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Oxidative Stress and Redox Regulation pp 59–84Cite as

Redox Homeostasis

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Abstract

Multiple factors, including small sulfur-containing molecules and oxidoreductases, are involved in the control of intracellular redox homeostasis. In this chapter, we first review properties and functions of the small sulfur-containing molecules glutathione, mycothiol, bacillithiol and trypanothione. These low molecular weight thiols, which cycle between a reduced and oxidized form, are present at high intracellular concentrations and function as redox buffers to protect cells against oxidative stress conditions. In the second part of this chapter, we focus on the two oxidoreductases, thioredoxin and glutaredoxin. These enzymes are key players in pathways aimed to reduce disulfide bonds in intracellular proteins and to maintain cellular redox homeostasis. We review the general properties of these enzymes and highlight their significant diversity. Finally, we discuss the recent discovery that monothiol glutaredoxins coordinate an iron sulfur cluster, which suggests a novel link between redox and iron homeostasis.

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References

  • Aldea M, Hernandez-Chico C, de la Campa AG, Kushner SR, Vicente M (1988) Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli. J Bacteriol 170:5169–5176

    CAS  PubMed Central  PubMed  Google Scholar 

  • Antelmann H, Helmann JD (2011) Thiol-based redox switches and gene regulation. Antioxid Redox Signal 14:1049–1063

    CAS  PubMed  Google Scholar 

  • Arner ES (1999) Superoxide production by dinitrophenyl-derivatized thioredoxin reductase–a model for the mechanism and correlation to immunostimulation by dinitrohalobenzenes. Biofactors 10:219–226

    CAS  PubMed  Google Scholar 

  • Arner ESJ, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109

    CAS  PubMed  Google Scholar 

  • Aslund F, Zheng M, Beckwith J, Storz G (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc Natl Acad Sci USA 96: 6161–6165

    CAS  PubMed  Google Scholar 

  • Awad S, Henderson GB, Cerami A, Held KD (1992) Effects of trypanothione on the biological activity of irradiated transforming DNA. Int J Radiat Biol 62:401–407

    CAS  PubMed  Google Scholar 

  • Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100:370–375

    CAS  PubMed  Google Scholar 

  • Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schurmann P, Droux M, Buchanan BB (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101:2642–2647

    CAS  PubMed  Google Scholar 

  • Bandyopadhyay S, Gama F, Molina-Navarro MM, Gualberto JM, Claxton R, Naik SG, Huynh BH, Herrero E, Jacquot JP, Johnson MK, Rouhier N (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27:1122–1133

    CAS  PubMed  Google Scholar 

  • Benhar M, Forrester MT, Hess DT, Stamler JS (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050–1054

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bzymek KP, Newton GL, Ta P, Fahey RC (2007) Mycothiol import by Mycobacterium smegmatis and function as a resource for metabolic precursors and energy production. J Bacteriol 189:6796–6805

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carnieri EG, Moreno SN, Docampo R (1993) Trypanothione-dependent peroxide metabolism in Trypanosoma cruzi different stages. Mol Biochem Parasitol 61:79–86

    CAS  PubMed  Google Scholar 

  • Casagrande S, Bonetto V, Fratelli M, Gianazza E, Eberini I, Massignan T, Salmona M, Chang G, Holmgren A, Ghezzi P (2002) Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc Natl Acad Sci USA 99:9745–9749

    CAS  PubMed  Google Scholar 

  • Castro H, Tomas AM (2008) Peroxidases of trypanosomatids. Antioxid Redox Signal 10: 1593–1606

    CAS  PubMed  Google Scholar 

  • Chakravarthi S, Jessop CE, Bulleid NJ (2006) The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep 7:271–275

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng NH, Liu JZ, Brock A, Nelson RS, Hirschi KD (2006) AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. J Biol Chem 281:26280–26288

    CAS  PubMed  Google Scholar 

  • Cheng Z, Arscott LD, Ballou DP, Williams CH (2007) The relationship of the redox potentials of thioredoxin and thioredoxin reductase from Drosophila melanogaster to the enzymatic mechanism: reduced thioredoxin is the reductant of glutathione in Drosophila. Biochemistry 46:7875–7885

    CAS  PubMed  Google Scholar 

  • Cheng NH, Liu JZ, Liu X, Wu Q, Thompson SM, Lin J, Chang J, Whitham SA, Park S, Cohen JD, Hirschi KD (2011) Arabidopsis monothiol glutaredoxin, AtGRXS17, is critical for temperature-dependent postembryonic growth and development via modulating auxin response. J Biol Chem 286:20398–20406

    CAS  PubMed  Google Scholar 

  • Chi BK, Gronau K, Mader U, Hessling B, Becher D, Antelmann H (2011) S-bacillithiolation protects against hypochlorite stress in Bacillus subtilis as revealed by transcriptomics and redox proteomics. Mol Cell Proteomics 10(11):M111.009506. doi: 10.1074/mcp.M111

    PubMed  Google Scholar 

  • Chibani K, Wingsle G, Jacquot JP, Gelhaye E, Rouhier N (2009) Comparative genomic study of the thioredoxin family in photosynthetic organisms with emphasis on Populus trichocarpa. Mol Plant 2:308–322

    CAS  PubMed  Google Scholar 

  • Collet JF, Messens J (2010) Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 13:1205–1216

    CAS  PubMed  Google Scholar 

  • Collet JF, D’Souza JC, Jakob U, Bardwell JC (2003) Thioredoxin 2, an oxidative stress-induced protein, contains a high affinity zinc binding site. J Biol Chem 278:45325–45332

    CAS  PubMed  Google Scholar 

  • Couturier J, Jacquot JP, Rouhier N (2009) Evolution and diversity of glutaredoxins in photosynthetic organisms. Cell Mol Life Sci 66:2539–2557

    CAS  PubMed  Google Scholar 

  • Couturier J, Stroher E, Albetel AN, Roret T, Muthuramalingam M, Tarrago L, Seidel T, Tsan P, Jacquot JP, Johnson MK, Dietz KJ, Didierjean C, Rouhier N (2011) Arabidopsis chloroplastic glutaredoxin C5 as a model to explore molecular determinants for iron-sulfur cluster binding into glutaredoxins. J Biol Chem 286:27515–27527

    CAS  PubMed  Google Scholar 

  • Dalle-Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, Rossi R (2008) Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid Redox Signal 10:445–473

    CAS  PubMed  Google Scholar 

  • Depuydt M, Leonard SE, Vertommen D, Denoncin K, Morsomme P, Wahni K, Messens J, Carroll K, Collet JF (2009) A periplasmic reducing system protects single cysteine residues from oxidation. Science 326:1109–1111

    CAS  PubMed  Google Scholar 

  • Depuydt M, Messens J, Collet JF (2011) How proteins form disulfide bonds. Antioxid Redox Signal 15:49–66

    CAS  PubMed  Google Scholar 

  • Dillet V, Dyson HJ, Bashford D (1998) Calculations of electrostatic interactions and pKas in the active site of Escherichia coli thioredoxin. Biochemistry 37:10298–10306

    CAS  PubMed  Google Scholar 

  • Dominici S, Valentini M, Maellaro E, del Bello B, Paolicchi A, Lorenzini E, Tongiani R, Comporti M, Pompella A (1999) Redox modulation of cell surface protein thiols in U937 lymphoma cells: the role of gamma-glutamyl transpeptidase-dependent H2O2 production and S-thiolation. Free Radic Biol Med 27:623–635

    CAS  PubMed  Google Scholar 

  • Dormeyer M, Reckenfelderbaumer N, Ludemann H, Krauth-Siegel RL (2001) Trypanothione-dependent synthesis of deoxyribonucleotides by Trypanosoma brucei ribonucleotide reductase. J Biol Chem 276:10602–10606

    CAS  PubMed  Google Scholar 

  • Dyson HJ, Tennant LL, Holmgren A (1991) Proton-transfer effects in the active-site region of Escherichia coli thioredoxin using two-dimensional 1H NMR. Biochemistry 30:4262–4268

    CAS  PubMed  Google Scholar 

  • Eklund H, Cambillau C, Sjoberg BM, Holmgren A, Jornvall H, Hoog JO, Branden CI (1984) Conformational and functional similarities between glutaredoxin and thioredoxins. EMBO J 3:1443–1449

    CAS  PubMed  Google Scholar 

  • El Hajjaji H, Dumoulin M, Matagne A, Colau D, Roos G, Messens J, Collet JF (2009) The zinc center influences the redox and thermodynamic properties of Escherichia coli thioredoxin 2. J Mol Biol 386:60–71

    CAS  PubMed  Google Scholar 

  • Fahey RC, Brown WC, Adams WB, Worsham MB (1978) Occurrence of glutathione in bacteria. J Bacteriol 133:1126–1129

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fairlamb AH, Cerami A (1992) Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 46:695–729

    CAS  PubMed  Google Scholar 

  • Fairlamb AH, Blackburn P, Ulrich P, Chait BT, Cerami A (1985) Trypanothione: a novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science 227:1485–1487

    CAS  PubMed  Google Scholar 

  • Feng J, Che Y, Milse J, Yin YJ, Liu L, Ruckert C, Shen XH, Qi SW, Kalinowski J, Liu SJ (2006) The gene ncgl2918 encodes a novel maleylpyruvate isomerase that needs mycothiol as cofactor and links mycothiol biosynthesis and gentisate assimilation in Corynebacterium glutamicum. J Biol Chem 281:10778–10785

    CAS  PubMed  Google Scholar 

  • Fernandes AP, Holmgren A (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 6:63–74

    CAS  PubMed  Google Scholar 

  • Filser M, Comini MA, Molina-Navarro MM, Dirdjaja N, Herrero E, Krauth-Siegel RL (2008) Cloning, functional analysis, and mitochondrial localization of Trypanosoma brucei monothiol glutaredoxin-1. Biol Chem 389:21–32

    CAS  PubMed  Google Scholar 

  • Flohe L, Hecht HJ, Steinert P (1999) Glutathione and trypanothione in parasitic hydroperoxide metabolism. Free Radic Biol Med 27:966–984

    CAS  PubMed  Google Scholar 

  • Ford E, Hughes MN, Wardman P (2002) Kinetics of the reactions of nitrogen dioxide with glutathione, cysteine, and uric acid at physiological pH. Free Radic Biol Med 32:1314–1323

    CAS  PubMed  Google Scholar 

  • Forman HJ, Maiorino M, Ursini F (2010) Signaling functions of reactive oxygen species. Biochemistry 49:835–842

    CAS  PubMed  Google Scholar 

  • Fuangthong M, Helmann JD (2002) The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc Natl Acad Sci USA 99: 6690–6695

    CAS  PubMed  Google Scholar 

  • Gaballa A, Newton GL, Antelmann H, Parsonage D, Upton H, Rawat M, Claiborne A, Fahey RC, Helmann JD (2010) Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in Bacilli. Proc Natl Acad Sci USA 107:6482–6486

    CAS  PubMed  Google Scholar 

  • Gallogly MM, Starke DW, Mieyal JJ (2009) Mechanistic and kinetic details of catalysis of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation. Antioxid Redox Signal 11:1059–1081

    CAS  PubMed  Google Scholar 

  • Gelhaye E, Rouhier N, Jacquot JP (2003) Evidence for a subgroup of thioredoxin h that requires GSH/Grx for its reduction. FEBS Lett 555:443–448

    CAS  PubMed  Google Scholar 

  • Gelhaye E, Rouhier N, Navrot N, Jacquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62:24–35

    CAS  PubMed  Google Scholar 

  • Ghezzi P, di Simplicio P (2007) Glutathionylation pathways in drug response. Curr Opin Pharmacol 7:398–403

    CAS  PubMed  Google Scholar 

  • Ghosh S, Hamdan SM, Cook TE, Richardson CC (2008) Interactions of Escherichia coli thioredoxin, the processivity factor, with bacteriophage T7 DNA polymerase and helicase. J Biol Chem 283:32077–32084

    CAS  PubMed  Google Scholar 

  • Gommel DU, Nogoceke E, Morr M, Kiess M, Kalisz HM, Flohe L (1997) Catalytic characteristics of tryparedoxin. Eur J Biochem 248:913–918

    CAS  PubMed  Google Scholar 

  • Guo Y, Huang C, Xie Y, Song F, Zhou X (2010) A tomato glutaredoxin gene SlGRX1 regulates plant responses to oxidative, drought and salt stresses. Planta 232:1499–1509

    CAS  PubMed  Google Scholar 

  • Hamdan SM, Marintcheva B, Cook T, Lee SJ, Tabor S, Richardson CC (2005) A unique loop in T7 DNA polymerase mediates the binding of helicase-primase, DNA binding protein, and processivity factor. Proc Natl Acad Sci USA 102:5096–5101

    CAS  PubMed  Google Scholar 

  • Hansen RE, Roth D, Winther JR (2009) Quantifying the global cellular thiol-disulfide status. Proc Natl Acad Sci USA 106:422–427

    CAS  PubMed  Google Scholar 

  • Helmann JD (2011) Bacillithiol, a new player in bacterial redox homeostasis. Antioxid Redox Signal 15:123–133

    CAS  PubMed  Google Scholar 

  • Heras B, Edeling MA, Schirra HJ, Raina S, Martin JL (2004) Crystal structures of the DsbG disulfide isomerase reveal an unstable disulfide. Proc Natl Acad Sci USA 101:8876–8881

    CAS  PubMed  Google Scholar 

  • Herrero E, Ros J, Belli G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780:1217–1235

    CAS  PubMed  Google Scholar 

  • Hirota K, Matsui M, Iwata S, Nishiyama A, Mori K, Yodoi J (1997) AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci USA 94:3633–3638

    CAS  PubMed  Google Scholar 

  • Hirota K, Murata M, Sachi Y, Nakamura H, Takeuchi J, Mori K, Yodoi J (1999) Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J Biol Chem 274:27891–27897

    CAS  PubMed  Google Scholar 

  • Hoffmann B, Uzarska MA, Berndt C, Godoy JR, Haunhorst P, Lillig CH, Lill R, Muhlenhoff U (2011) The multidomain thioredoxin-monothiol glutaredoxins represent a distinct functional group. Antioxid Redox Signal 15:19–30

    CAS  PubMed  Google Scholar 

  • Holmgren A (1976) Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc Natl Acad Sci USA 73:2275–2279

    CAS  PubMed  Google Scholar 

  • Holmgren A (1989) Thioredoxin and glutaredoxin systems. J Biol Chem 264:13963–13966

    CAS  PubMed  Google Scholar 

  • Holmgren A, Bjornstedt M (1995) Thioredoxin and thioredoxin reductase. Methods Enzymol 252:199–208

    CAS  PubMed  Google Scholar 

  • Holmgren A, Soderberg BO, Eklund H, Branden CI (1975) Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8 Å resolution. Proc Natl Acad Sci USA 72:2305–2309

    CAS  PubMed  Google Scholar 

  • Hwang C, Sinskey AJ, Lodish HF (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257:1496–1502

    CAS  PubMed  Google Scholar 

  • Iwema T, Picciocchi A, Traore DA, Ferrer JL, Chauvat F, Jacquamet L (2009) Structural basis for delivery of the intact [Fe2S2] cluster by monothiol glutaredoxin. Biochemistry 48:6041–6043

    CAS  PubMed  Google Scholar 

  • Jbel M, Mercier A, Labbe S (2011) Grx4 monothiol glutaredoxin is required for iron limitation-dependent inhibition of Fep1. Eukaryot Cell 10:629–645

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johansson C, Lillig CH, Holmgren A (2004) Human mitochondrial glutaredoxin reduces S-glutathionylated proteins with high affinity accepting electrons from either glutathione or thioredoxin reductase. J Biol Chem 279:7537–7543

    CAS  PubMed  Google Scholar 

  • Koh CS, Navrot N, Didierjean C, Rouhier N, Hirasawa M, Knaff DB, Wingsle G, Samian R, Jacquot JP, Corbier C, Gelhaye E (2008) An atypical catalytic mechanism involving three cysteines of thioredoxin. J Biol Chem 283:23062–23072

    CAS  PubMed  Google Scholar 

  • Koppenol WH, Moreno JJ, Pryor WA, Ischiropoulos H, Beckman JS (1992) Peroxynitrite, a cloaked oxidant formed by nitric-oxide and superoxide. Chem Res Toxicol 5:834–842

    CAS  PubMed  Google Scholar 

  • Krause G, Holmgren A (1991) Substitution of the conserved tryptophan 31 in Escherichia coli thioredoxin by site-directed mutagenesis and structure-function analysis. J Biol Chem 266:4056–4066

    CAS  PubMed  Google Scholar 

  • Krauth-Siegel L, Leroux AE (2012) Low molecular mass antioxidants in parasites. Antioxid Redox Signal 17(4):583–607

    CAS  PubMed  Google Scholar 

  • Krauth-Siegel RL, Bauer H, Schirmer RH (2005) Dithiol proteins as guardians of the intracellular redox milieu in parasites: old and new drug targets in trypanosomes and malaria-causing plasmodia. Angew Chem Int Ed Engl 44:690–715

    CAS  PubMed  Google Scholar 

  • Kumanovics A, Chen OS, Li L, Bagley D, Adkins EM, Lin H, Dingra NN, Outten CE, Keller G, Winge D, Ward DM, Kaplan J (2008) Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial iron-sulfur cluster synthesis. J Biol Chem 283:10276–10286

    CAS  PubMed  Google Scholar 

  • Kumar C, Igbaria A, D’Autreaux B, Planson AG, Junot C, Godat E, Bachhawat AK, Delaunay-Moisan A, Toledano MB (2011) Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J 30:2044–2056

    CAS  PubMed  Google Scholar 

  • Kuster GM, Siwik DA, Pimentel DR, Colucci WS (2006) Role of reversible, thioredoxin-sensitive oxidative protein modifications in cardiac myocytes. Antioxid Redox Signal 8:2153–2159

    CAS  PubMed  Google Scholar 

  • la Camera S, L’Haridon F, Astier J, Zander M, Abou-Mansour E, Page G, Thurow C, Wendehenne D, Gatz C, Metraux JP, Lamotte O (2011) The glutaredoxin ATGRXS13 is required to facilitate Botrytis cinerea infection of Arabidopsis thaliana plants. Plant J 68:507–519

    PubMed  Google Scholar 

  • Laporte D, Olate E, Salinas P, Salazar M, Jordana X, Holuigue L (2011) Glutaredoxin GRXS13 plays a key role in protection against photooxidative stress in Arabidopsis. J Exp Bot 63(1):503–515

    PubMed  Google Scholar 

  • Laurent TC, Moore EC, Reichard P (1964) Enzymatic synthesis of deoxyribonucleotides. Iv. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J Biol Chem 239:3436–3444

    CAS  PubMed  Google Scholar 

  • Lee J-W, Soonsanga S, Helmann JD (2007) A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. Proc Natl Acad Sci USA 104:8743–8748

    CAS  PubMed  Google Scholar 

  • Lennon BW, Williams CH, Ludwig ML (2000) Twists in catalysis: alternating conformations of Escherichia coli thioredoxin reductase. Science 289:1190–1194

    CAS  PubMed  Google Scholar 

  • Li H, Mapolelo DT, Dingra NN, Naik SG, Lees NS, Hoffman BM, Riggs-Gelasco PJ, Huynh BH, Johnson MK, Outten CE (2009) The yeast iron regulatory proteins Grx3/4 and Fra2 form heterodimeric complexes containing a [2Fe-2S] cluster with cysteinyl and histidyl ligation. Biochemistry 48:9569–9581

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li H, Mapolelo DT, Dingra NN, Keller G, Riggs-Gelasco PJ, Winge DR, Johnson MK, Outten CE (2011) Histidine 103 in Fra2 is an iron-sulfur cluster ligand in the [2Fe-2S] Fra2-Grx3 complex and is required for in vivo iron signaling in yeast. J Biol Chem 286:867–876

    CAS  PubMed  Google Scholar 

  • Lillig CH, Berndt C, Vergnolle O, Lonn ME, Hudemann C, Bill E, Holmgren A (2005) Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc Natl Acad Sci USA 102:8168–8173

    CAS  PubMed  Google Scholar 

  • Lillig CH, Berndt C, Holmgren A (2008) Glutaredoxin systems. Biochim Biophys Acta 1780:1304–1317

    CAS  PubMed  Google Scholar 

  • Ludemann H, Dormeyer M, Sticherling C, Stallmann D, Follmann H, Krauth-Siegel RL (1998) Trypanosoma brucei tryparedoxin, a thioredoxin-like protein in African trypanosomes. FEBS Lett 431:381–385

    CAS  PubMed  Google Scholar 

  • Martin JL (1995) Thioredoxin–a fold for all reasons. Structure 3:245–250

    CAS  PubMed  Google Scholar 

  • Martin H, Dean M (1991) Identification of a thioredoxin-related protein associated with plasma membranes. Biochem Biophys Res Commun 175:123–128

    CAS  PubMed  Google Scholar 

  • Maruyama T, Sachi Y, Furuke K, Kitaoka Y, Kanzaki H, Yoshimura Y, Yodoi J (1999) Induction of thioredoxin, a redox-active protein, by ovarian steroid hormones during growth and differentiation of endometrial stromal cells in vitro. Endocrinology 140:365–372

    CAS  PubMed  Google Scholar 

  • McCarthy AA, Haebel PW, Torronen A, Rybin V, Baker EN, Metcalf P (2000) Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat Struct Biol 7:196–199

    CAS  PubMed  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760

    CAS  PubMed  Google Scholar 

  • Melchers J, Dirdjaja N, Ruppert T, Krauth-Siegel RL (2007) Glutathionylation of trypanosomal thiol redox proteins. J Biol Chem 282:8678–8694

    CAS  PubMed  Google Scholar 

  • Mercier A, Labbe S (2009) Both Php4 function and subcellular localization are regulated by iron via a multistep mechanism involving the glutaredoxin Grx4 and the exportin Crm1. J Biol Chem 284:20249–20262

    CAS  PubMed  Google Scholar 

  • Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, Shelton MD (2008) Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 10: 1941–1988

    CAS  PubMed  Google Scholar 

  • Miranda-Vizuete A, Damdimopoulos AE, Gustafsson J, Spyrou G (1997) Cloning, expression, and characterization of a novel Escherichia coli thioredoxin. J Biol Chem 272:30841–30847

    CAS  PubMed  Google Scholar 

  • Misset-Smits M, van Ophem PW, Sakuda S, Duine JA (1997) Mycothiol, 1-O-(2′-[N-acetyl-L-cysteinyl]amido-2′-deoxy-alpha-D-glucopyranosyl)-D- myo-inositol, is the factor of NAD/factor-dependent formaldehyde dehydrogenase. FEBS Lett 409:221–222

    CAS  PubMed  Google Scholar 

  • Mitchell DA, Marletta MA (2005) Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat Chem Biol 1:154–158

    CAS  PubMed  Google Scholar 

  • Mitchell DA, Erwin PA, Michel T, Marletta MA (2005) S-Nitrosation and regulation of inducible nitric oxide synthase. Biochemistry 44:4636–4647

    CAS  PubMed  Google Scholar 

  • Mitchell DA, Morton SU, Fernhoff NB, Marletta MA (2007) Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc Natl Acad Sci USA 104:11609–11614

    CAS  PubMed  Google Scholar 

  • Molina-Navarro MM, Casas C, Piedrafita L, Belli G, Herrero E (2006) Prokaryotic and eukaryotic monothiol glutaredoxins are able to perform the functions of Grx5 in the biogenesis of Fe/S clusters in yeast mitochondria. FEBS Lett 580:2273–2280

    CAS  PubMed  Google Scholar 

  • Moore EC, Reichard P, Thelander L (1964) Enzymatic synthesis of deoxyribonucleotides. V. Purification and properties of thioredoxin reductase from Escherichia coli B. J Biol Chem 239:3445–3452

    CAS  PubMed  Google Scholar 

  • Muhlenhoff U, Gerber J, Richhardt N, Lill R (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J 22:4815–4825

    PubMed  Google Scholar 

  • Muhlenhoff U, Molik S, Godoy JR, Uzarska MA, Richter N, Seubert A, Zhang Y, Stubbe J, Pierrel F, Herrero E, Lillig CH, Lill R (2010) Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound iron-sulfur cluster. Cell Metab 12: 373–385

    PubMed  Google Scholar 

  • Muller EG (1991) Thioredoxin deficiency in yeast prolongs S phase and shortens the G1 interval of the cell cycle. J Biol Chem 266:9194–9202

    CAS  PubMed  Google Scholar 

  • Nakamura T, Nakamura H, Hoshino T, Ueda S, Wada H, Yodoi J (2005) Redox regulation of lung inflammation by thioredoxin. Antioxid Redox Signal 7:60–71

    CAS  PubMed  Google Scholar 

  • Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ndamukong I, Abdallat AA, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007) SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J 50:128–139

    CAS  PubMed  Google Scholar 

  • Newton GL, Bewley CA, Dwyer TJ, Horn R, Aharonowitz Y, Cohen G, Davies J, Faulkner DJ, Fahey RC (1995) The structure of U17 isolated from Streptomyces clavuligerus and its properties as an antioxidant thiol. Eur J Biochem 230:821–825

    CAS  PubMed  Google Scholar 

  • Newton GL, Av-Gay Y, Fahey RC (2000) A novel mycothiol-dependent detoxification pathway in mycobacteria involving mycothiol S-conjugate amidase. Biochemistry 39:10739–10746

    CAS  PubMed  Google Scholar 

  • Newton GL, Buchmeier N, Fahey RC (2008) Biosynthesis and functions of mycothiol, the unique protective thiol of Actinobacteria. Microbiol Mol Biol Rev 72:471–494

    CAS  PubMed Central  PubMed  Google Scholar 

  • Newton GL, Rawat M, la Clair JJ, Jothivasan VK, Budiarto T, Hamilton CJ, Claiborne A, Helmann JD, Fahey RC (2009) Bacillithiol is an antioxidant thiol produced in Bacilli. Nat Chem Biol 5:625–627

    CAS  PubMed Central  PubMed  Google Scholar 

  • Newton GL, Leung SS, Wakabayashi JI, Rawat M, Fahey RC (2011) The DinB superfamily includes novel mycothiol, bacillithiol, and glutathione S-transferases. Biochemistry 50: 10751–10760

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nicely NI, Parsonage D, Paige C, Newton GL, Fahey RC, Leonardi R, Jackowski S, Mallett TC, Claiborne A (2007) Structure of the type III pantothenate kinase from Bacillus anthracis at 2.0 A resolution: implications for coenzyme A-dependent redox biology. Biochemistry 46: 3234–3245

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nogoceke E, Gommel DU, Kiess M, Kalisz HM, Flohe L (1997) A unique cascade of oxidoreductases catalyses trypanothione-mediated peroxide metabolism in Crithidia fasciculata. Biol Chem 378:827–836

    CAS  PubMed  Google Scholar 

  • Nulton-Persson AC, Starke DW, Mieyal JJ, Szweda LI (2003) Reversible inactivation of alpha-ketoglutarate dehydrogenase in response to alterations in the mitochondrial glutathione status. Biochemistry 42:4235–4242

    CAS  PubMed  Google Scholar 

  • Ojeda L, Keller G, Muhlenhoff U, Rutherford JC, Lill R, Winge DR (2006) Role of glutaredoxin-3 and glutaredoxin-4 in the iron regulation of the Aft1 transcriptional activator in Saccharomyces cerevisiae. J Biol Chem 281:17661–17669

    CAS  PubMed  Google Scholar 

  • Ordóñez E, van Belle K, Roos G, de Galan S, Letek M, Gil JA, Wyns L, Mateos LM, Messens J (2009) Arsenate reductase, mycothiol, and mycoredoxin concert thiol/disulfide exchange. J Biol Chem 284:15107–15116

    PubMed  Google Scholar 

  • Oza SL, Tetaud E, Ariyanayagam MR, Warnon SS, Fairlamb AH (2002) A single enzyme catalyses formation of Trypanothione from glutathione and spermidine in Trypanosoma cruzi. J Biol Chem 277:35853–35861

    CAS  PubMed  Google Scholar 

  • Pedrajas JR, Kosmidou E, Miranda-Vizuete A, Gustafsson JA, Wright AP, Spyrou G (1999) Identification and functional characterization of a novel mitochondrial thioredoxin system in Saccharomyces cerevisiae. J Biol Chem 274:6366–6373

    CAS  PubMed  Google Scholar 

  • Peskin AV, Winterbourn CC (2001) Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate. Free Radic Biol Med 30:572–579

    CAS  PubMed  Google Scholar 

  • Powis G, Mustacich D, Coon A (2000) The role of the redox protein thioredoxin in cell growth and cancer. Free Radic Biol Med 29:312–322

    CAS  PubMed  Google Scholar 

  • Pujol-Carrion N, Belli G, Herrero E, Nogues A, De la Torre-Ruiz MA (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J Cell Sci 119:4554–4564

    CAS  PubMed  Google Scholar 

  • Qin J, Clore GM, Gronenborn AM (1994) The high-resolution three-dimensional solution structures of the oxidized and reduced states of human thioredoxin. Structure 2:503–522

    CAS  PubMed  Google Scholar 

  • Quijano C, Alvarez B, Gatti RM, Augusto O, Radi R (1997) Pathways of peroxynitrite oxidation of thiol groups. Biochem J 322:167–173

    CAS  PubMed  Google Scholar 

  • Radi R, Beckman JS, Bush KM, Freeman BA (1991) Peroxynitrite oxidation of sulfhydryls – the cytotoxic potential of superoxide and nitric-oxide. J Biol Chem 266:4244–4250

    CAS  PubMed  Google Scholar 

  • Rawat M, Av-Gay Y (2007) Mycothiol-dependent proteins in actinomycetes. FEMS Microbiol Rev 31:278–292

    CAS  PubMed  Google Scholar 

  • Reckenfelderbaumer N, Krauth-Siegel RL (2002) Catalytic properties, thiol pK value, and redox potential of Trypanosoma brucei tryparedoxin. J Biol Chem 277:17548–17555

    CAS  PubMed  Google Scholar 

  • Reinemer P, Dirr HW, Ladenstein R, Schaffer J, Gallay O, Huber R (1991) The three-dimensional structure of class pi glutathione S-transferase in complex with glutathione sulfonate at 2.3 Å resolution. EMBO J 10:1997–2005

    CAS  PubMed  Google Scholar 

  • Ren B, Huang W, Åkesson B, Ladenstein R (1997) The crystal structure of seleno-glutathione peroxidase from human plasma at 2.9 Å resolution. J Mol Biol 268:869–885

    CAS  PubMed  Google Scholar 

  • Rietsch A, Bessette P, Georgiou G, Beckwith J (1997) Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin. J Bacteriol 179:6602–6608

    CAS  PubMed Central  PubMed  Google Scholar 

  • Riondet C, Desouris JP, Montoya JG, Chartier Y, Meyer Y, Reichheld JP (2011) A dicotyledon-specific glutaredoxin GRXC1 family with dimer-dependent redox regulation is functionally redundant with GRXC2. Plant Cell Environ 35(2):360–373

    PubMed  Google Scholar 

  • Ritz D, Patel H, Doan B, Zheng M, Aslund F, Storz G, Beckwith J (2000) Thioredoxin 2 is involved in the oxidative stress response in Escherichia coli. J Biol Chem 275:2505–2512

    CAS  PubMed  Google Scholar 

  • Rodriguez-Manzaneque MT, Tamarit J, Belli G, Ros J, Herrero E (2002) Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13:1109–1121

    CAS  PubMed Central  PubMed  Google Scholar 

  • Roos G, Messens J (2011) Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic Biol Med 51:314–326

    CAS  PubMed  Google Scholar 

  • Roos G, Garcia-Pino A, van Belle K, Brosens E, Wahni K, Vandenbussche G, Wyns L, Loris R, Messens J (2007) The conserved active site proline determines the reducing power of Staphylococcus aureus thioredoxin. J Mol Biol 368:800–811

    CAS  PubMed  Google Scholar 

  • Roos G, Foloppe N, van Laer K, Wyns L, Nilsson L, Geerlings P, Messens J (2009) How thioredoxin dissociates its mixed disulfide. PLOS Comput Biol 5:e1000461

    PubMed Central  PubMed  Google Scholar 

  • Rouhier N, Gelhaye E, Sautiere PE, Brun A, Laurent P, Tagu D, Gerard J, de Fay E, Meyer Y, Jacquot JP (2001) Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiol 127:1299–1309

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rouhier N, Unno H, Bandyopadhyay S, Masip L, Kim SK, Hirasawa M, Gualberto JM, Lattard V, Kusunoki M, Knaff DB, Georgiou G, Hase T, Johnson MK, Jacquot JP (2007) Functional, structural, and spectroscopic characterization of a glutathione-ligated [2Fe-2S] cluster in poplar glutaredoxin C1. Proc Natl Acad Sci USA 104:7379–7384

    CAS  PubMed  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166

    CAS  PubMed  Google Scholar 

  • Rouhier N, Couturier J, Johnson MK, Jacquot JP (2010) Glutaredoxins: roles in iron homeostasis. Trends Biochem Sci 35:43–52

    CAS  PubMed Central  PubMed  Google Scholar 

  • Russel M (1991) Filamentous phage assembly. Mol Microbiol 5:1607–1613

    CAS  PubMed  Google Scholar 

  • Schmidt H, Krauth-Siegel RL (2003) Functional and physicochemical characterization of the thioredoxin system in Trypanosoma brucei. J Biol Chem 278:46329–46336

    CAS  PubMed  Google Scholar 

  • Schroeder BO, Wu Z, Nuding S, Groscurth S, Marcinowski M, Beisner J, Buchner J, Schaller M, Stange EF, Wehkamp J (2011) Reduction of disulphide bonds unmasks potent antimicrobial activity of human beta-defensin 1. Nature 469:419–423

    CAS  PubMed  Google Scholar 

  • Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10:1235–1274

    PubMed  Google Scholar 

  • Spies HS, Steenkamp DJ (1994) Thiols of intracellular pathogens. Identification of ovothiol A in Leishmania donovani and structural analysis of a novel thiol from Mycobacterium bovis. Eur J Biochem 224:203–213

    CAS  PubMed  Google Scholar 

  • Sundaram S, Wu S, Ma LQ, Rathinasabapathi B (2009) Expression of a Pteris vittata glutaredoxin PvGRX5 in transgenic Arabidopsis thaliana increases plant arsenic tolerance and decreases arsenic accumulation in the leaves. Plant Cell Environ 32:851–858

    CAS  PubMed  Google Scholar 

  • Tarrago L, Laugier E, Zaffagnini M, Marchand C, Le Maréchal P, Rouhier N, Lemaire SD, Rey P (2009) Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J Biol Chem 284:18963–18971

    CAS  PubMed  Google Scholar 

  • Thomson L, Denicola A, Radi R (2003) The trypanothione-thiol system in Trypanosoma cruzi as a key antioxidant mechanism against peroxynitrite-mediated cytotoxicity. Arch Biochem Biophys 412:55–64

    CAS  PubMed  Google Scholar 

  • Tian G, Xiang S, Noiva R, Lennarz WJ, Schindelin H (2006) The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 124:61–73

    CAS  PubMed  Google Scholar 

  • Townsend DM (2007) S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol Interv 7:313–324

    CAS  PubMed  Google Scholar 

  • Vlamis-Gardikas A (2008) The multiple functions of the thiol-based electron flow pathways of Escherichia coli: eternal concepts revisited. Biochim Biophys Acta 1780:1170–1200

    CAS  PubMed  Google Scholar 

  • Vogt RN, Steenkamp DJ, Zheng R, Blanchard JS (2003) The metabolism of nitrosothiols in the Mycobacteria: identification and characterization of S-nitrosomycothiol reductase. Biochem J 374:657–666

    CAS  PubMed  Google Scholar 

  • Wang R, Yin YJ, Wang F, Li M, Feng J, Zhang HM, Zhang JP, Liu SJ, Chang WR (2007) Crystal structures and site-directed mutagenesis of a mycothiol-dependent enzyme reveal a novel folding and molecular basis for mycothiol-mediated maleylpyruvate isomerization. J Biol Chem 282:16288–16294

    CAS  PubMed  Google Scholar 

  • Watson WH, Pohl J, Montfort WR, Stuchlik O, Reed MS, Powis G, Jones DP (2003) Redox potential of human thioredoxin 1 and identification of a second dithiol/disulfide motif. J Biol Chem 278:33408–33415

    CAS  PubMed  Google Scholar 

  • Wingert RA, Galloway JL, Barut B, Foott H, Fraenkel P, Axe JL, Weber GJ, Dooley K, Davidson AJ, Schmid B, Paw BH, Shaw GC, Kingsley P, Palis J, Schubert H, Chen O, Kaplan J, Zon LI (2005) Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature 436:1035–1039

    CAS  PubMed  Google Scholar 

  • Winterbourn CC, Hampton MB (2008) Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45:549–561

    CAS  PubMed  Google Scholar 

  • Wong JH, Cai N, Balmer Y, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB (2004) Thioredoxin targets of developing wheat seeds identified by complementary proteomic approaches. Phytochemistry 65:1629–1640

    CAS  PubMed  Google Scholar 

  • Xia TH, Bushweller JH, Sodano P, Billeter M, Bjornberg O, Holmgren A, Wuthrich K (1992) NMR structure of oxidized Escherichia coli glutaredoxin: comparison with reduced E. coli glutaredoxin and functionally related proteins. Protein Sci 1:310–321

    CAS  PubMed  Google Scholar 

  • Xia B, Vlamis-Gardikas A, Holmgren A, Wright PE, Dyson HJ (2001) Solution structure of Escherichia coli glutaredoxin-2 shows similarity to mammalian glutathione-S-transferases. J Mol Biol 310:907–918

    CAS  PubMed  Google Scholar 

  • Xing S, Zachgo S (2008) ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J 53:790–801

    CAS  PubMed  Google Scholar 

  • Xu SZ, Sukumar P, Zeng F, Li J, Jairaman A, English A, Naylor J, Ciurtin C, Majeed Y, Milligan CJ, Bahnasi YM, Al-Shawaf E, Porter KE, Jiang LH, Emery P, Sivaprasadarao A, Beech DJ (2008) TRPC channel activation by extracellular thioredoxin. Nature 451:69–72

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zaffagnini M, Michelet L, Massot V, Trost P, Lemaire SD (2008) Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii reveals the unique properties of a chloroplastic CGFS-type glutaredoxin. J Biol Chem 283:8868–8876

    CAS  PubMed  Google Scholar 

  • Zhang HW, Squadrito GL, Uppu RM, Lemercier JN, Cueto R, Pryor WA (1997) Inhibition of peroxynitrite-mediated oxidation of glutathione by carbon dioxide. Arch Biochem Biophys 339:183–189

    CAS  PubMed  Google Scholar 

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Acknowledgements

JM is a group leader of the VIB and JFC is a Chercheur Qualifié of the Belgian FNRS. JM is indebted to JFC for helpful redox discussions over the past 5 years and JFC to JM. This work was supported by the European Research Council (FP7/2007–2013) ERC independent researcher starting grant 282335 – Sulfenic to JFC.

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Authors and Affiliations

  1. Department of Structural Biology, Vlaams Instituut voor Biotechnologie (VIB), Pleinlaan 2, B-1050, Brussels, Belgium

    Joris Messens

  2. Structural Biology Brussels, Vrije Universiteit Brussel (VUB), Pleinlaan 2, B-1050, Brussels, Belgium

    Joris Messens

  3. Brussels Center for Redox Biology, Brussels, Belgium

    Joris Messens & Jean-François Collet

  4. Faculté des Sciences, Unité Mixte de Recherches 1136, Interactions Arbres Microorganismes, Lorraine University-INRA, IFR 110 EFABA, Vandoeuvre Cedex, France

    Nicolas Rouhier

  5. de Duve Institute, Université catholique de Louvain, 75-39 Avenue Hippocrate, B-1200, Brussels, Belgium

    Jean-François Collet

  6. WELBIO, B-1200, Brussels, Belgium

    Jean-François Collet

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  1. Joris Messens
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  2. Nicolas Rouhier
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  3. Jean-François Collet
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Correspondence to Joris Messens or Jean-François Collet .

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Editors and Affiliations

  1. Mol.,Cel. and Developmental Biology, University of Michigan, Ann Arbor, Michigan, USA

    Ursula Jakob

  2. The Alexander Silberman Institute of Life Science, Department of Biological Chemistry, The Hebrew University of Jerusalem, Jerusalem, Israel

    Dana Reichmann

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Messens, J., Rouhier, N., Collet, JF. (2013). Redox Homeostasis. In: Jakob, U., Reichmann, D. (eds) Oxidative Stress and Redox Regulation. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5787-5_3

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