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Published Online: 20 August 2018

Biological Production, Detection, and Fate of Hydrogen Peroxide

Publication: Antioxidants & Redox Signaling
Volume 29, Issue Number 6

Abstract

Significance: Hydrogen peroxide (H2O2) is generated in numerous biological processes. It transmits cellular signals, contributes to oxidative folding of exported proteins, and, in excess, can be damaging to cells and tissues. Although a strong oxidant, high activation energy barriers make it unreactive with most biological molecules. Its main reactions are with transition metal centers, selenoproteins and selected thiol proteins, with glutathione peroxidases (GPxs) and peroxiredoxins (Prxs) being major targets. It reacts slowly with most thiol proteins, and how they become oxidized during redox signal transmission is not well understood.
Recent Advances: Kinetic analysis indicates that Prxs and GPxs are overwhelmingly favored as targets for H2O2 in cells. Studies with localized probes indicate that H2O2 can be produced in cellular microdomains and be consumed by highly reactive targets before it can diffuse to other parts of the cell. Inactivation of these targets alone will not confine it to its site of production. Kinetic data indicate that oxidation of regulatory thiol proteins by H2O2 requires a facilitated mechanism such as directed transfer from source to target or a relay mediated through a highly reactive sensor.
Critical Issues and Future Directions: Absolute rates of H2O2 production and steady-state concentrations in cells still need to be characterized. More information on cellular sites of production and action is required, and specific mechanisms of oxidation of regulatory proteins during redox signaling require further characterization. Antioxid. Redox Signal. 29, 541–551.

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References

1.
Adam FI, Bounds PL, Kissner R, and Koppenol WH. Redox properties and activity of iron-citrate complexes: evidence for redox cycling. Chem Res Toxicol 28: 604–614, 2015.
2.
Antunes F and Brito PM. Quantitative biology of hydrogen peroxide signaling. Redox Biol 13: 1–7, 2017.
3.
Antunes F and Cadenas E. Estimation of H2O2 gradients across biomembranes. FEBS Lett 475: 121–126, 2000.
4.
Appenzeller-Herzog C, Banhegyi G, Bogeski I, Davies KJ, Delaunay-Moisan A, Forman HJ, Gorlach A, Kietzmann T, Laurindo F, Margittai E, Meyer AJ, Riemer J, Rutzler M, Simmen T, Sitia R, Toledano MB, and Touw IP. Transit of H2O2 across the endoplasmic reticulum membrane is not sluggish. Free Radic Biol Med 94: 157–160, 2016.
5.
Appenzeller-Herzog C, Riemer J, Zito E, Chin KT, Ron D, Spiess M, and Ellgaard L. Disulphide production by Ero1alpha-PDI relay is rapid and effectively regulated. EMBO J 29: 3318–3329, 2010.
6.
Bakhmutova-Albert EV, Yao H, Denevan DE, and Richardson DE. Kinetics and mechanism of peroxymonocarbonate formation. Inorg Chem 49: 11287–11296, 2010.
7.
Bersweiler A, D'Autreaux B, Mazon H, Kriznik A, Belli G, Delaunay-Moisan A, Toledano MB, and Rahuel-Clermont S. A scaffold protein that chaperones a cysteine-sulfenic acid in H2O2 signaling. Nat Chem Biol 13: 909–915, 2017.
8.
Bertolotti M, Farinelli G, Galli M, Aiuti A, and Sitia R. AQP8 transports NOX2-generated H2O2 across the plasma membrane to promote signaling in B cells. J Leukoc Biol 100: 1071–1079, 2016.
9.
Bertolotti M, Yim SH, Garcia-Manteiga JM, Masciarelli S, Kim YJ, Kang MH, Iuchi Y, Fujii J, Vene R, Rubartelli A, Rhee SG, and Sitia R. B- to plasma-cell terminal differentiation entails oxidative stress and profound reshaping of the antioxidant responses. Antioxid Redox Signal 13: 1133–1144, 2010.
10.
Bienert GP and Chaumont F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 1840: 1596–1604, 2014.
11.
Bilan DS and Belousov VV. HyPer family probes: state of the art. Antioxid Redox Signal 24: 731–751, 2016.
12.
Bilan DS and Belousov VV. New tools for redox biology: from imaging to manipulation. Free Radic Biol Med 109: 167–188, 2017.
13.
Bogdanova YA, Schultz C, and Belousov VV. Local generation and imaging of hydrogen peroxide in living cells. Curr Protoc Chem Biol 9: 117–127, 2017.
14.
Bonekamp NA, Volkl A, Fahimi HD, and Schrader M. Reactive oxygen species and peroxisomes: struggling for balance. Biofactors 35: 346–355, 2009.
15.
Bonini MG, Rota C, Tomasi A, and Mason RP. The oxidation of 2′,7′-dichlorofluorescin to reactive oxygen species: a self-fulfilling prophesy? Free Radic Biol Med 40: 968–975, 2006.
16.
Carballal S, Radi R, Kirk MC, Barnes S, Freeman BA, and Alvarez B. Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite. Biochemistry 42: 9906–9914, 2003.
17.
Chen K, Kirber MT, Xiao H, Yang Y, and Keaney JF Jr. Regulation of ROS signal transduction by NADPH oxidase 4 localization. J Cell Biol 181: 1129–1139, 2008.
18.
Chevion M. A site-specific mechanism for free radical induced biological damage: the essential role of redox-active transition metals. Free Radic Biol Med 5: 27–37, 1988.
19.
Chung C, Srikun D, Lim CS, Chang CJ, and Cho BR. A two-photon fluorescent probe for ratiometric imaging of hydrogen peroxide in live tissue. Chem Commun 47: 9618–9620, 2011.
20.
Cocheme HM, Quin C, McQuaker SJ, Cabreiro F, Logan A, Prime TA, Abakumova I, Patel JV, Fearnley IM, James AM, Porteous CM, Smith RA, Saeed S, Carre JE, Singer M, Gems D, Hartley RC, Partridge L, and Murphy MP. Measurement of H2O2 within living Drosophila during aging using a ratiometric mass spectrometry probe targeted to the mitochondrial matrix. Cell Metab 13: 340–350, 2011.
21.
Cox AG, Pearson AG, Pullar JM, Jonsson TJ, Lowther WT, Winterbourn C, and Hampton MB. Mitochondrial peroxiredoxin 3 is more resilient to hyperoxidation than cytoplasmic peroxiredoxins. Biochem J 421: 51–58, 2009.
22.
Davies MJ, Hawkins CL, Pattison DI, and Rees MD. Mammalian heme peroxidases: from molecular mechanisms to health implications. Antioxid Redox Signal 10: 1199–1234, 2008.
23.
del Rio LA, Sandalio LM, Corpas FJ, Palma JM, and Barroso JB. Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141: 330–335, 2006.
24.
Delaunay A, Pflieger D, Barrault MB, Vinh J, and Toledano MB. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111: 471–481, 2002.
25.
Dikalov SI and Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal 20: 372–382, 2012.
26.
Fass D and Thorpe C. Chemistry and enzymology of disulfide cross-linking in proteins. Chem Rev 118: 1169–1198, 2018.
27.
Ferrer-Sueta G, Manta B, Botti H, Radi R, Trujillo M, and Denicola A. Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem Res Toxicol 24: 438–450, 2011.
28.
Flohe L, Toppo S, Cozza G, and Ursini F. A comparison of thiol peroxidase mechanisms. Antioxid Redox Signal 15: 763–780, 2011.
29.
Forman HJ and Azzi A. On the virtual existence of superoxide anions in mitochondria: thoughts regarding its role in pathophysiology. FASEB J 11: 374–375, 1997.
30.
Forman HJ, Maiorino M, and Ursini F. Signaling functions of reactive oxygen species. Biochemistry 49: 835–842, 2010.
31.
Ganini D, Leinisch F, Kumar A, Jiang J, Tokar EJ, Malone CC, Petrovich RM, and Mason RP. Fluorescent proteins such as eGFP lead to catalytic oxidative stress in cells. Redox Biol 12: 462–468, 2017.
32.
Goldstein S, Meyerstein D, and Czapski G. The Fenton reagents. Free Radic Biol Med 15: 435–445, 1993.
33.
Gonzalez-Flecha B and Demple B. Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli. J Bacteriol 179: 382–388, 1997.
34.
Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, Kaiser CA, Thorpe C, and Fass D. Generating disulfides enzymatically: reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc Natl Acad Sci U S A 103: 299–304, 2006.
35.
Hall A, Parsonage D, Poole LB, and Karplus PA. Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization. J Mol Biol 402: 194–209, 2010.
36.
Hansen HG, Schmidt JD, Soltoft CL, Ramming T, Geertz-Hansen HM, Christensen B, Sorensen ES, Juncker AS, Appenzeller-Herzog C, and Ellgaard L. Hyperactivity of the Ero1alpha oxidase elicits endoplasmic reticulum stress but no broad antioxidant response. J Biol Chem 287: 39513–39523, 2012.
37.
Haque A, Andersen JN, Salmeen A, Barford D, and Tonks NK. Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147: 185–198, 2011.
38.
Hara-Chikuma M, Chikuma S, Sugiyama Y, Kabashima K, Verkman AS, Inoue S, and Miyachi Y. Chemokine-dependent T cell migration requires aquaporin-3-mediated hydrogen peroxide uptake. J Exp Med 209: 1743–1752, 2012.
39.
Hara-Chikuma M, Satooka H, Watanabe S, Honda T, Miyachi Y, Watanabe T, and Verkman AS. Aquaporin-3-mediated hydrogen peroxide transport is required for NF-kappaB signalling in keratinocytes and development of psoriasis. Nat Commun 6: 7454, 2015.
40.
Hara-Chikuma M, Watanabe S, and Satooka H. Involvement of aquaporin-3 in epidermal growth factor receptor signaling via hydrogen peroxide transport in cancer cells. Biochem Biophys Res Commun 471: 603–609, 2016.
41.
Hider RC and Kong X. Iron speciation in the cytosol: an overview. Dalton Trans 42: 3220–3229, 2013.
42.
Huang BK, Stein KT, and Sikes HD. Modulating and measuring intracellular H2O2 using genetically encoded tools to study its toxicity to human cells. ACS Synth Biol 5: 1389–1395, 2016.
43.
Hugo M, Turell L, Manta B, Botti H, Monteiro G, Netto LE, Alvarez B, Radi R, and Trujillo M. Thiol and sulfenic acid oxidation of AhpE, the one-cysteine peroxiredoxin from Mycobacterium tuberculosis: kinetics, acidity constants, and conformational dynamics. Biochemistry 48: 9416–9426, 2009.
44.
Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol 57: 395–418, 2003.
45.
Imlay JA. Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755–776, 2008.
46.
Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11: 443–454, 2013.
47.
Jarvis RM, Hughes SM, and Ledgerwood EC. Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic Biol Med 53: 1522–1530, 2012.
48.
Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA, Osipov AN, Belikova NA, Kapralov AA, Kini V, Vlasova II, Zhao Q, Zou M, Di P, Svistunenko DA, Kurnikov IV, and Borisenko GG. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1: 223–232, 2005.
49.
Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ, 2nd, and Ischiropoulos H. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52: 1–6, 2012.
50.
Karplus PA. A primer on peroxiredoxin biochemistry. Free Radic Biol Med 80: 183–190, 2015.
51.
Kettle AJ, Carr AC, and Winterbourn CC. Assays using horseradish peroxidase and phenolic substrates require superoxide dismutase for accurate determination of hydrogen peroxide production by neutrophils. Free Radic Biol Med 17: 161–164, 1994.
52.
Kettle AJ and Winterbourn CC. Myeloperoxidase: structure and function of the green heme enzyme of neutrophils. In: Heme Peroxidases, edited by Raven EL and Dunford HB. Cambridge, United Kingdom: Royal Society of Chemistry, 2016, pp. 272–308.
53.
Lambeth JD and Neish AS. Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu Rev Pathol 9: 119–145, 2014.
54.
Lee C, Lee SM, Mukhopadhyay P, Kim SJ, Lee SC, Ahn WS, Yu MH, Storz G, and Ryu SE. Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 11: 1179–1185, 2004.
55.
Leto TL, Morand S, Hurt D, and Ueyama T. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid Redox Signal 11: 2607–2619, 2009.
56.
Lippert AR, Van de Bittner GC, and Chang CJ. Boronate oxidation as a bioorthogonal reaction approach for studying the chemistry of hydrogen peroxide in living systems. Acc Chem Res 44: 793–804, 2011.
57.
Malinouski M, Zhou Y, Belousov VV, Hatfield DL, and Gladyshev VN. Hydrogen peroxide probes directed to different cellular compartments. PLoS One 6: e14564, 2011.
58.
Manta B, Hugo M, Ortiz C, Ferrer-Sueta G, Trujillo M, and Denicola A. The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2. Arch Biochem Biophys 484: 146–154, 2009.
59.
Marinho HS, Real C, Cyrne L, Soares H, and Antunes F. Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol 2: 535–562, 2014.
60.
Masciarelli S and Sitia R. Building and operating an antibody factory: redox control during B to plasma cell terminal differentiation. Biochim Biophys Acta 1783: 578–588, 2008.
61.
Matlashov ME, Belousov VV, and Enikolopov G. How much H2O2 is produced by recombinant D-amino acid oxidase in mammalian cells? Antioxid Redox Signal 20: 1039–1044, 2014.
62.
Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, and Hell R. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52: 973–986, 2007.
63.
Meyer AJ and Dick TP. Fluorescent protein-based redox probes. Antioxid Redox Signal 13: 621–650, 2010.
64.
Miller EW, Albers AE, Pralle A, Isacoff EY, and Chang CJ. Boronate-based fluorescent probes for imaging cellular hydrogen peroxide. J Am Chem Soc 127: 16652–16659, 2005.
65.
Miller EW, Dickinson BC, and Chang CJ. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci U S A 107: 15681–15686, 2010.
66.
Mishin V, Gray JP, Heck DE, Laskin DL, and Laskin JD. Application of the Amplex red/horseradish peroxidase assay to measure hydrogen peroxide generation by recombinant microsomal enzymes. Free Radic Biol Med 48: 1485–1491, 2010.
67.
Mishina NM, Markvicheva KN, Fradkov AF, Zagaynova EV, Schultz C, Lukyanov S, and Belousov VV. Imaging H2O2 microdomains in receptor tyrosine kinases signaling. Methods Enzymol 526: 175–187, 2013.
68.
Mishina NM, Mishin AS, Belyaev Y, Bogdanova EA, Lukyanov S, Schultz C, and Belousov VV. Live-cell STED microscopy with genetically encoded biosensor. Nano Lett 15: 2928–2932, 2015.
69.
Mishina NM, Tyurin-Kuzmin PA, Markvicheva KN, Vorotnikov AV, Tkachuk VA, Laketa V, Schultz C, Lukyanov S, and Belousov VV. Does cellular hydrogen peroxide diffuse or act locally? Antioxid Redox Signal 14: 1–7, 2011.
70.
Molin M, Yang J, Hanzen S, Toledano MB, Labarre J, and Nystrom T. Life span extension and H2O2 resistance elicited by caloric restriction require the peroxiredoxin Tsa1 in Saccharomyces cerevisiae. Mol Cell 43: 823–833, 2011.
71.
Morgan B, Van Laer K, Owusu TN, Ezerina D, Pastor-Flores D, Amponsah PS, Tursch A, and Dick TP. Real-time monitoring of basal H2O2 levels with peroxiredoxin-based probes. Nat Chem Biol 12: 437–443, 2016.
72.
Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1–13, 2009.
73.
Nagy P and 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 129: 14082–14091, 2007.
74.
Nagy P, Karton A, Betz A, Peskin AV, Pace P, O'Reilly RJ, Hampton MB, Radom L, and Winterbourn CC. Model for the exceptional reactivity of peroxiredoxins 2 and 3 with hydrogen peroxide: a kinetic and computational study. J Biol Chem 286: 18048–18055, 2011.
75.
Nagy P and Winterbourn CC. Redox chemistry of biological thiols. In: Advances in Molecular Toxicology, edited by Fishbein JC. New York, NY: Elsevier, 2010, pp. 183–222.
76.
Oshino N, Chance B, Sies H, and Bucher T. The role of H2O2 generation in perfused rat liver and the reaction of catalase compound I and hydrogen donors. Arch Biochem Biophys 154: 117–131, 1973.
77.
Parsonage D, Nelson KJ, Ferrer-Sueta G, Alley S, Karplus PA, Furdui CM, and Poole LB. Dissecting peroxiredoxin catalysis: separating binding, peroxidation, and resolution for a bacterial AhpC. Biochemistry 54: 1567–1575, 2015.
78.
Peskin AV, Dickerhof N, Poynton RA, Paton LN, Pace PE, Hampton MB, and Winterbourn CC. Hyperoxidation of peroxiredoxins 2 and 3: rate constants for the reactions of the sulfenic acid of the peroxidative cysteine. J Biol Chem 288: 14170–14177, 2013.
79.
Peskin AV, Low FM, Paton LN, Maghzal GJ, Hampton MB, and Winterbourn CC. The high reactivity of peroxiredoxin 2 with H2O2 is not reflected in its reaction with other oxidants and thiol reagents. J Biol Chem 282: 11885–11892, 2007.
80.
Peskin AV, Pace PE, Behring JB, Paton LN, Soethoudt M, Bachschmid MM, and Winterbourn CC. Glutathionylation of the active site cysteines of peroxiredoxin 2 and recycling by glutaredoxin. J Biol Chem 291: 3053–3062, 2016.
81.
Ramming T, Hansen HG, Nagata K, Ellgaard L, and Appenzeller-Herzog C. GPx8 peroxidase prevents leakage of H2O2 from the endoplasmic reticulum. Free Radic Biol Med 70: 106–116, 2014.
82.
Rhee SG, Bae YS, Lee SR, and Kwon J. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE 2000: PE1, 2000.
83.
Rhee SG and Kil IS. Multiple functions and regulation of mammalian peroxiredoxins. Annu Rev Biochem 86: 749–775, 2017.
84.
Rhee SG, Woo HA, and Kang D. The role of peroxiredoxins in the transduction of H2O2 signals. Antioxid Redox Signal 28: 537–557, 2018.
85.
Richardson DE, Regino CA, Yao H, and Johnson JV. Methionine oxidation by peroxymonocarbonate, a reactive oxygen species formed from CO2/bicarbonate and hydrogen peroxide. Free Radic Biol Med 35: 1538–1550, 2003.
86.
Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, and Barford D. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423: 769–773, 2003.
87.
Santos CX, Hafstad AD, Beretta M, Zhang M, Molenaar C, Kopec J, Fotinou D, Murray TV, Cobb AM, Martin D, Zeh Silva M, Anilkumar N, Schroder K, Shanahan CM, Brewer AC, Brandes RP, Blanc E, Parsons M, Belousov V, Cammack R, Hider RC, Steiner RA, and Shah AM. Targeted redox inhibition of protein phosphatase 1 by Nox4 regulates eIF2alpha-mediated stress signaling. EMBO J 35: 319–334, 2016.
88.
Schrader M and Fahimi HD. Peroxisomes and oxidative stress. Biochim Biophys Acta 1763: 1755–1766, 2006.
89.
Schwarzlander M, Dick TP, Meyer AJ, and Morgan B. Dissecting redox biology using fluorescent protein sensors. Antioxid Redox Signal 24: 680–712, 2016.
90.
Seaver LC and Imlay JA. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183: 7173–7181, 2001.
91.
Seaver LC and Imlay JA. Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J Biol Chem 279: 48742–48750, 2004.
92.
Sies H. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox Biol 11: 613–619, 2017.
93.
Sies H and Chance B. The steady state level of catalase compound I in isolated hemoglobin-free perfused rat liver. FEBS Lett 11: 172–176, 1970.
94.
Sobotta MC, Liou W, Stocker S, Talwar D, Oehler M, Ruppert T, Scharf AN, and Dick TP. Peroxiredoxin-2 and STAT3 form a redox relay for H2O2 signaling. Nat Chem Biol 11: 64–70, 2015.
95.
Srikun D, Miller EW, Domaille DW, and Chang CJ. An ICT-based approach to ratiometric fluorescence imaging of hydrogen peroxide produced in living cells. J Am Chem Soc 130: 4596–4597, 2008.
96.
Stadtman ER. Metal ion catalysed oxidation of proteins: biochemical mechanism and biological consequences. Free Radic Biol Med 9: 315–325, 1990.
97.
Stocker S, Van Laer K, Mijuskovic A, and Dick TP. The conundrum of hydrogen peroxide signaling and the emerging role of peroxiredoxins as redox relay hubs. Antioxid Redox Signal 28: 558–573, 2018.
98.
Sutton HC and Winterbourn CC. On the participation of higher oxidation states of iron and copper in Fenton-type reactions. Free Radic Biol Med 6: 53–60, 1989.
99.
Tavender TJ and Bulleid NJ. Molecular mechanisms regulating oxidative activity of the Ero1 family in the endoplasmic reticulum. Antioxid Redox Signal 13: 1177–1187, 2010.
100.
Tavender TJ, Sheppard AM, and Bulleid NJ. Peroxiredoxin IV is an endoplasmic reticulum-localized enzyme forming oligomeric complexes in human cells. Biochem J 411: 191–199, 2008.
101.
Tavender TJ, Springate JJ, and Bulleid NJ. Recycling of peroxiredoxin IV provides a novel pathway for disulphide formation in the endoplasmic reticulum. EMBO J 29: 4185–4197, 2010.
102.
Thiagarajah JR, Chang J, Goettel JA, Verkman AS, and Lencer WI. Aquaporin-3 mediates hydrogen peroxide-dependent responses to environmental stress in colonic epithelia. Proc Natl Acad Sci U S A 114: 568–573, 2017.
103.
Tonks NK. Redox redux: revisiting PTPs and the control of cell signaling. Cell 121: 667–670, 2005.
104.
Toppo S, Flohe L, Ursini F, Vanin S, and Maiorino M. Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme. Biochim Biophys Acta 1790: 1486–1500, 2009.
105.
Trindade DF, Cerchiaro G, and Augusto O. A role for peroxymonocarbonate in the stimulation of biothiol peroxidation by the bicarbonate/carbon dioxide pair. Chem Res Toxicol 19: 1475–1482, 2006.
106.
Trujillo M, Clippe A, Manta B, Ferrer-Sueta G, Smeets A, Declercq JP, Knoops B, and Radi R. Pre-steady state kinetic characterization of human peroxiredoxin 5: taking advantage of Trp84 fluorescence increase upon oxidation. Arch Biochem Biophys 467: 95–106, 2007.
107.
Trujillo M, Ferrer-Sueta G, and Radi R. Kinetic studies on peroxynitrite reduction by peroxiredoxins. Methods Enzymol 441: 173–196, 2008.
108.
Truong TH and Carroll KS. Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 51: 9954–9965, 2012.
109.
Tu BP and Weissman JS. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164: 341–346, 2004.
110.
Vasquez-Vivar J, Denicola A, Radi R, and Augusto O. Peroxynitrite-mediated decarboxylation of pyruvate to both carbon dioxide and carbon dioxide radical anion. Chem Res Toxicol 10: 786–794, 1997.
111.
Veal EA, Day AM, and Morgan BA. Hydrogen peroxide sensing and signaling. Mol Cell 26: 1–14, 2007.
112.
Veal EA, Findlay VJ, Day AM, Bozonet SM, Evans JM, Quinn J, and Morgan BA. A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol Cell 15: 129–139, 2004.
113.
Votyakova TV and Reynolds IJ. Detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation. Arch Biochem Biophys 431: 138–144, 2004.
114.
Walling C. Fenton's reagent revisited. Acc Chem Res 8: 125–131, 1975.
115.
Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med 43: 995–1022, 2007.
116.
Weller J, Kizina KM, Can K, Bao G, and Muller M. Response properties of the genetically encoded optical H2O2 sensor HyPer. Free Radic Biol Med 76: 227–241, 2014.
117.
Winterbourn CC. Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicol Lett 82–83: 969–974, 1995.
118.
Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4: 278–286, 2008.
119.
Winterbourn CC. Biological chemistry of reactive oxygen species. In: Encyclopedia of Radicals in Chemistry, Biology and Materials, edited by Chatgilialoglu C and Studer A. Chichester, United Kingdom: Wiley, 2012, pp. 1259–1282.
120.
Winterbourn CC. The biological chemistry of hydrogen peroxide. Methods Enzymol 528: 3–25, 2013.
121.
Winterbourn CC. The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Biochim Biophys Acta 1840: 730–738, 2014.
122.
Winterbourn CC, French JK, and Claridge RF. Superoxide dismutase as an inhibitor of reactions of semiquinone radicals. FEBS Lett 94: 269–272, 1978.
123.
Winterbourn CC and Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45: 549–561, 2008.
124.
Winterbourn CC, Kettle AJ, and Hampton MB. Reactive oxygen species and neutrophil function. Annu Rev Biochem 85: 765–792, 2016.
125.
Winterbourn CC and Metodiewa D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27: 322–328, 1999.
126.
Wood ZA, Poole LB, and Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650–653, 2003.
127.
Wrona M and Wardman P. Properties of the radical intermediate obtained on oxidation of 2′,7′-dichlorodihydrofluorescein, a probe for oxidative stress. Free Radic Biol Med 41: 657–667, 2006.
128.
Yu Z, Persson HL, Eaton JW, and Brunk UT. Intralysosomal iron: a major determinant of oxidant-induced cell death. Free Radic Biol Med 34: 1243–1252, 2003.
129.
Zielonka J, Sikora A, Hardy M, Joseph J, Dranka BP, and Kalyanaraman B. Boronate probes as diagnostic tools for real time monitoring of peroxynitrite and hydroperoxides. Chem Res Toxicol 25: 1793–1799, 2012.

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cover image Antioxidants & Redox Signaling
Antioxidants & Redox Signaling
Volume 29Issue Number 6August 20, 2018
Pages: 541 - 551
PubMed: 29113458

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Published in print: August 20, 2018
Published online: 20 August 2018
Published ahead of print: 14 December 2017
Published ahead of production: 7 November 2017
Accepted: 4 November 2017
Received: 25 October 2017

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Christine C. Winterbourn
Department of Pathology, Centre for Free Radical Research, University of Otago Christchurch, Christchurch, New Zealand.

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Address correspondence to:Prof. Christine C. WinterbournDepartment of PathologyCentre for Free Radical ResearchUniversity of Otago ChristchurchP.O. Box 4345Christchurch 8140New Zealand
E-mail: [email protected]

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