaling in caveolae/lipid rafts and post-ischemic angiogenesis in mice. PLOS ONE 5:e10189 [Google Scholar]
  96. Kaplan N, Urao N, Furuta E, Kim SJ, Razvi M. 96.  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 [Google Scholar]
  97. Michalek RD, Nelson KJ, Holbrook BC, Yi JS, Stridiron D. 97.  et al. 2007. The requirement of reversible cysteine sulfenic acid formation for T cell activation and function. J. Immunol. 179:6456–67 [Google Scholar]
  98. Wani R, Qian J, Yin L, Bechtold E, King SB. 98.  et al. 2011. Isoform-specific regulation of Akt by PDGF-induced reactive oxygen species. PNAS 108:10550–55 [Google Scholar]
  99. Klomsiri C, Rogers LC, Soito L, McCauley AK, King SB. 99.  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 [Google Scholar]
  100. Qian J, Klomsiri C, Wright MW, King SB, Tsang AW. 100.  et al. 2011. Simple synthesis of 1,3-cyclopentanedione derived probes for labeling sulfenic acid proteins. Chem. Commun. 47:9203–5 [Google Scholar]
  101. Qian J, Wani R, Klomsiri C, Poole LB, Tsang AW, Furdui CM. 101.  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 [Google Scholar]
  102. Cohen MS, Hadjivassiliou H, Taunton J. 102.  2007. A clickable inhibitor reveals context-dependent autoactivation of p90 RSK. Nat. Chem. Biol. 3:156–60 [Google Scholar]
  103. Seo YH, Carroll KS. 103.  2009. Profiling protein thiol oxidation in tumor cells using sulfenic acid–specific antibodies. PNAS 106:16163–68 [Google Scholar]
  104. Hang HC, Loureiro J, Spooner E, van der Velden AW, Kim YM. 104.  et al. 2006. Mechanism-based probe for the analysis of cathepsin cysteine proteases in living cells. Am. Chem. Soc. Chem. Biol. 1:713–23 [Google Scholar]
  105. Speers AE, Cravatt BF. 105.  2004. Profiling enzyme activities in vivo using click chemistry methods. Chem. Biol. 11:535–46 [Google Scholar]
  106. Go YM, Jones DP. 106.  2008. Redox compartmentalization in eukaryotic cells. Biochim. Biophys. Acta 1780:1273–90 [Google Scholar]
  107. Leonard SE, Garcia FJ, Goodsell DS, Carroll KS. 107.  2011. Redox-based probes for protein tyrosine phosphatases. Angew. Chem. 50:4423–27 [Google Scholar]
  108. Seo YH, Carroll KS. 108.  2009. Facile synthesis and biological evaluation of a cell-permeable probe to detect redox-regulated proteins. Bioorg. Med. Chem. Lett. 19:356–59 [Google Scholar]
  109. Patterson DM, Nazarova LA, Prescher JA. 109.  2014. Finding the right (bioorthogonal) chemistry. Am. Chem. Soc. Chem. Biol. 9:592–605 [Google Scholar]
  110. Truong TH, Carroll KS. 110.  2012. Bioorthogonal chemical reporters for analyzing protein sulfenylation in cells. Curr. Protoc. Chem. Biol. 4:101–22 [Google Scholar]
  111. Paulsen CE, Carroll KS. 111.  2009. Chemical dissection of an essential redox switch in yeast. Chem. Biol. 16:217–25 [Google Scholar]
  112. Depuydt M, Leonard SE, Vertommen D, Denoncin K, Morsomme P. 112.  et al. 2009. A periplasmic reducing system protects single cysteine residues from oxidation. Science 326:1109–11 [Google Scholar]
  113. Gupta V, Carroll KS. 113.  2014. Sulfenic acid chemistry, detection and cellular lifetime. Biochim. Biophys. Acta 1840:847–75 [Google Scholar]
  114. Leonard SE, Reddie KG, Carroll KS. 114.  2009. Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. Am. Chem. Soc. Chem. Biol. 4:783–99 [Google Scholar]
  115. Charron G, Zhang MM, Yount JS, Wilson J, Raghavan AS. 115.  et al. 2009. Robust fluorescent detection of protein fatty-acylation with chemical reporters. J. Am. Chem. Soc. 131:4967–75 [Google Scholar]
  116. Paulsen CE, Truong TH, Garcia FJ, Homann A, Gupta V. 116.  et al. 2012. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat. Chem. Biol. 8:57–64 [Google Scholar]
  117. Maller C, Schröder E, Eaton P. 117.  2011. Glyceraldehyde 3-phosphate dehydrogenase is unlikely to mediate hydrogen peroxide signaling: studies with a novel anti-dimedone sulfenic acid antibody. Antioxid. Redox Signal. 14:49–60 [Google Scholar]
  118. Seo YH, Carroll KS. 118.  2011. Quantification of protein sulfenic acid modifications using isotope-coded dimedone and iododimedone. Angew. Chem. 50:1342–45 [Google Scholar]
  119. Truong TH, Garcia FJ, Seo YH, Carroll KS. 119.  2011. Isotope-coded chemical reporter and acid-cleavable affinity reagents for monitoring protein sulfenic acids. Bioorg. Med. Chem. Lett. 21:5015–20 [Google Scholar]
  120. Zhu X, Tanaka F, Lerner RA, Barbas CF 3rd, Wilson IA. 120.  2009. Direct observation of an enamine intermediate in amine catalysis. J. Am. Chem. Soc. 131:18206–7 [Google Scholar]
  121. Yang J, Gupta V, Carroll KS, Liebler DC. 121.  2014. Site-specific mapping and quantification of protein S-sulphenylation in cells. Nat. Commun. 5:4776 [Google Scholar]
  122. Tanner JJ, Parsons ZD, Cummings AH, Zhou H, Gates KS. 122.  2011. Redox regulation of protein tyrosine phosphatases: structural and chemical aspects. Antioxid. Redox Signal. 15:77–97 [Google Scholar]
  123. Karisch R, Neel BG. 123.  2013. Methods to monitor classical protein tyrosine phosphatase oxidation. FEBS J. 280:459–75 [Google Scholar]
  124. Garcia FJ, Carroll KS. 124.  2014. Redox-based probes as tools to monitor oxidized protein tyrosine phosphatases in living cells. Eur. J. Med. Chem. 88:28–33 [Google Scholar]
  125. Persson C, Sjöblom T, Groen A, Kappert K, Engström U. 125.  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 [Google Scholar]
  126. Karisch R, Fernandez M, Taylor P, Virtanen C, St-Germain JR. 126.  et al. 2011. Global proteomic assessment of the classical protein tyrosine phosphatome and “redoxome”. Cell 146:826–40 [Google Scholar]
  127. Haque A, Andersen JN, Salmeen A, Barford D, Tonks NK. 127.  2011. Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147:185–98 [Google Scholar]
  128. Truong TH, Carroll KS. 128.  2012. Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 51:9954–65 [Google Scholar]
  129. Truong TH, Carroll KS. 129.  2013. Redox regulation of protein kinases. Crit. Rev. Biochem. Mol. Biol. 48:332–56 [Google Scholar]
  130. Schwartz PA, Kuzmic P, Solowiej J, Bergqvist S, Bolanos B. 130.  et al. 2014. Covalent EGFR inhibitor analysis reveals importance of reversible interactions to potency and mechanisms of drug resistance. PNAS 111:173–78 [Google Scholar]
  131. Ellis HR, Poole LB. 131.  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 [Google Scholar]
  132. Denu JM, Tanner KG. 132.  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 [Google Scholar]
  133. Fuangthong M, Helmann JD. 133.  2002. The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine–sulfenic acid derivative. PNAS 99:6690–95 [Google Scholar]
  134. Griffiths SW, King J, Cooney CL. 134.  2002. The reactivity and oxidation pathway of cysteine 232 in recombinant human α1-antitrypsin. J. Biol. Chem. 277:25486–92 [Google Scholar]
  135. Poole TH, Reisz JA, Zhao W, Poole LB, Furdui CM, King SB. 135.  2014. Strained cycloalkynes as new protein sulfenic acid traps. J. Am. Chem. Soc. 136:6167–70 [Google Scholar]
  136. van Geel R, Pruijn GJ, van Delft FL, Boelens WC. 136.  2012. Preventing thiol–yne addition improves the specificity of strain-promoted azide–alkyne cycloaddition. Bioconjug. Chem. 23:392–98 [Google Scholar]
  137. Beatty KE, Fisk JD, Smart BP, Lu YY, Szychowski J. 137.  et al. 2010. Live-cell imaging of cellular proteins by a strain-promoted azide–alkyne cycloaddition. ChemBioChem 11:2092–95 [Google Scholar]
  138. Lo Conte M, Staderini S, Marra A, Sanchez-Navarro M, Davis BG, Dondoni A. 138.  2011. Multi-molecule reaction of serum albumin can occur through thiol–yne coupling. Chem. Commun. 47:11086–88 [Google Scholar]
  139. Kim EJ, Kang DW, Leucke HF, Bond MR, Ghosh S. 139.  et al. 2013. Optimizing the selectivity of DIFO-based reagents for intracellular bioorthogonal applications. Carbohydr. Res. 377:18–27 [Google Scholar]
  140. Liu CT, Benkovic SJ. 140.  2013. Capturing a sulfenic acid with arylboronic acids and benzoxaborole. J. Am. Chem. Soc. 135:14544–47 [Google Scholar]
  141. Jonsson TJ, Johnson LC, Lowther WT. 141.  2008. Structure of the sulphiredoxin–peroxiredoxin complex reveals an essential repair embrace. Nature 451:98–101 [Google Scholar]
  142. Murakami T, Nojiri M, Nakayama H, Odaka M, Yohda M. 142.  et al. 2000. Post-translational modification is essential for catalytic activity of nitrile hydratase. Protein Sci. 9:1024–30 [Google Scholar]
  143. Fu X, Kassim SY, Parks WC, Heinecke JW. 143.  2001. Hypochlorous acid oxygenates the cysteine switch domain of pro-matrilysin (MMP-7). A mechanism for matrix metalloproteinase activation and atherosclerotic plaque rupture by myeloperoxidase. J. Biol. Chem. 276:41279–87 [Google Scholar]
  144. Blackinton J, Lakshminarasimhan M, Thomas KJ, Ahmad R, Greggio E. 144.  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 [Google Scholar]
  145. Witze ES, Old WM, Resing KA, Ahn NG. 145.  2007. Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 4:798–806 [Google Scholar]
  146. Woo HA, Kang SW, Kim HK, Yang KS, Chae HZ, Rhee SG. 146.  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 [Google Scholar]
  147. Hamann M, Zhang T, Hendrich S, Thomas JA. 147.  2002. Quantitation of protein sulfinic and sulfonic acid, irreversibly oxidized protein cysteine sites in cellular proteins. Methods Enzymol. 348:146–56 [Google Scholar]
  148. Lo Conte M, Carroll KS. 148.  2012. Chemoselective ligation of sulfinic acids with aryl-nitroso compounds. Angew. Chem. 51:6502–5 [Google Scholar]
  149. Fujiwara N, Nakano M, Kato S, Yoshihara D, Ookawara T. 149.  et al. 2007. Oxidative modification to cysteine sulfonic acid of Cys111 in human copper–zinc superoxide dismutase. J. Biol. Chem. 282:35933–44 [Google Scholar]
  150. Tasaki T, Kwon YT. 150.  2007. The mammalian N-end rule pathway: new insights into its components and physiological roles. Trends Biochem. Sci. 32:520–28 [Google Scholar]
  151. Lim JC, Choi HI, Park YS, Nam HW, Woo HA. 151.  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 [Google Scholar]
  152. Chang YC, Huang CN, Lin CH, Chang HC, Wu CC. 152.  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 [Google Scholar]
/content/journals/10.1146/annurev-biochem-060614-034018
Loading
/content/journals/10.1146/annurev-biochem-060614-034018
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error