Reactive oxygen species (ROS) are the key mediators of pathogenesis in cardiovascular diseases. Members of the thioredoxin superfamily take an active part in scavenging reactive oxygen species, thus playing an essential role in maintaining the intracellular redox status. The alteration in the expression levels of thioredoxin family members and related molecules constitute effective biomarkers in various diseases, including cardiovascular complications that involve oxidative stress. Thioredoxin, glutaredoxin, peroxiredoxin, and glutathione peroxidase, along with their isoforms, are involved in interaction with the members of metabolic and signaling pathways, thus making them attractive targets for clinical intervention. Studies with cells and transgenic animals have supported this notion and raised the hope for possible gene therapy as modern genetic medicine. Of all the molecules, thioredoxins, glutaredoxins, and peroxiredoxins are emphasized, because a growing body of evidence reveals their essential and regulatory role in several steps of redox regulation. In this review, we discuss some pertinent observations regarding their distribution, structure, functions, and interactions with the several survival- and death-signaling pathways, especially in the myocardium. Antioxid. Redox Signal. 11, 2741–2758.
Get full access to this article
View all access options for this article.
References
1.
AdachiT, PimentelDR, HeibeckT, HouX, LeeYJ, JiangB, IdoY, CohenRA. S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J Biol Chem, 279:29857–29862. 2004.
2.
AgoT, LiuT, ZhaiP, ChenW, LiH, MolkentinJD, VatnerSF, SadoshimaJ. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell, 133:978–993. 2008.
3.
AgoT, SadoshimaJ. Thioredoxin1 as a negative regulator of cardiac hypertrophy. Antioxid Redox Signal, 9:679–687. 2007.
4.
AgoT, YehI, YamamotoM, Schinke-BraunM, BrownJA, TianB, SadoshimaJ. Thioredoxin1 upregulates mitochondrial proteins related to oxidative phosphorylation and TCA cycle in the heart. Antioxid Redox Signal, 8:1635–1650. 2006.
5.
ArakiM, NanriH, EjimaK, MurasatoY, FujiwaraT, NakashimaY, IkedaM. Antioxidant function of the mitochondrial protein SP-22 in the cardiovascular system. J Biol Chem, 274:2271–2278. 1999.
6.
BabichevY, IsakovN. Tyrosine phosphorylation of PICOT and its translocation to the nucleus in response of human T cells to oxidative stress. Adv Exp Med Biol, 495:41–45. 2001.
7.
BallingerSW, PattersonC, Knight-LozanoCA, BurowDL, ConklinCA, HuZ, ReufJ, HoraistC, LebovitzR, HunterGC, McIntyreK, RungeMS. Mitochondrial integrity and function in atherogenesis. Circulation, 106:544–549. 2002.
8.
BandyopadhyayS, StarkeDW, MieyalJJ, GronostajskiRM. Thioltransferase (glutaredoxin) reactivates the DNA-binding activity of oxidation-inactivated nuclear factor I. J Biol Chem, 273:392–397. 1998.
9.
BeerSM, TaylorER, BrownSE, DahmCC, CostaNJ, RunswickMJ, MurphyMP. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant DEFENSE. J Biol Chem, 279:47939–47951. 2004.
10.
BerggrenM, GallegosA, GasdaskaJ, PowisG. Cellular thioredoxin reductase activity is regulated by selenium. Anticancer Res, 17:3377–3380. 1997.
11.
BerggrenMM, PowisG. Alternative splicing is associated with decreased expression of the redox proto-oncogene thioredoxin-1 in human cancers. Arch Biochem Biophys, 389:144–149. 2001.
12.
BerndtC, HudemannC, HanschmannEM, AxelssonR, HolmgrenA, LilligCH. How does iron-sulfur cluster coordination regulate the activity of human glutaredoxin 2?Antioxid Redox Signal, 9:151–157. 2007.
13.
BjornstedtM, XueJ, HuangW, AkessonB, HolmgrenA. The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J Biol Chem, 269:29382–29384. 1994.
14.
BloomfieldKL, OsborneSA, KennedyDD, ClarkeFM, TonissenKF. Thioredoxin-mediated redox control of the transcription factor Sp1 and regulation of the thioredoxin gene promoter. Gene, 319:107–116. 2003.
BrixiusK, SchwingerRH, HoyerF, NappA, RennerR, BolckB, KuminA, FischerU, MehlhornU, WernerS, BlochW. Isoform-specific downregulation of peroxiredoxin in human failing myocardium. Life Sci, 81:823–831. 2007.
17.
CamaschellaC, CampanellaA, De FalcoL, BoschettoL, MerliniR, SilvestriL, LeviS, IolasconA. The human counterpart of zebrafish shiraz shows sideroblastic-like microcytic anemia and iron overload. Blood, 110:1353–1358. 2007.
18.
ChaH, KimJM, OhJG, JeongMH, ParkCS, ParkJ, JeongHJ, ParkBK, LeeYH, JeongD, YangDK, BerneckerOY, Kim doH, HajjarRJ, ParkWJ. PICOT is a critical regulator of cardiac hypertrophy and cardiomyocyte contractility. J Mol Cell Cardiol, 45:796–803. 2008.
ChaeHZ, KimHJ, KangSW, RheeSG. Characterization of three isoforms of mammalian peroxiredoxin that reduce peroxides in the presence of thioredoxin. Diabetes Res Clin Pract, 45:101–112. 1999.
21.
ChangTS, ChoCS, ParkS, YuS, KangSW, RheeSG. Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria. J Biol Chem, 279:41975–41984. 2004.
22.
ChiuehCC, AndohT, ChockPB. Induction of thioredoxin and mitochondrial survival proteins mediates preconditioning-induced cardioprotection and neuroprotection. Ann N Y Acad Sci, 1042:403–418. 2005.
ConradM, JakupogluC, MorenoSG, LipplS, BanjacA, SchneiderM, BeckH, HatzopoulosAK, JustU, SinowatzF, SchmahlW, ChienKR, WurstW, BornkammGW, BrielmeierM. Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function. Mol Cell Biol, 24:9414–9423. 2004.
25.
CunneaPM, Miranda-VizueteA, BertoliG, SimmenT, DamdimopoulosAE, HermannS, LeinonenS, HuikkoMP, GustafssonJA, SitiaR, SpyrouG. ERdj5, an endoplasmic reticulum (ER)-resident protein containing DnaJ and thioredoxin domains, is expressed in secretory cells or following ER stress. J Biol Chem, 278:1059–1066. 2003.
26.
DaiJ, WangX, FengJ, KongW, XuQ, ShenX. Regulatory role of thioredoxin in homocysteine-induced monocyte chemoattractant protein-1 secretion in monocytes/macrophages. FEBS Lett, 582:3893–3898. 2008.
27.
DamdimopoulosAE, Miranda-VizueteA, Pelto-HuikkoM, GustafssonJA, SpyrouG. Human mitochondrial thioredoxin: involvement in mitochondrial membrane potential and cell death. J Biol Chem, 277:33249–33257. 2002.
DasS, DerP, RaychaudhuriU, MaulikN, DasDK. The effect of Euryale ferox (Makhana), an herb of aquatic origin, on myocardial ischemic reperfusion injury. Mol Cell Biochem, 289:55–63. 2006.
30.
DiotteNM, XiongY, GaoJ, ChuaBH, HoYS. Attenuation of doxorubicin-induced cardiac injury by mitochondrial glutaredoxin 2. Biochim Biophys Acta, 1793:427–438. 2009.
31.
DudleyJ, DasS, MukherjeeS, DasDK. Resveratrol, a unique phytoalexin present in red wine, delivers either survival signal or death signal to the ischemic myocardium depending on dose. J Nutr Biochem, 20:443–452. 2009.
32.
DwivediVK, ChandraM, MisraPC, MisraA, MisraMK. Status of some free radical scavenging enzymes in the blood of myocardial infarction patients. J Enzyme Inhib Med Chem, 21:43–46. 2006.
33.
EbrahimianT, SairamMR, SchiffrinEL, TouyzRM. Cardiac hypertrophy is associated with altered thioredoxin and ASK-1 signaling in a mouse model of menopause. Am J Physiol Heart Circ Physiol, 295:H1481–H1488. 2008.
34.
EmaM, HirotaK, MimuraJ, AbeH, YodoiJ, SogawaK, PoellingerL, Fujii-KuriyamaY. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J, 18:1905–1914. 1999.
35.
EnokssonM, FernandesAP, PrastS, LilligCH, HolmgrenA, OrreniusS. Overexpression of glutaredoxin 2 attenuates apoptosis by preventing cytochrome c release. Biochem Biophys Res Commun, 327:774–779. 2005.
36.
FernandesAP, HolmgrenA. Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal, 6:63–74. 2004.
37.
FisherAB, DodiaC, ManevichY, ChenJW, FeinsteinSI. Phospholipid hydroperoxides are substrates for non-selenium glutathione peroxidase. J Biol Chem, 274:21326–21334. 1999.
38.
FujinoG, NoguchiT, MatsuzawaA, YamauchiS, SaitohM, TakedaK, IchijoH. Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol Cell Biol, 27:8152–8163. 2007.
39.
FunatoY, MikiH. Nucleoredoxin, a novel thioredoxin family member involved in cell growth and differentiation. Antioxid Redox Signal, 9:1035–1057. 2007.
40.
FurmanC, RundlofAK, LarigauderieG, JayeM, BriccaG, CopinC, KandoussiAM, FruchartJC, ArnerES, RouisM. Thioredoxin reductase 1 is upregulated in atherosclerotic plaques: specific induction of the promoter in human macrophages by oxidized low-density lipoproteins. Free Radic Biol Med, 37:71–85. 2004.
41.
GalloglyMM, MieyalJJ. Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr Opin Pharmacol, 7:381–391. 2007.
42.
GalloglyMM, StarkeDW, LeonbergAK, OspinaSM, MieyalJJ. Kinetic and mechanistic characterization and versatile catalytic properties of mammalian glutaredoxin 2: implications for intracellular roles. Biochemistry, 47:11144–11157. 2008.
43.
GasdaskaJR, HarneyJW, GasdaskaPY, PowisG, BerryMJ. Regulation of human thioredoxin reductase expression and activity by 3'-untranslated region selenocysteine insertion sequence and mRNA instability elements. J Biol Chem, 274:25379–25385. 1999.
44.
GasdaskaPY, GasdaskaJR, CochranS, PowisG. Cloning and sequencing of a human thioredoxin reductase. FEBS Lett, 373:5–9. 1995.
45.
GasdaskaPY, OblongJE, CotgreaveIA, PowisG. The predicted amino acid sequence of human thioredoxin is identical to that of the autocrine growth factor human adult T-cell derived factor (ADF): thioredoxin mRNA is elevated in some human tumors. Biochim Biophys Acta, 1218:292–296. 1994.
46.
GiguereP, TurcotteME, HamelinE, ParentA, BrissonJ, LarocheG, LabrecqueP, DupuisG, ParentJL. Peroxiredoxin-4 interacts with and regulates the thromboxane A(2) receptor. FEBS Lett, 581:3863–3868. 2007.
47.
GilmoreTD. Introduction: the Rel/NF-kappaB signal transduction pathway. Semin Cancer Biol, 8:61–62. 1997.
48.
GladyshevVN, LiuA, NovoselovSV, KrysanK, SunQA, KryukovVM, KryukovGV, LouMF. Identification and characterization of a new mammalian glutaredoxin (thioltransferase), Grx2. J Biol Chem, 276:30374–30380. 2001.
49.
HaggD, EnglundMC, JernasM, SchmidtC, WiklundO, HultenLM, OhlssonBG, CarlssonLM, CarlssonB, SvenssonPA. Oxidized LDL induces a coordinated up-regulation of the glutathione and thioredoxin systems in human macrophages. Atherosclerosis, 185:282–289. 2006.
HaraT, KondoN, NakamuraH, OkuyamaH, MitsuiA, HoshinoY, YodoiJ. Cell-surface thioredoxin-1: possible involvement in thiol-mediated leukocyte-endothelial cell interaction through lipid rafts. Antioxid Redox Signal, 9:1427–1437. 2007.
52.
HariharanJ, HebbarP, RanieJ, Philomena, SinhaAM, DattaS. Alternative forms of the human thioredoxin mRNA: identification and characterization. Gene, 173:265–270. 1996.
53.
HashemySI, HolmgrenA. Regulation of the catalytic activity and structure of human thioredoxin 1 via oxidation and S-nitrosylation of cysteine residues. J Biol Chem, 283:21890–21898. 2008.
54.
HattoriF, MurayamaN, NoshitaT, OikawaS. Mitochondrial peroxiredoxin-3 protects hippocampal neurons from excitotoxic injury in vivo. J Neurochem, 86:860–868. 2003.
55.
HerreroE, de la Torre-RuizMA. Monothiol glutaredoxins: a common domain for multiple functions. Cell Mol Life Sci, 64:1518–1530. 2007.
56.
HiraokaY, KishimotoC, TakadaH, KurokawaM, OchiaiH, ShirakiK, SasayamaS. Role of oxygen derived free radicals in the pathogenesis of coxsackievirus B3 myocarditis in mice. Cardiovasc Res, 27:957–961. 1993.
57.
HiroiT, WatabeS, TakimotoK, YagoN, YamamotoY, TakahashiSY. The cDNA sequence encoding bovine SP-22, a new defence system against reactive oxygen species in mitochondria. DNA Seq, 6:239–242. 1996.
58.
HirotaK, MatsuiM, IwataS, NishiyamaA, MoriK, YodoiJ. AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci U S A, 94:3633–3638. 1997.
59.
HirotaK, MatsuiM, MurataM, TakashimaY, ChengFS, ItohT, FukudaK, YodoiJ. Nucleoredoxin, glutaredoxin, and thioredoxin differentially regulate NF-kappaB, AP-1, and CREB activation in HEK293 cells. Biochem Biophys Res Commun, 274:177–182. 2000.
60.
HirotaK, MurataM, SachiY, NakamuraH, TakeuchiJ, MoriK, YodoiJ. 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. 1999.
61.
HokamakiJ, KawanoH, SoejimaH, MiyamotoS, KajiwaraI, KojimaS, SakamotoT, SugiyamaS, YoshimuraM, NakamuraH, YodoiJ, OgawaH. Plasma thioredoxin levels in patients with unstable angina. Int J Cardiol, 99:225–231. 2005.
62.
HolmgrenA. Enzymatic reduction-oxidation of protein disulfides by thioredoxin. Methods Enzymol, 107:295–300. 1984.
63.
HolmgrenA. Glutathione-dependent synthesis of deoxyribonucleotides: characterization of the enzymatic mechanism of Escherichia coli glutaredoxin. J Biol Chem, 254:3672–3678. 1979.
64.
HolmgrenA. Glutathione-dependent synthesis of deoxyribonucleotides: purification and characterization of glutaredoxin from Escherichia coli. J Biol Chem, 254:3664–3671. 1979.
65.
HolmgrenA. Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc Natl Acad Sci U S A, 73:2275–2279. 1976.
66.
HolmgrenA. Reduction of disulfides by thioredoxin: exceptional reactivity of insulin and suggested functions of thioredoxin in mechanism of hormone action. J Biol Chem, 254:9113–9119. 1979.
67.
HolmgrenA. Thioredoxin. Annu Rev Biochem, 54:237–271. 1985.
68.
HolmgrenA. Thioredoxin and glutaredoxin systems. J Biol Chem, 264:13963–13966. 1989.
69.
HolmgrenA, SoderbergBO, EklundH, BrandenCI. Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8 A resolution. Proc Natl Acad Sci U S A, 72:2305–2309. 1975.
70.
HoshinoY, ShiojiK, NakamuraH, MasutaniH, YodoiJ. From oxygen sensing to heart failure: role of thioredoxin. Antioxid Redox Signal, 9:689–699. 2007.
71.
HosodaA, KimataY, TsuruA, KohnoK. JPDI, a novel endoplasmic reticulum-resident protein containing both a BiP-interacting J-domain and thioredoxin-like motifs. J Biol Chem, 278:2669–2676. 2003.
InomataY, TaniharaH, TanitoM, OkuyamaH, HoshinoY, KinumiT, KawajiT, KondoN, YodoiJ, NakamuraH. Suppression of choroidal neovascularization by thioredoxin-1 via interaction with complement factor H. Invest Ophthalmol Vis Sci, 49:5118–5125. 2008.
75.
IsakovN, WitteS, AltmanA. PICOT-HD: a highly conserved protein domain that is often associated with thioredoxin and glutaredoxin modules. Trends Biochem Sci, 25:537–539. 2000.
76.
JeongD, ChaH, KimE, KangM, YangDK, KimJM, YoonPO, OhJG, BerneckerOY, SakataS, LeTT, CuiL, LeeYH, Kim doH, WooSH, LiaoR, HajjarRJ, ParkWJ. PICOT inhibits cardiac hypertrophy and enhances ventricular function and cardiomyocyte contractility. Circ Res, 99:307–314. 2006.
JeongW, YoonHW, LeeSR, RheeSG. Identification and characterization of TRP14, a thioredoxin-related protein of 14 kDa: new insights into the specificity of thioredoxin function. J Biol Chem, 279:3142–3150. 2004.
79.
JimenezA, Miranda-VizueteA. Purification and characterization of delta3Trx-1, a splicing variant of human thioredoxin-1 lacking exon 3. Protein Expr Purif, 27:319–324. 2003.
80.
JimenezA, ZuW, RaweVY, Pelto-HuikkoM, FlickingerCJ, SutovskyP, GustafssonJA, OkoR, Miranda-VizueteA. Spermatocyte/spermatid-specific thioredoxin-3, a novel Golgi apparatus-associated thioredoxin, is a specific marker of aberrant spermatogenesis. J Biol Chem, 279:34971–34982. 2004.
81.
JohanssonC, LilligCH, HolmgrenA. Human mitochondrial glutaredoxin reduces S-glutathionylated proteins with high affinity accepting electrons from either glutathione or thioredoxin reductase. J Biol Chem, 279:7537–7543. 2004.
82.
KagaS, ZhanL, MatsumotoM, MaulikN. Resveratrol enhances neovascularization in the infarcted rat myocardium through the induction of thioredoxin-1, heme oxygenase-1 and vascular endothelial growth factor. J Mol Cell Cardiol, 39:813–822. 2005.
83.
Kaimul AhsanM, NakamuraH, TanitoM, YamadaK, UtsumiH, YodoiJ. Thioredoxin-1 suppresses lung injury and apoptosis induced by diesel exhaust particles (DEP) by scavenging reactive oxygen species and by inhibiting DEP-induced downregulation of Akt. Free Radic Biol Med, 39:1549–1559. 2005.
84.
Kaimul AhsanM, NakamuraH, MasutaniH, YodoiJ. Thioredoxin and thioredoxin-binding protein-2 in cancer and metabolic syndrome. Free Radic Biol Med, 43:861–868. 2007.
85.
KimK, RheeSG, StadtmanER. Nonenzymatic cleavage of proteins by reactive oxygen species generated by dithiothreitol and iron. J Biol Chem, 260:15394–15397. 1985.
86.
KishimotoC, ShiojiK, NakamuraH, NakayamaY, YodoiJ, SasayamaS. Serum thioredoxin (TRX) levels in patients with heart failure. Jpn Circ J, 65:491–494. 2001.
87.
KleemannR, KapurniotuA, MischkeR, HeldJ, BernhagenJ. Characterization of catalytic centre mutants of macrophage migration inhibitory factor (MIF) and comparison to Cys81Ser MIF. Eur J Biochem, 261:753–766. 1999.
88.
Kobayashi-MiuraM, ShiojiK, HoshinoY, MasutaniH, NakamuraH, YodoiJ. Oxygen sensing and redox signaling: the role of thioredoxin in embryonic development and cardiac diseases. Am J Physiol Heart Circ Physiol, 292:H2040–H2050. 2007.
KondoN, IshiiY, SonA, Sakakura-NishiyamaJ, KwonYW, TanitoM, NishinakaY, MatsuoY, NakayamaT, TaniguchiM, YodoiJ. Cysteine-dependent immune regulation by TRX and MIF/GIF family proteins. Immunol Lett, 92:143–147. 2004.
91.
KrauseG, LundstromJ, BareaJL, Pueyo de la CuestaC, HolmgrenA. Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J Biol Chem, 266:9494–9500. 1991.
92.
KumarS, BjornstedtM, HolmgrenA. Selenite is a substrate for calf thymus thioredoxin reductase and thioredoxin and elicits a large non-stoichiometric oxidation of NADPH in the presence of oxygen. Eur J Biochem, 207:435–439. 1992.
93.
KurookaH, KatoK, MinoguchiS, TakahashiY, IkedaJ, HabuS, OsawaN, BuchbergAM, MoriwakiK, ShisaH, HonjoT. Cloning and characterization of the nucleoredoxin gene that encodes a novel nuclear protein related to thioredoxin. Genomics, 39:331–339. 1997.
94.
KusterGM, PimentelDR, AdachiT, IdoY, BrennerDA, CohenRA, LiaoR, SiwikDA, ColucciWS. Alpha-adrenergic receptor-stimulated hypertrophy in adult rat ventricular myocytes is mediated via thioredoxin-1-sensitive oxidative modification of thiols on Ras. Circulation, 111:1192–1198. 2005.
95.
KusterGM, SiwikDA, PimentelDR, ColucciWS. Role of reversible, thioredoxin-sensitive oxidative protein modifications in cardiac myocytes. Antioxid Redox Signal, 8:2153–2159. 2006.
96.
LaughnerBJ, SehnkePC, FerlRJ. A novel nuclear member of the thioredoxin superfamily. Plant Physiol, 118:987–996. 1998.
97.
LaurentTC, MooreEC, ReichardP. Enzymatic synthesis of deoxyribonucleotides. IV: isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J Biol Chem, 239:3436–3444. 1964.
98.
LeeKK, MurakawaM, TakahashiS, TsubukiS, KawashimaS, SakamakiK, YoneharaS. Purification, molecular cloning, and characterization of TRP32, a novel thioredoxin-related mammalian protein of 32 kDa. J Biol Chem, 273:19160–19166. 1998.
99.
LeeSR, YangKS, KwonJ, LeeC, JeongW, RheeSG. Reversible inactivation of the tumor suppressor PTEN by H2O2. J Biol Chem, 277:20336–20342. 2002.
100.
LeferDJ, GrangerDN. Oxidative stress and cardiac disease. Am J Med, 109:315–323. 2000.
101.
LiX, TangK, XieB, LiS, RozanskiGJ. Regulation of Kv4 channel expression in failing rat heart by the thioredoxin system. Am J Physiol Heart Circ Physiol, 295:H416–H424. 2008.
102.
LiX, XuZ, LiS, RozanskiGJ. Redox regulation of Ito remodeling in diabetic rat heart. Am J Physiol Heart Circ Physiol, 288:H1417–H1424. 2005.
LilligCH, BerndtC, VergnolleO, LonnME, HudemannC, BillE, HolmgrenA. Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc Natl Acad Sci U S A, 102:8168–8173. 2005.
105.
LilligCH, LonnME, EnokssonM, FernandesAP, HolmgrenA. Short interfering RNA-mediated silencing of glutaredoxin 2 increases the sensitivity of HeLa cells toward doxorubicin and phenylarsine oxide. Proc Natl Acad Sci U S A, 101:13227–13232. 2004.
106.
LiuW, NakamuraH, ShiojiK, TanitoM, OkaS, AhsanMK, SonA, IshiiY, KishimotoC, YodoiJ. Thioredoxin-1 ameliorates myosin-induced autoimmune myocarditis by suppressing chemokine expressions and leukocyte chemotaxis in mice. Circulation, 110:1276–1283. 2004.
107.
LonnME, HudemannC, BerndtC, CherkasovV, CapaniF, HolmgrenA, LilligCH. Expression pattern of human glutaredoxin 2 isoforms: identification and characterization of two testis/cancer cell-specific isoforms. Antioxid Redox Signal, 10:547–557. 2008.
108.
LuanR, LiuS, YinT, LauWB, WangQ, GuoW, WangH, TaoL. High glucose sensitizes adult cardiomyocytes to ischaemia/reperfusion injury through nitrative thioredoxin inactivation. Cardiovasc Res, 83:294–302. 2009.
109.
LundbergM, FernandesAP, KumarS, HolmgrenA. Cellular and plasma levels of human glutaredoxin 1 and 2 detected by sensitive ELISA systems. Biochem Biophys Res Commun, 319:801–809. 2004.
110.
LundbergM, JohanssonC, ChandraJ, EnokssonM, JacobssonG, LjungJ, JohanssonM, HolmgrenA. Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J Biol Chem, 276:26269–26275. 2001.
111.
MalikG, NagyN, HoYS, MaulikN, DasDK. Role of glutaredoxin-1 in cardioprotection: an insight with Glrx1 transgenic and knockout animals. J Mol Cell Cardiol, 44:261–269. 2008.
112.
ManevichY, SweitzerT, PakJH, FeinsteinSI, MuzykantovV, FisherAB. 1-Cys peroxiredoxin overexpression protects cells against phospholipid peroxidation-mediated membrane damage. Proc Natl Acad Sci U S A, 99:11599–11604. 2002.
113.
MasutaniH, NishiyamaA, KownYW, KimYC, NakamuraH, YodoiJ. FuchsJ, PackerL. Redox regulation of gene expression and transcription factors in response to environmental oxidants. Enviromental stressors in health and disease. New York: Dekker, 2001; 115–134.
114.
MatsuiM, OshimaM, OshimaH, TakakuK, MaruyamaT, YodoiJ, TaketoMM. Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev Biol, 178:179–185. 1996.
115.
MatsuoY, AkiyamaN, NakamuraH, YodoiJ, NodaM, Kizaka-KondohS. Identification of a novel thioredoxin-related transmembrane protein. J Biol Chem, 276:10032–10038. 2001.
116.
MatsushimaS, IdeT, YamatoM, MatsusakaH, HattoriF, IkeuchiM, KubotaT, SunagawaK, HasegawaY, KuriharaT, OikawaS, KinugawaS, TsutsuiH. Overexpression of mitochondrial peroxiredoxin-3 prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation, 113:1779–1786. 2006.
117.
MaulikN, DasDK. Emerging potential of thioredoxin and thioredoxin interacting proteins in various disease conditions. Biochim Biophys Acta, 1780:1368–1382. 2008.
118.
Miranda-VizueteA, LjungJ, DamdimopoulosAE, GustafssonJA, OkoR, Pelto-HuikkoM, SpyrouG. Characterization of Sptrx, a novel member of the thioredoxin family specifically expressed in human spermatozoa. J Biol Chem, 276:31567–31574. 2001.
MiwaK, KishimotoC, NakamuraH, MakitaT, IshiiK, OkudaN, TaniguchiA, ShiojiK, YodoiJ, SasayamaS. Increased oxidative stress with elevated serum thioredoxin level in patients with coronary spastic angina. Clin Cardiol, 26:177–181. 2003.
121.
MiwaK, KishimotoC, NakamuraH, MakitaT, IshiiK, OkudaN, YodoiJ, SasayamaS. Serum thioredoxin and alpha-tocopherol concentrations in patients with major risk factors. Circ J, 69:291–294. 2005.
122.
MiyamotoS, KawanoH, HokamakiJ, SoejimaH, KojimaS, KudohT, NagayoshiY, SugiyamaS, SakamotoT, YoshimuraM, NakamuraH, YodoiJ, OgawaH. Increased plasma levels of thioredoxin in patients with glucose intolerance. Intern Med, 44:1127–1132. 2005.
123.
MiyamotoS, SakamotoT, SoejimaH, ShimomuraH, KajiwaraI, KojimaS, HokamakiJ, SugiyamaS, YoshimuraM, OzakiY, NakamuraH, YodoiJ, OgawaH. Plasma thioredoxin levels and platelet aggregability in patients with acute myocardial infarction. Am Heart J, 146:465–471. 2003.
124.
MoothaVK, BunkenborgJ, OlsenJV, HjerrildM, WisniewskiJR, StahlE, BolouriMS, RayHN, SihagS, KamalM, PattersonN, LanderES, MannM. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell, 115:629–640. 2003.
125.
MuC, ZhaoJ, WangL, SongL, ZhangH, LiC, QiuL, GaiY. Molecular cloning and characterization of peroxiredoxin 6 from Chinese mitten crab Eriocheir sinensis. Fish Shellfish Immunol, 26:821–827. 2009.
126.
MukherjeeS, GangopadhyayH, DasDK. Broccoli: a unique vegetable that protects mammalian hearts through the redox cycling of the thioredoxin superfamily. J Agric Food Chem, 56:609–617. 2008.
127.
MurataH, IharaY, NakamuraH, YodoiJ, SumikawaK, KondoT. Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J Biol Chem, 278:50226–50233. 2003.
128.
NagyN, MalikG, FisherAB, DasDK. Targeted disruption of peroxiredoxin 6 gene renders the heart vulnerable to ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol, 291:H2636–H2640. 2006.
129.
NagyN, MalikG, TosakiA, HoYS, MaulikN, DasDK. Overexpression of glutaredoxin-2 reduces myocardial cell death by preventing both apoptosis and necrosis. J Mol Cell Cardiol, 44:252–260. 2008.
130.
NakamuraH. Extracellular functions of thioredoxin. Novartis Found Symp, 291:184–192discussion 192–185, 221–1842008.
131.
NakamuraH, HerzenbergLA, BaiJ, ArayaS, KondoN, NishinakaY, YodoiJ. Circulating thioredoxin suppresses lipopolysaccharide-induced neutrophil chemotaxis. Proc Natl Acad Sci U S A, 98:15143–15148. 2001.
132.
NakamuraH, MasutaniH, YodoiJ. Extracellular thioredoxin and thioredoxin-binding protein 2 in control of cancer. Semin Cancer Biol, 16:444–451. 2006.
133.
NakamuraH, MatsudaM, FurukeK, KitaokaY, IwataS, TodaK, InamotoT, YamaokaY, OzawaK, YodoiJ. Adult T cell leukemia-derived factor/human thioredoxin protects endothelial F-2 cell injury caused by activated neutrophils or hydrogen peroxide. Immunol Lett, 42:75–80. 1994.
134.
NakamuraH, NakamuraK, YodoiJ. Redox regulation of cellular activation. Annu Rev Immunol, 15:351–369. 1997.
135.
NakamuraH, VaageJ, ValenG, PadillaCA, BjornstedtM, HolmgrenA. Measurements of plasma glutaredoxin and thioredoxin in healthy volunteers and during open-heart surgery. Free Radic Biol Med, 24:1176–1186. 1998.
136.
NakamuraT, HoshinoY, YamadaA, TerataniA, FurukawaS, OkuyamaH, UedaS, WadaH, YodoiJ, NakamuraH. Recombinant human thioredoxin-1 becomes oxidized in circulation and suppresses bleomycin-induced neutrophil recruitment in the rat airway. Free Radic Res, 41:1089–1098. 2007.
137.
NishidaK, OtsuK. The role of apoptosis signal-regulating kinase 1 in cardiomyocyte apoptosis. Antioxid Redox Signal, 8:1729–1736. 2006.
138.
NonnL, WilliamsRR, EricksonRP, PowisG. The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol Cell Biol, 23:916–922. 2003.
139.
OkudaM, InoueN, AzumiH, SenoT, SumiY, HirataK, KawashimaS, HayashiY, ItohH, YodoiJ, YokoyamaM. Expression of glutaredoxin in human coronary arteries: its potential role in antioxidant protection against atherosclerosis. Arterioscler Thromb Vasc Biol, 21:1483–1487. 2001.
140.
PaiHV, StarkeDW, LesnefskyEJ, HoppelCL, MieyalJJ. What is the functional significance of the unique location of glutaredoxin 1 (GRx1) in the intermembrane space of mitochondria?Antioxid Redox Signal, 9:2027–2033. 2007.
141.
PappasAC, ZoidisE, SuraiPF, ZervasG. Selenoproteins and maternal nutrition. Comp Biochem Physiol B Biochem Mol Biol, 151:361–372. 2008.
142.
ParkAM, SuzukiYJ. Effects of intermittent hypoxia on oxidative stress-induced myocardial damage in mice. J Appl Physiol, 102:1806–1814. 2007.
143.
PatwariP, LeeRT. Thioredoxins, mitochondria, and hypertension. Am J Pathol, 170:805–808. 2007.
PeltoniemiMJ, RytilaPH, HarjuTH, SoiniYM, SalmenkiviKM, RuddockLW, KinnulaVL. Modulation of glutaredoxin in the lung and sputum of cigarette smokers and chronic obstructive pulmonary disease. Respir Res, 7:133. 2006.
146.
PeterF, Nguyen VanP, SolingHD. Different sorting of Lys-Asp-Glu-Leu proteins in rat liver. J Biol Chem, 267:10631–10637. 1992.
147.
PimentelDR, AdachiT, IdoY, HeibeckT, JiangB, LeeY, MelendezJA, CohenRA, ColucciWS. Strain-stimulated hypertrophy in cardiac myocytes is mediated by reactive oxygen species-dependent Ras S-glutathiolation. J Mol Cell Cardiol, 41:613–622. 2006.
148.
RabilloudT, HellerM, GasnierF, LucheS, ReyC, AebersoldR, BenahmedM, LouisotP, LunardiJ. Proteomics analysis of cellular response to oxidative stress: evidence for in vivo overoxidation of peroxiredoxins at their active site. J Biol Chem, 277:19396–19401. 2002.
149.
RheeSG, ChaeHZ, KimK. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med, 38:1543–1552. 2005.
150.
RheeSG, KangSW, ChangTS, JeongW, KimK. Peroxiredoxin, a novel family of peroxidases. IUBMB Life, 52:35–41. 2001.
151.
RheeSG, KimKH, ChaeHZ, YimMB, UchidaK, NettoLE, StadtmanER. Antioxidant defense mechanisms: a new thiol-specific antioxidant enzyme. Ann N Y Acad Sci, 738:86–92. 1994.
152.
RouhierN, GelhayeE, JacquotJP. Glutaredoxin-dependent peroxiredoxin from poplar: protein-protein interaction and catalytic mechanism. J Biol Chem, 277:13609–13614. 2002.
153.
RundlofAK, ArnerES. Regulation of the mammalian selenoprotein thioredoxin reductase 1 in relation to cellular phenotype, growth, and signaling events. Antioxid Redox Signal, 6:41–52. 2004.
154.
SadekCM, DamdimopoulosAE, Pelto-HuikkoM, GustafssonJA, SpyrouG, Miranda-VizueteA. Sptrx-2, a fusion protein composed of one thioredoxin and three tandemly repeated NDP-kinase domains is expressed in human testis germ cells. Genes Cells, 6:1077–1090. 2001.
155.
SadekCM, JimenezA, DamdimopoulosAE, KieselbachT, NordM, GustafssonJA, SpyrouG, DavisEC, OkoR, van der HoornFA, Miranda-VizueteA. Characterization of human thioredoxin-like 2: a novel microtubule-binding thioredoxin expressed predominantly in the cilia of lung airway epithelium and spermatid manchette and axoneme. J Biol Chem, 278:13133–13142. 2003.
156.
SaitohM, NishitohH, FujiiM, TakedaK, TobiumeK, SawadaY, KawabataM, MiyazonoK, IchijoH. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J, 17:2596–2606. 1998.
157.
SamarelAM. PICOT: a multidomain scaffolding inhibitor of hypertrophic signal transduction. Circ Res, 102:625–627. 2008.
158.
SatohM, MatterCM, OgitaH, TakeshitaK, WangCY, DornGW2nd, LiaoJK. Inhibition of apoptosis-regulated signaling kinase-1 and prevention of congestive heart failure by estrogen. Circulation, 115:3197–3204. 2007.
159.
SchulzePC, De KeulenaerGW, YoshiokaJ, KassikKA, LeeRT. Vitamin D3-upregulated protein-1 (VDUP-1) regulates redox-dependent vascular smooth muscle cell proliferation through interaction with thioredoxin. Circ Res, 91:689–695. 2002.
160.
SeoMS, KangSW, KimK, BainesIC, LeeTH, RheeSG. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem, 275:20346–20354. 2000.
161.
SheltonMD, MieyalJJ. Regulation by reversible S-glutathionylation: molecular targets implicated in inflammatory diseases. Mol Cells, 25:332–346. 2008.
162.
ShiojiK, KishimotoC, NakamuraH, MasutaniH, YuanZ, OkaS, YodoiJ. Overexpression of thioredoxin-1 in transgenic mice attenuates Adriamycin-induced cardiotoxicity. Circulation, 106:1403–1409. 2002.
163.
ShiojiK, NakamuraH, MasutaniH, YodoiJ. Redox regulation by thioredoxin in cardiovascular diseases. Antioxid Redox Signal, 5:795–802. 2003.
164.
ShorroshBS, DixonRA. Molecular characterization and expression of an alfalfa protein with sequence similarity to mammalian ERp72, a glucose-regulated endoplasmic reticulum protein containing active site sequences of protein disulphide isomerase. Plant J, 2:51–58. 1992.
SongJJ, RheeJG, SuntharalingamM, WalshSA, SpitzDR, LeeYJ. Role of glutaredoxin in metabolic oxidative stress: glutaredoxin as a sensor of oxidative stress mediated by H2O2. J Biol Chem, 277:46566–46575. 2002.
167.
SpyrouG, EnmarkE, Miranda-VizueteA, GustafssonJ. Cloning and expression of a novel mammalian thioredoxin. J Biol Chem, 272:2936–2941. 1997.
168.
SunQA, KirnarskyL, ShermanS, GladyshevVN. Selenoprotein oxidoreductase with specificity for thioredoxin and glutathione systems. Proc Natl Acad Sci U S A, 98:3673–3678. 2001.
169.
SunQA, ZappacostaF, FactorVM, WirthPJ, HatfieldDL, GladyshevVN. Heterogeneity within animal thioredoxin reductases: evidence for alternative first exon splicing. J Biol Chem, 276:3106–3114. 2001.
170.
TagayaY, MaedaY, MitsuiA, KondoN, MatsuiH, HamuroJ, BrownN, AraiK, YokotaT, WakasugiH, YodoiJ. ATL-derived factor (ADF), an IL-2 receptor/Tac inducer homologous to thioredoxin; possible involvement of dithiol-reduction in the IL-2 receptor induction. EMBO J, 8:757–764. 1989.
171.
TamakiH, NakamuraH, NishioA, NakaseH, UenoS, UzaN, KidoM, InoueS, MikamiS, AsadaM, KiriyaK, KitamuraH, OhashiS, FukuiT, KawasakiK, MatsuuraM, IshiiY, OkazakiK, YodoiJ, ChibaT. Human thioredoxin-1 ameliorates experimental murine colitis in association with suppressed macrophage inhibitory factor production. Gastroenterology, 131:1110–1121. 2006.
TaoL, GaoE, BryanNS, QuY, LiuHR, HuA, ChristopherTA, LopezBL, YodoiJ, KochWJ, FeelischM, MaXL. Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: role of S-nitrosation [corrected]Proc Natl Acad Sci U S A, 101:11471–11476. 2004.
UrataY, IharaY, MurataH, GotoS, KojiT, YodoiJ, InoueS, KondoT. 17Beta-estradiol protects against oxidative stress-induced cell death through the glutathione/glutaredoxin-dependent redox regulation of Akt in myocardiac H9c2 cells. J Biol Chem, 281:13092–13102. 2006.
183.
UwayamaJ, HirayamaA, YanagawaT, WarabiE, SugimotoR, ItohK, YamamotoM, YoshidaH, KoyamaA, IshiiT. Tissue Prx I in the protection against Fe-NTA and the reduction of nitroxyl radicals. Biochem Biophys Res Commun, 339:226–231. 2006.
184.
VergauwenB, PauwelsF, JacquemotteF, MeyerTE, CusanovichMA, BartschRG, Van BeeumenJJ. Characterization of glutathione amide reductase from Chromatium gracile: identification of a novel thiol peroxidase (Prx/Grx) fueled by glutathione amide redox cycling. J Biol Chem, 276:20890–20897. 2001.
185.
VogelsteinB, LaneD, LevineAJ. Surfing the p53 network. Nature, 408:307–310. 2000.
186.
WahlgrenCM, PekkariK. Elevated thioredoxin after angioplasty in peripheral arterial disease. Eur J Vasc Endovasc Surg, 29:281–286. 2005.
187.
WatabeS, HiroiT, YamamotoY, FujiokaY, HasegawaH, YagoN, TakahashiSY. SP-22 is a thioredoxin-dependent peroxide reductase in mitochondria. Eur J Biochem, 249:52–60. 1997.
188.
WatsonWH, PohlJ, MontfortWR, StuchlikO, ReedMS, PowisG, JonesDP. Redox potential of human thioredoxin 1 and identification of a second dithiol/disulfide motif. J Biol Chem, 278:33408–33415. 2003.
189.
WhiteDW, GilmoreTD. Transcription factors, oncogenes, and apoptosis. Science, 276:185. 1997.
WitteS, VillalbaM, BiK, LiuY, IsakovN, AltmanA. Inhibition of the c-Jun N-terminal kinase/AP-1 and NF-kappaB pathways by PICOT, a novel protein kinase C-interacting protein with a thioredoxin homology domain. J Biol Chem, 275:1902–1909. 2000.
192.
WorldC, BerkB. Reactive oxygen species-mediated regulation of thioredoxin translocation in vascular smooth muscle cells. Vasc Pharmacol, 45:188–188. 2006.
193.
WrammertJ, KallbergE, LeandersonT. Identification of a novel thioredoxin-related protein, PC-TRP, which is preferentially expressed in plasma cells. Eur J Immunol, 34:137–146. 2004.
194.
YamamotoM, YangG, HongC, LiuJ, HolleE, YuX, WagnerT, VatnerSF, SadoshimaJ. Inhibition of endogenous thioredoxin in the heart increases oxidative stress and cardiac hypertrophy. J Clin Invest, 112:1395–1406. 2003.
195.
YangCS, LeeDS, SongCH, AnSJ, LiS, KimJM, KimCS, YooDG, JeonBH, YangHY, LeeTH, LeeZW, El-BennaJ, YuDY, JoEK. Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxin-induced lethal shock. J Exp Med, 204:583–594. 2007.
196.
YangKS, KangSW, WooHA, HwangSC, ChaeHZ, KimK, RheeSG. Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J Biol Chem, 277:38029–38036. 2002.
YodoiJ, TagayaY, OkadaM, TaniguchiY, HirataM, NaramuraM, MaedaM. Interleukin-2 receptor-inducing factor(s) in adult T cell leukemia. Acta Haematol, 78,suppl 1:56–63. 1987.
199.
YodoiJ, TakatsukiK, MasudaT. Letter: Two cases of T-cell chronic lymphocytic leukemia in Japan. N Engl J Med, 290:572–573. 1974.
200.
YoshidaY, YoshikawaA, KinumiT, OgawaY, SaitoY, OharaK, YamamotoH, ImaiY, NikiE. Hydroxyoctadecadienoic acid and oxidatively modified peroxiredoxins in the blood of Alzheimer's disease patients and their potential as biomarkers. Neurobiol Aging, 30:174–185. 2009.
201.
YoshiokaJ, SchulzePC, CupesiM, SylvanJD, MacGillivrayC, GannonJ, HuangH, LeeRT. Thioredoxin-interacting protein controls cardiac hypertrophy through regulation of thioredoxin activity. Circulation, 109:2581–2586. 2004.
ZhangH, LuoY, ZhangW, HeY, DaiS, ZhangR, HuangY, BernatchezP, GiordanoFJ, ShadelG, SessaWC, MinW. Endothelial-specific expression of mitochondrial thioredoxin improves endothelial cell function and reduces atherosclerotic lesions. Am J Pathol, 170:1108–1120. 2007.
204.
ZhangJ, LiYD, PatelJM, BlockER. Thioredoxin overexpression prevents NO-induced reduction of NO synthase activity in lung endothelial cells. Am J Physiol, 275:L288–L293. 1998.
205.
ZhangR, Al-LamkiR, BaiL, StrebJW, MianoJM, BradleyJ, MinW. Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner. Circ Res, 94:1483–1491. 2004.
206.
ZhongL, ArnerES, HolmgrenA. Structure and mechanism of mammalian thioredoxin reductase: the active site is a redox-active selenolthiol/selenenylsulfide formed from the conserved cysteine-selenocysteine sequence. Proc Natl Acad Sci U S A, 97:5854–5859. 2000.
207.
ZhongL, ArnerES, LjungJ, AslundF, HolmgrenA. Rat and calf thioredoxin reductase are homologous to glutathione reductase with a carboxyl-terminal elongation containing a conserved catalytically active penultimate selenocysteine residue. J Biol Chem, 273:8581–8591. 1998.
208.
ZhongL, HolmgrenA. Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J Biol Chem, 275:18121–18128. 2000.
209.
ZhouY, KokKH, ChunAC, WongCM, WuHW, LinMC, FungPC, KungH, JinDY. Mouse peroxiredoxin V is a thioredoxin peroxidase that inhibits p53-induced apoptosis. Biochem Biophys Res Commun, 268:921–927. 2000.
