Thiol-based redox-active proteins as cardioprotective therapeutic agents in cardiovascular diseases

Abstract

Thiol-based redox compounds, namely thioredoxins (Trxs), glutaredoxins (Grxs) and peroxiredoxins (Prxs), stand as a pivotal group of proteins involved in antioxidant processes and redox signaling. Glutaredoxins (Grxs) are considered as one of the major families of proteins involved in redox regulation by removal of S-glutathionylation and thereby reactivation of other enzymes with thiol-dependent activity. Grxs are also coupled to Trxs and Prxs recycling and thereby indirectly contribute to reactive oxygen species (ROS) detoxification. Peroxiredoxins (Prxs) are a ubiquitous family of peroxidases, which play an essential role in the detoxification of hydrogen peroxide, aliphatic and aromatic hydroperoxides, and peroxynitrite. The Trxs, Grxs and Prxs systems, which reversibly induce thiol modifications, regulate redox signaling involved in various biological events in the cardiovascular system. This review focuses on the current knowledge of the role of Trxs, Grxs and Prxs on cardiovascular pathologies and especially in cardiac hypertrophy, ischemia/reperfusion (I/R) injury and heart failure as well as in the presence of cardiovascular risk factors, such as hypertension, hyperlipidemia, hyperglycemia and metabolic syndrome. Further studies on the roles of thiol-dependent redox systems in the cardiovascular system will support the development of novel protective and therapeutic strategies against cardiovascular diseases.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Availability of data and materials

Not applicable.

Code availability

Not applicable.

References

  1. 1.

    Abbasi A, Corpeleijn E, Postmus D, Gansevoort RT, de Jong PE, Gans RO, Struck J, Schulte J, Hillege HL, van der Harst P, Peelen LM, Beulens JW, Stolk RP, Navis G, Bakker SJ (2012) Peroxiredoxin 4, a novel circulating biomarker for oxidative stress and the risk of incident cardiovascular disease and all-cause mortality. J Am Heart Assoc 1:e002956. https://doi.org/10.1161/JAHA.112.002956

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Adluri R, Samuel SM, Thirunavukkarasu M, Muang-In S, Zhan LJ, Akita Y, Ho YS, Maulik N (2009) In vivo angiogenic and anti-apoptotic signaling of Trx1 against acute myocardial infarction: an insight with transgenic mice overexpressing Trx1. Circulation 120:S1128–S1128

    Google Scholar 

  3. 3.

    Adluri RS, Thirunavukkarasu M, Zhan L, Dunna NR, Akita Y, Selvaraju V, Otani H, Sanchez JA, Ho YS, Maulik N (2012) Glutaredoxin-1 overexpression enhances neovascularization and diminishes ventricular remodeling in chronic myocardial infarction. PLoS ONE 7:e34790. https://doi.org/10.1371/journal.pone.0034790

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J (2010) Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res 106:1253–1264. https://doi.org/10.1161/CIRCRESAHA.109.213116

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Ago T, Sadoshima J (2007) Thioredoxin1 as a negative regulator of cardiac hypertrophy. Antioxid Redox Signal 9:679–687. https://doi.org/10.1089/ars.2007.1529

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Ahsan MK, Lekli I, Ray D, Yodoi J, Das DK (2009) Redox regulation of cell survival by the thioredoxin superfamily: an implication of redox gene therapy in the heart. Antioxid Redox Signal 11:2741–2758. https://doi.org/10.1089/ARS.2009.2683

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Andreadou I, Iliodromitis EK, Lazou A, Gorbe A, Giricz Z, Schulz R, Ferdinandy P (2017) Effect of hypercholesterolaemia on myocardial function, ischaemia-reperfusion injury and cardioprotection by preconditioning, postconditioning and remote conditioning. Br J Pharmacol 174:1555–1569. https://doi.org/10.1111/bph.13704

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Andreadou I, Iliodromitis EK, Szabo C, Papapetropoulos A (2015) Hydrogen sulfide and PKG in ischemia-reperfusion injury: sources, signaling, accelerators and brakes. Basic Res Cardiol 110:510. https://doi.org/10.1007/s00395-015-0510-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Andreadou I, Schulz R, Papapetropoulos A, Turan B, Ytrehus K, Ferdinandy P, Daiber A, Di Lisa F (2020) The role of mitochondrial reactive oxygen species, NO and H2 S in ischaemia/reperfusion injury and cardioprotection. J Cell Mol Med 24:6510–6522. https://doi.org/10.1111/jcmm.15279

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Arkat S, Umbarkar P, Singh S, Sitasawad SL (2016) Mitochondrial Peroxiredoxin-3 protects against hyperglycemia induced myocardial damage in Diabetic cardiomyopathy. Free Radic Biol Med 97:489–500. https://doi.org/10.1016/j.freeradbiomed.2016.06.019

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483–495. https://doi.org/10.1016/j.cell.2005.02.001

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Beer SM, Taylor ER, Brown SE, Dahm CC, Costa NJ, Runswick MJ, Murphy MP (2004) 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. https://doi.org/10.1074/jbc.M408011200

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Benhar M, Thompson JW, Moseley MA, Stamler JS (2010) Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry 49:6963–6969. https://doi.org/10.1021/bi100619k

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Berndt C, Lillig CH, Holmgren A (2007) Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am J Physiol Heart Circ Physiol 292:H1227-1236. https://doi.org/10.1152/ajpheart.01162.2006

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Beyrath J, Pellegrini M, Renkema H, Houben L, Pecheritsyna S, van Zandvoort P, van den Broek P, Bekel A, Eftekhari P, Smeitink JAM (2018) KH176 safeguards mitochondrial diseased cells from redox stress-induced cell death by interacting with the thioredoxin system/peroxiredoxin enzyme machinery. Sci Rep 8:6577. https://doi.org/10.1038/s41598-018-24900-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Bibli SI, Andreadou I, Chatzianastasiou A, Tzimas C, Sanoudou D, Kranias E, Brouckaert P, Coletta C, Szabo C, Kremastinos DT, Iliodromitis EK, Papapetropoulos A (2015) Cardioprotection by H2S engages a cGMP-dependent protein kinase G/phospholamban pathway. Cardiovasc Res 106:432–442. https://doi.org/10.1093/cvr/cvv129

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Bibli SI, Papapetropoulos A, Iliodromitis EK, Daiber A, Randriamboavonjy V, Steven S, Brouckaert P, Chatzianastasiou A, Kypreos KE, Hausenloy DJ, Fleming I, Andreadou I (2019) Nitroglycerine limits infarct size through S-nitrosation of cyclophilin D: a novel mechanism for an old drug. Cardiovasc Res 115:625–636. https://doi.org/10.1093/cvr/cvy222

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Boengler K, Buechert A, Heinen Y, Roeskes C, Hilfiker-Kleiner D, Heusch G, Schulz R (2008) Cardioprotection by ischemic postconditioning is lost in aged and STAT3-deficient mice. Circ Res 102:131–135. https://doi.org/10.1161/CIRCRESAHA.107.164699

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Boengler K, Schluter KD, Schermuly RT, Schulz R (2020) Cardioprotection in right heart failure. Br J Pharmacol 177:5413–5431. https://doi.org/10.1111/bph.14992

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Botker HE, Cabrera-Fuentes HA, Ruiz-Meana M, Heusch G, Ovize M (2020) Translational issues for mitoprotective agents as adjunct to reperfusion therapy in patients with ST-segment elevation myocardial infarction. J Cell Mol Med 24:2717–2729. https://doi.org/10.1111/jcmm.14953

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Botker HE, Hausenloy D, Andreadou I, Antonucci S, Boengler K, Davidson SM, Deshwal S, Devaux Y, Di Lisa F, Di Sante M, Efentakis P, Femmino S, Garcia-Dorado D, Giricz Z, Ibanez B, Iliodromitis E, Kaludercic N, Kleinbongard P, Neuhauser M, Ovize M, Pagliaro P, Rahbek-Schmidt M, Ruiz-Meana M, Schluter KD, Schulz R, Skyschally A, Wilder C, Yellon DM, Ferdinandy P, Heusch G (2018) Practical guidelines for rigor and reproducibility in preclinical and clinical studies on cardioprotection. Basic Res Cardiol 113:39. https://doi.org/10.1007/s00395-018-0696-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Brand MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45:466–472. https://doi.org/10.1016/j.exger.2010.01.003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Brandt M, Garlapati V, Oelze M, Sotiriou E, Knorr M, Kroller-Schon S, Kossmann S, Schonfelder T, Morawietz H, Schulz E, Schultheiss HP, Daiber A, Munzel T, Wenzel P (2016) NOX2 amplifies acetaldehyde-mediated cardiomyocyte mitochondrial dysfunction in alcoholic cardiomyopathy. Sci Rep 6:32554. https://doi.org/10.1038/srep32554

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Brixius K, Schwinger RH, Hoyer F, Napp A, Renner R, Bolck B, Kumin A, Fischer U, Mehlhorn U, Werner S, Bloch W (2007) Isoform-specific downregulation of peroxiredoxin in human failing myocardium. Life Sci 81:823–831. https://doi.org/10.1016/j.lfs.2007.07.014

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Brot N, Weissbach H (1983) Biochemistry and physiological role of methionine sulfoxide residues in proteins. Arch Biochem Biophys 223:271–281. https://doi.org/10.1016/0003-9861(83)90592-1

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Buettner GR, Wagner BA, Rodgers VG (2013) Quantitative redox biology: an approach to understand the role of reactive species in defining the cellular redox environment. Cell Biochem Biophys 67:477–483. https://doi.org/10.1007/s12013-011-9320-3

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Burns M, Rizvi SHM, Tsukahara Y, Pimentel DR, Luptak I, Hamburg NM, Matsui R, Bachschmid MM (2020) Role of glutaredoxin-1 and glutathionylation in cardiovascular diseases. Int J Mol Sci. https://doi.org/10.3390/ijms21186803

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Cadete VJ, Lin HB, Sawicka J, Wozniak M, Sawicki G (2012) Proteomic analysis of right and left cardiac ventricles under aerobic conditions and after ischemia/reperfusion. Proteomics 12:2366–2377. https://doi.org/10.1002/pmic.201100604

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Canton M, Skyschally A, Menabo R, Boengler K, Gres P, Schulz R, Haude M, Erbel R, Di Lisa F, Heusch G (2006) Oxidative modification of tropomyosin and myocardial dysfunction following coronary microembolization. Eur Heart J 27:875–881. https://doi.org/10.1093/eurheartj/ehi751

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Carretero A, Gomez-Cabrera MC, Rios-Navarro C, Salvador-Pascual A, Bodi V, Vina J (2020) Early reductive stress and late onset overexpression of antioxidant enzymes in experimental myocardial infarction. Free Radic Res 54:173–184. https://doi.org/10.1080/10715762.2020.1735632

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Chang TS, Cho CS, Park S, Yu S, Kang SW, Rhee SG (2004) Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria. J Biol Chem 279:41975–41984. https://doi.org/10.1074/jbc.M407707200

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Chatzianastasiou A, Bibli SI, Andreadou I, Efentakis P, Kaludercic N, Wood ME, Whiteman M, Di Lisa F, Daiber A, Manolopoulos VG, Szabo C, Papapetropoulos A (2016) Cardioprotection by H2S donors: nitric oxide-dependent and independent mechanisms. J Pharmacol Exp Ther 358:431–440. https://doi.org/10.1124/jpet.116.235119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Chen CA, De Pascali F, Basye A, Hemann C, Zweier JL (2013) Redox modulation of endothelial nitric oxide synthase by glutaredoxin-1 through reversible oxidative post-translational modification. Biochemistry 52:6712–6723. https://doi.org/10.1021/bi400404s

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Chen CA, Wang TY, Varadharaj S, Reyes LA, Hemann C, Talukder MA, Chen YR, Druhan LJ, Zweier JL (2010) S-glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 468:1115–1118. https://doi.org/10.1038/nature09599

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Chen CH, Budas GR, Churchill EN, Disatnik MH, Hurley TD, Mochly-Rosen D (2008) Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science 321:1493–1495. https://doi.org/10.1126/science.1158554

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Chen Q, Thompson J, Hu Y, Das A, Lesnefsky EJ (2019) Cardiac specific knockout of p53 decreases ER stress-induced mitochondrial damage. Front Cardiovasc Med 6:10. https://doi.org/10.3389/fcvm.2019.00010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Chen Q, Thompson J, Hu Y, Lesnefsky EJ (2020) Cardiomyocyte specific deletion of p53 decreases cell injury during ischemia-reperfusion: role of Mitochondria. Free Radic Biol Med 158:162–170. https://doi.org/10.1016/j.freeradbiomed.2020.06.006

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Chiao YA, Zamilpa R, Lopez EF, Dai Q, Escobar GP, Hakala K, Weintraub ST, Lindsey ML (2010) In vivo matrix metalloproteinase-7 substrates identified in the left ventricle post-myocardial infarction using proteomics. J Proteome Res 9:2649–2657. https://doi.org/10.1021/pr100147r

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Chouchani ET, Methner C, Nadtochiy SM, Logan A, Pell VR, Ding S, James AM, Cocheme HM, Reinhold J, Lilley KS, Partridge L, Fearnley IM, Robinson AJ, Hartley RC, Smith RA, Krieg T, Brookes PS, Murphy MP (2013) Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I. Nat Med 19:753–759. https://doi.org/10.1038/nm.3212

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Cieniewski-Bernard C, Mulder P, Henry JP, Drobecq H, Dubois E, Pottiez G, Thuillez C, Amouyel P, Richard V, Pinet F (2008) Proteomic analysis of left ventricular remodeling in an experimental model of heart failure. J Proteome Res 7:5004–5016. https://doi.org/10.1021/pr800409u

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Cochain C, Channon KM, Silvestre JS (2013) Angiogenesis in the infarcted myocardium. Antioxid Redox Signal 18:1100–1113. https://doi.org/10.1089/ars.2012.4849

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Crow MT, Mani K, Nam YJ, Kitsis RN (2004) The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 95:957–970. https://doi.org/10.1161/01.RES.0000148632.35500.d9

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Cullingford TE, Wait R, Clerk A, Sugden PH (2006) Effects of oxidative stress on the cardiac myocyte proteome: modifications to peroxiredoxins and small heat shock proteins. J Mol Cell Cardiol 40:157–172. https://doi.org/10.1016/j.yjmcc.2005.10.004

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    D’Annunzio V, Perez V, Boveris A, Gelpi RJ, Poderoso JJ (2016) Role of thioredoxin-1 in ischemic preconditioning, postconditioning and aged ischemic hearts. Pharmacol Res 109:24–31. https://doi.org/10.1016/j.phrs.2016.03.009

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Dai Q, Escobar GP, Hakala KW, Lambert JM, Weintraub ST, Lindsey ML (2008) The left ventricle proteome differentiates middle-aged and old left ventricles in mice. J Proteome Res 7:756–765. https://doi.org/10.1021/pr700685e

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Daiber A, Di Lisa F, Oelze M, Kroller-Schon S, Steven S, Schulz E, Munzel T (2017) Crosstalk of mitochondria with NADPH oxidase via reactive oxygen and nitrogen species signalling and its role for vascular function. Br J Pharmacol 174:1670–1689. https://doi.org/10.1111/bph.13403

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Daiber A, Hahad O, Andreadou I, Steven S, Daub S, Munzel T (2021) Redox-related biomarkers in human cardiovascular disease—classical footprints and beyond. Redox Biol 42:101875. https://doi.org/10.1016/j.redox.2021.101875

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Dalle-Donne I, Colombo G, Gagliano N, Colombo R, Giustarini D, Rossi R, Milzani A (2011) S-glutathiolation in life and death decisions of the cell. Free Radic Res 45:3–15. https://doi.org/10.3109/10715762.2010.515217

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Davidson SM, Ferdinandy P, Andreadou I, Botker HE, Heusch G, Ibanez B, Ovize M, Schulz R, Yellon DM, Hausenloy DJ, Garcia-Dorado D, Action CC (2019) Multitarget strategies to reduce myocardial ischemia/reperfusion injury: JACC review topic of the week. J Am Coll Cardiol 73:89–99. https://doi.org/10.1016/j.jacc.2018.09.086

    Article  PubMed  Google Scholar 

  50. 50.

    Day AM, Brown JD, Taylor SR, Rand JD, Morgan BA, Veal EA (2012) Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival. Mol Cell 45:398–408. https://doi.org/10.1016/j.molcel.2011.11.027

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    de Koning MLY, Assa S, Maagdenberg CG, van Veldhuisen DJ, Pasch A, van Goor H, Lipsic E, van der Harst P (2020) Safety and tolerability of sodium thiosulfate in patients with an acute coronary syndrome undergoing coronary angiography: a dose-escalation safety pilot study (SAFE-ACS). J Interv Cardiol 2020:6014915. https://doi.org/10.1155/2020/6014915

    Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Dekkers DH, Bezstarosti K, Gurusamy N, Luijk K, Verhoeven AJ, Rijkers EJ, Demmers JA, Lamers JM, Maulik N, Das DK (2008) Identification by a differential proteomic approach of the induced stress and redox proteins by resveratrol in the normal and diabetic rat heart. J Cell Mol Med 12:1677–1689. https://doi.org/10.1111/j.1582-4934.2008.00227.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Del Olmo M, Kramer A, Herzel H (2019) A robust model for circadian redox oscillations. Int J Mol Sci. https://doi.org/10.3390/ijms20092368

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Detienne G, De Haes W, Mergan L, Edwards SL, Temmerman L, Van Bael S (2018) Beyond ROS clearance: peroxiredoxins in stress signaling and aging. Ageing Res Rev 44:33–48. https://doi.org/10.1016/j.arr.2018.03.005

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Di Lisa F, Giorgio M, Ferdinandy P, Schulz R (2017) New aspects of p66Shc in ischaemia reperfusion injury and other cardiovascular diseases. Br J Pharmacol 174:1690–1703. https://doi.org/10.1111/bph.13478

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Diedrich M, Tadic J, Mao L, Wacker MA, Nebrich G, Hetzer R, Regitz-Zagrosek V, Klose J (2007) Heart protein expression related to age and sex in mice and humans. Int J Mol Med 20:865–874

    CAS  PubMed  Google Scholar 

  57. 57.

    Dikalov S (2011) Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med 51:1289–1301. https://doi.org/10.1016/j.freeradbiomed.2011.06.033

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Dogar I, Dixon S, Gill R, Young A, Mallay S, Oldford C, Mailloux RJ (2020) C57BL/6J mice upregulate catalase to maintain the hydrogen peroxide buffering capacity of liver mitochondria. Free Radic Biol Med 146:59–69. https://doi.org/10.1016/j.freeradbiomed.2019.10.409

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    Donelson J, Wang Q, Monroe TO, Jiang X, Zhou J, Yu H, Mo Q, Sun Q, Marini JC, Wang X, Nakata PA, Hirschi KD, Wang J, Rodney GG, Wehrens XHT, Cheng N (2019) Cardiac-specific ablation of glutaredoxin 3 leads to cardiac hypertrophy and heart failure. Physiol Rep 7:e14071. https://doi.org/10.14814/phy2.14071

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Dubois-Deruy E, Peugnet V, Turkieh A, Pinet F (2020) Oxidative stress in cardiovascular diseases. Antioxidants (Basel). https://doi.org/10.3390/antiox9090864

    Article  Google Scholar 

  61. 61.

    Dunn LL, Buckle AM, Cooke JP, Ng MK (2010) The emerging role of the thioredoxin system in angiogenesis. Arterioscler Thromb Vasc Biol 30:2089–2098. https://doi.org/10.1161/ATVBAHA.110.209643

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Elko EA, Cunniff B, Seward DJ, Chia SB, Aboushousha R, van de Wetering C, van der Velden J, Manuel A, Shukla A, Heintz NH, Anathy V, van der Vliet A, Janssen-Heininger YMW (2019) Peroxiredoxins and beyond; redox systems regulating lung physiology and disease. Antioxid Redox Signal 31:1070–1091. https://doi.org/10.1089/ars.2019.7752

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Engstrom NE, Holmgren A, Larsson A, Soderhall S (1974) Isolation and characterization of calf liver thioredoxin. J Biol Chem 249:205–210

    CAS  Article  Google Scholar 

  64. 64.

    Faber MJ, Dalinghaus M, Lankhuizen IM, Bezstarosti K, Verhoeven AJ, Duncker DJ, Helbing WA, Lamers JM (2007) Time dependent changes in cytoplasmic proteins of the right ventricle during prolonged pressure overload. J Mol Cell Cardiol 43:197–209. https://doi.org/10.1016/j.yjmcc.2007.05.002

    CAS  Article  PubMed  Google Scholar 

  65. 65.

    Ferdinandy P, Hausenloy DJ, Heusch G, Baxter GF, Schulz R (2014) Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacol Rev 66:1142–1174. https://doi.org/10.1124/pr.113.008300

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    Fernandez-Caggiano M, Schroder E, Cho HJ, Burgoyne J, Barallobre-Barreiro J, Mayr M, Eaton P (2016) Oxidant-induced interprotein disulfide formation in cardiac protein DJ-1 occurs via an interaction with peroxiredoxin 2. J Biol Chem 291:10399–10410. https://doi.org/10.1074/jbc.M115.699850

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Folda A, Citta A, Scalcon V, Cali T, Zonta F, Scutari G, Bindoli A, Rigobello MP (2016) Mitochondrial thioredoxin system as a modulator of cyclophilin D redox state. Sci Rep 6:23071. https://doi.org/10.1038/srep23071

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Fonarow GC, Srikanthan P (2006) Diabetic cardiomyopathy. Endocrinol Metab Clin North Am 35(575–599):ix. https://doi.org/10.1016/j.ecl.2006.05.003

    CAS  Article  Google Scholar 

  69. 69.

    Fukai T, Galis ZS, Meng XP, Parthasarathy S, Harrison DG (1998) Vascular expression of extracellular superoxide dismutase in atherosclerosis. J Clin Invest 101:2101–2111. https://doi.org/10.1172/JCI2105

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Gallogly MM, Shelton MD, Qanungo S, Pai HV, Starke DW, Hoppel CL, Lesnefsky EJ, Mieyal JJ (2010) Glutaredoxin regulates apoptosis in cardiomyocytes via NFkappaB targets Bcl-2 and Bcl-xL: implications for cardiac aging. Antioxid Redox Signal 12:1339–1353. https://doi.org/10.1089/ars.2009.2791

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. 71.

    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. https://doi.org/10.1089/ARS.2008.2291

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Galougahi KK, Liu CC, Garcia A, Fry NA, Hamilton EJ, Rasmussen HH, Figtree GA (2013) Protein kinase-dependent oxidative regulation of the cardiac Na+-K+ pump: evidence from in vivo and in vitro modulation of cell signalling. J Physiol 591:2999–3015. https://doi.org/10.1113/jphysiol.2013.252817

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Gaucher C, Boudier A, Dahboul F, Parent M, Leroy P (2013) S-nitrosation/denitrosation in cardiovascular pathologies: facts and concepts for the rational design of S-nitrosothiols. Curr Pharm Des 19:458–472

    CAS  Article  Google Scholar 

  74. 74.

    Giordano FJ (2005) Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115:500–508

    CAS  Article  Google Scholar 

  75. 75.

    Godoy JR, Funke M, Ackermann W, Haunhorst P, Oesteritz S, Capani F, Elsasser HP, Lillig CH (2011) Redox atlas of the mouse. Immunohistochemical detection of glutaredoxin-, peroxiredoxin-, and thioredoxin-family proteins in various tissues of the laboratory mouse. Biochim Biophys Acta 1810:2–92. https://doi.org/10.1016/j.bbagen.2010.05.006

    CAS  Article  PubMed  Google Scholar 

  76. 76.

    Gout I (2018) Coenzyme A, protein CoAlation and redox regulation in mammalian cells. Biochem Soc Trans 46:721–728. https://doi.org/10.1042/BST20170506

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Griendling KK, FitzGerald GA (2003) Oxidative stress and cardiovascular injury: Part II: animal and human studies. Circulation 108:2034–2040

    Article  Google Scholar 

  78. 78.

    Grippo JF, Holmgren A, Pratt WB (1985) Proof that the endogenous, heat-stable glucocorticoid receptor-activating factor is thioredoxin. J Biol Chem 260:93–97

    CAS  Article  Google Scholar 

  79. 79.

    Guo W, Liu X, Li J, Shen Y, Zhou Z, Wang M, Xie Y, Feng X, Wang L, Wu X (2018) Prdx1 alleviates cardiomyocyte apoptosis through ROS-activated MAPK pathway during myocardial ischemia/reperfusion injury. Int J Biol Macromol 112:608–615. https://doi.org/10.1016/j.ijbiomac.2018.02.009

    CAS  Article  PubMed  Google Scholar 

  80. 80.

    Haendeler J, Popp R, Goy C, Tischler V, Zeiher AM, Dimmeler S (2005) Cathepsin D and H2O2 stimulate degradation of thioredoxin-1: implication for endothelial cell apoptosis. J Biol Chem 280:42945–42951. https://doi.org/10.1074/jbc.M506985200

    CAS  Article  PubMed  Google Scholar 

  81. 81.

    Hampton MB, Vick KA, Skoko JJ, Neumann CA (2018) Peroxiredoxin involvement in the initiation and progression of human cancer. Antioxid Redox Signal 28:591–608. https://doi.org/10.1089/ars.2017.7422

    CAS  Article  PubMed  Google Scholar 

  82. 82.

    Han J, Weisbrod RM, Shao D, Watanabe Y, Yin X, Bachschmid MM, Seta F, Janssen-Heininger YMW, Matsui R, Zang M, Hamburg NM, Cohen RA (2016) The redox mechanism for vascular barrier dysfunction associated with metabolic disorders: glutathionylation of Rac1 in endothelial cells. Redox Biol 9:306–319. https://doi.org/10.1016/j.redox.2016.09.003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Hattori F, Murayama N, Noshita T, Oikawa S (2003) Mitochondrial peroxiredoxin-3 protects hippocampal neurons from excitotoxic injury in vivo. J Neurochem 86:860–868. https://doi.org/10.1046/j.1471-4159.2003.01918.x

    CAS  Article  PubMed  Google Scholar 

  84. 84.

    Hausenloy DJ, Barrabes JA, Botker HE, Davidson SM, Di Lisa F, Downey J, Engstrom T, Ferdinandy P, Carbrera-Fuentes HA, Heusch G, Ibanez B, Iliodromitis EK, Inserte J, Jennings R, Kalia N, Kharbanda R, Lecour S, Marber M, Miura T, Ovize M, Perez-Pinzon MA, Piper HM, Przyklenk K, Schmidt MR, Redington A, Ruiz-Meana M, Vilahur G, Vinten-Johansen J, Yellon DM, Garcia-Dorado D (2016) Ischaemic conditioning and targeting reperfusion injury: a 30 year voyage of discovery. Basic Res Cardiol 111:70. https://doi.org/10.1007/s00395-016-0588-8

    Article  PubMed  PubMed Central  Google Scholar 

  85. 85.

    Hausenloy DJ, Schulz R, Girao H, Kwak BR, De Stefani D, Rizzuto R, Bernardi P, Di Lisa F (2020) Mitochondrial ion channels as targets for cardioprotection. J Cell Mol Med 24:7102–7114. https://doi.org/10.1111/jcmm.15341

    Article  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Hayashi S, Hajiro-Nakanishi K, Makino Y, Eguchi H, Yodoi J, Tanaka H (1997) Functional modulation of estrogen receptor by redox state with reference to thioredoxin as a mediator. Nucleic Acids Res 25:4035–4040. https://doi.org/10.1093/nar/25.20.4035

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Heinzel FR, Luo Y, Dodoni G, Boengler K, Petrat F, Di Lisa F, de Groot H, Schulz R, Heusch G (2006) Formation of reactive oxygen species at increased contraction frequency in rat cardiomyocytes. Cardiovasc Res 71:374–382. https://doi.org/10.1016/j.cardiores.2006.05.014

    CAS  Article  PubMed  Google Scholar 

  88. 88.

    Heinzel FR, Luo Y, Li X, Boengler K, Buechert A, Garcia-Dorado D, Di Lisa F, Schulz R, Heusch G (2005) Impairment of diazoxide-induced formation of reactive oxygen species and loss of cardioprotection in connexin 43 deficient mice. Circ Res 97:583–586. https://doi.org/10.1161/01.RES.0000181171.65293.65

    CAS  Article  PubMed  Google Scholar 

  89. 89.

    Hematian S, Siegler MA, Karlin KD (2012) Heme/copper assembly mediated nitrite and nitric oxide interconversion. J Am Chem Soc 134:18912–18915. https://doi.org/10.1021/ja3083818

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Heppner DE, Janssen-Heininger YMW, van der Vliet A (2017) The role of sulfenic acids in cellular redox signaling: reconciling chemical kinetics and molecular detection strategies. Arch Biochem Biophys 616:40–46. https://doi.org/10.1016/j.abb.2017.01.008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Herrero E, de la Torre-Ruiz MA (2007) Monothiol glutaredoxins: a common domain for multiple functions. Cell Mol Life Sci 64:1518–1530. https://doi.org/10.1007/s00018-007-6554-8

    CAS  Article  PubMed  Google Scholar 

  92. 92.

    Heusch G (2015) Molecular basis of cardioprotection: signal transduction in ischemic pre-, post-, and remote conditioning. Circ Res 116:674–699. https://doi.org/10.1161/CIRCRESAHA.116.305348

    CAS  Article  PubMed  Google Scholar 

  93. 93.

    Heusch G (2020) Myocardial ischaemia-reperfusion injury and cardioprotection in perspective. Nat Rev Cardiol 17:773–789. https://doi.org/10.1038/s41569-020-0403-y

    Article  PubMed  Google Scholar 

  94. 94.

    Heusch G (2012) Reduction of infarct size by ischaemic post-conditioning in humans: fact or fiction? Eur Heart J 33:13–15. https://doi.org/10.1093/eurheartj/ehr341

    Article  PubMed  Google Scholar 

  95. 95.

    Heusch P, Canton M, Aker S, van de Sand A, Konietzka I, Rassaf T, Menazza S, Brodde OE, Di Lisa F, Heusch G, Schulz R (2010) The contribution of reactive oxygen species and p38 mitogen-activated protein kinase to myofilament oxidation and progression of heart failure in rabbits. Br J Pharmacol 160:1408–1416. https://doi.org/10.1111/j.1476-5381.2010.00793.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Hiroi M, Nagahara Y, Miyauchi R, Misaki Y, Goda T, Kasezawa N, Sasaki S, Yamakawa-Kobayashi K (2011) The combination of genetic variations in the PRDX3 gene and dietary fat intake contribute to obesity risk. Obesity (Silver Spring) 19:882–887. https://doi.org/10.1038/oby.2010.275

    CAS  Article  Google Scholar 

  97. 97.

    Hirschhauser C, Bornbaum J, Reis A, Bohme S, Kaludercic N, Menabo R, Di Lisa F, Boengler K, Shah AM, Schulz R, Schmidt HH (2015) NOX4 in mitochondria: yeast two-hybrid-based interaction with complex I without relevance for basal reactive oxygen species? Antioxid Redox Signal 23:1106–1112. https://doi.org/10.1089/ars.2014.6238

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  98. 98.

    Ho YS, Xiong Y, Ho DS, Gao J, Chua BH, Pai H, Mieyal JJ (2007) Targeted disruption of the glutaredoxin 1 gene does not sensitize adult mice to tissue injury induced by ischemia/reperfusion and hyperoxia. Free Radic Biol Med 43:1299–1312. https://doi.org/10.1016/j.freeradbiomed.2007.07.025

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  99. 99.

    Holmgren A (1995) Thioredoxin structure and mechanism—conformational-changes on oxidation of the active-site sulfhydryls to a disulfide. Structure 3:239–243. https://doi.org/10.1016/S0969-2126(01)00153-8

    CAS  Article  PubMed  Google Scholar 

  100. 100.

    Holmstrom KM, Finkel T (2014) Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol 15:411–421. https://doi.org/10.1038/nrm3801

    CAS  Article  PubMed  Google Scholar 

  101. 101.

    Hsu YJ, Lin CW, Cho SL, Yang WS, Yang CM, Yang CH (2020) Protective effect of fenofibrate on oxidative stress-induced apoptosis in retinal-choroidal vascular endothelial cells: implication for diabetic retinopathy treatment. Antioxidants (Basel). https://doi.org/10.3390/antiox9080712

    Article  PubMed Central  Google Scholar 

  102. 102.

    Hu C, Zhang H, Qiao Z, Wang Y, Zhang P, Yang D (2018) Loss of thioredoxin 2 alters mitochondrial respiratory function and induces cardiomyocyte hypertrophy. Exp Cell Res 372:61–72. https://doi.org/10.1016/j.yexcr.2018.09.010

    CAS  Article  PubMed  Google Scholar 

  103. 103.

    Huang Q, Zhou HJ, Zhang H, Huang Y, Hinojosa-Kirschenbaum F, Fan P, Yao L, Belardinelli L, Tellides G, Giordano FJ, Budas GR, Min W (2015) Thioredoxin-2 inhibits mitochondrial reactive oxygen species generation and apoptosis stress kinase-1 activity to maintain cardiac function. Circulation 131:1082–1097. https://doi.org/10.1161/CIRCULATIONAHA.114.012725

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  104. 104.

    Huang QH, Xu LY, Huang Y, Zhang HF, Giordano FJ, Min W (2010) Mitochondrial Redox Protein Thioredoxin 2 Is Essential for Preserving Cardiac Function. Circulation 122: A17258

    Article  Google Scholar 

  105. 105.

    Ibarrola J, Arrieta V, Sadaba R, Martinez-Martinez E, Garcia-Pena A, Alvarez V, Fernandez-Celis A, Gainza A, Santamaria E, Fernandez-Irigoyen J, Cachofeiro V, Zalba G, Fay R, Rossignol P, Lopez-Andres N (2018) Galectin-3 down-regulates antioxidant peroxiredoxin-4 in human cardiac fibroblasts: a new pathway to induce cardiac damage. Clin Sci (Lond) 132:1471–1485. https://doi.org/10.1042/CS20171389

    CAS  Article  Google Scholar 

  106. 106.

    Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, Takagi M, Matsumoto K, Miyazono K, Gotoh Y (1997) Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90–94. https://doi.org/10.1126/science.275.5296.90

    CAS  Article  PubMed  Google Scholar 

  107. 107.

    Ida T, Sawa T, Ihara H, Tsuchiya Y, Watanabe Y, Kumagai Y, Suematsu M, Motohashi H, Fujii S, Matsunaga T, Yamamoto M, Ono K, Devarie-Baez NO, Xian M, Fukuto JM, Akaike T (2014) Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc Natl Acad Sci U S A 111:7606–7611. https://doi.org/10.1073/pnas.1321232111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Isakov N, Witte S, Altman A (2000) PICOT-HD: a highly conserved protein domain that is often associated with thioredoxin and glutaredoxin modules. Trends Biochem Sci 25:537–539. https://doi.org/10.1016/S0968-0004(00)01685-6

    CAS  Article  PubMed  Google Scholar 

  109. 109.

    Iwamoto K, Watanabe J (1985) Dose-dependent presystemic elimination of propranolol due to hepatic first-pass metabolism in rats. J Pharm Pharmacol 37:826–828. https://doi.org/10.1111/j.2042-7158.1985.tb04979.x

    CAS  Article  PubMed  Google Scholar 

  110. 110.

    Jakobs P, Serbulea V, Leitinger N, Eckers A, Haendeler J (2017) Nuclear factor (erythroid-derived 2)-like 2 and thioredoxin-1 in atherosclerosis and ischemia/reperfusion injury in the heart. Antioxid Redox Signal 26:630–644. https://doi.org/10.1089/ars.2016.6795

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Jekell A, Hossain A, Alehagen U, Dahlstrom U, Rosen A (2004) Elevated circulating levels of thioredoxin and stress in chronic heart failure. Eur J Heart Fail 6:883–890. https://doi.org/10.1016/j.ejheart.2004.03.003

    CAS  Article  PubMed  Google Scholar 

  112. 112.

    Jin X, Chen C, Li D, Su Q, Hang Y, Zhang P, Hu W (2017) PRDX2 in myocyte hypertrophy and survival is mediated by TLR4 in acute infarcted myocardium. Sci Rep 7:6970. https://doi.org/10.1038/s41598-017-06718-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  113. 113.

    Kaludercic N, Mialet-Perez J, Paolocci N, Parini A, Di Lisa F (2014) Monoamine oxidases as sources of oxidants in the heart. J Mol Cell Cardiol 73:34–42. https://doi.org/10.1016/j.yjmcc.2013.12.032

    CAS  Article  PubMed  Google Scholar 

  114. 114.

    Kanaan GN, Ichim B, Gharibeh L, Maharsy W, Patten DA, Xuan JY, Reunov A, Marshall P, Veinot J, Menzies K, Nemer M, Harper ME (2018) Glutaredoxin-2 controls cardiac mitochondrial dynamics and energetics in mice, and protects against human cardiac pathologies. Redox Biol 14:509–521. https://doi.org/10.1016/j.redox.2017.10.019

    CAS  Article  PubMed  Google Scholar 

  115. 115.

    Kaplan P, Tatarkova Z, Lichardusova L, Kmetova Sivonova M, Tomascova A, Racay P, Lehotsky J (2019) Age-associated changes in antioxidants and redox proteins of rat heart. Physiol Res 68:883–892. https://doi.org/10.33549/physiolres.934170

    CAS  Article  PubMed  Google Scholar 

  116. 116.

    Kariz S, Mankoc S, Petrovic D (2015) Association of thioredoxin reductase 2 (TXNRD2) gene polymorphisms with myocardial infarction in Slovene patients with type 2 diabetes mellitus. Diabetes Res Clin Pract 108:323–328. https://doi.org/10.1016/j.diabres.2015.01.038

    CAS  Article  PubMed  Google Scholar 

  117. 117.

    Karplus PA (2015) A primer on peroxiredoxin biochemistry. Free Radic Biol Med 80:183–190. https://doi.org/10.1016/j.freeradbiomed.2014.10.009

    CAS  Article  PubMed  Google Scholar 

  118. 118.

    Karvounis HI, Papadopoulos CE, Zaglavara TA, Nouskas IG, Gemitzis KD, Parharidis GE, Louridas GE (2004) Evidence of left ventricular dysfunction in asymptomatic elderly patients with non-insulin-dependent diabetes mellitus. Angiology 55:549–555. https://doi.org/10.1177/000331970405500511

    Article  PubMed  Google Scholar 

  119. 119.

    Kihlstrom M (1990) Protection effect of endurance training against reoxygenation-induced injuries in rat heart. J Appl Physiol (1985) 68:1672–1678. https://doi.org/10.1152/jappl.1990.68.4.1672

    CAS  Article  Google Scholar 

  120. 120.

    Kim J, Kim J, Kook H, Park WJ (2017) PICOT alleviates myocardial ischemia-reperfusion injury by reducing intracellular levels of reactive oxygen species. Biochem Biophys Res Commun 485:807–813. https://doi.org/10.1016/j.bbrc.2017.02.136

    CAS  Article  PubMed  Google Scholar 

  121. 121.

    Kim JY, Kim MH, Lee HJ, Huh JW, Lee SR, Lee HS, Lee DS (2020) Peroxiredoxin 4 inhibits insulin-induced adipogenesis through regulation of ER stress in 3T3-L1 cells. Mol Cell Biochem 468:97–109. https://doi.org/10.1007/s11010-020-03714-w

    CAS  Article  PubMed  Google Scholar 

  122. 122.

    Kim Y, Jang HH (2019) Role of cytosolic 2-Cys Prx1 and Prx2 in redox signaling. Antioxidants (Basel). https://doi.org/10.3390/antiox8060169

    Article  PubMed Central  Google Scholar 

  123. 123.

    Kimura Y, Goto Y, Kimura H (2010) Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid Redox Signal 12:1–13. https://doi.org/10.1089/ars.2008.2282

    CAS  Article  PubMed  Google Scholar 

  124. 124.

    Kishimoto C, Shioji K, Nakamura H, Nakayama Y, Yodoi J, Sasayama S (2001) Serum thioredoxin (TRX) levels in patients with heart failure. Jpn Circ J 65:491–494

    CAS  Article  Google Scholar 

  125. 125.

    Klaus A, Zorman S, Berthier A, Polge C, Ramirez S, Michelland S, Seve M, Vertommen D, Rider M, Lentze N, Auerbach D, Schlattner U (2013) Glutathione S-transferases interact with AMP-activated protein kinase: evidence for S-glutathionylation and activation in vitro. PLoS ONE 8:e62497. https://doi.org/10.1371/journal.pone.0062497

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  126. 126.

    Knoops B, Argyropoulou V, Becker S, Ferte L, Kuznetsova O (2016) Multiple roles of peroxiredoxins in inflammation. Mol Cells 39:60–64. https://doi.org/10.14348/molcells.2016.2341

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  127. 127.

    Koneru S, Penumathsa SV, Thirunavukkarasu M, Zhan L, Maulik N (2009) Thioredoxin-1 gene delivery induces heme oxygenase-1 mediated myocardial preservation after chronic infarction in hypertensive rats. Am J Hypertens 22:183–190. https://doi.org/10.1038/ajh.2008.318

    CAS  Article  PubMed  Google Scholar 

  128. 128.

    Kumar V, Kitaeff N, Hampton MB, Cannell MB, Winterbourn CC (2009) Reversible oxidation of mitochondrial peroxiredoxin 3 in mouse heart subjected to ischemia and reperfusion. FEBS Lett 583:997–1000. https://doi.org/10.1016/j.febslet.2009.02.018

    CAS  Article  PubMed  Google Scholar 

  129. 129.

    Kuzuya K, Ichihara S, Suzuki Y, Inoue C, Ichihara G, Kurimoto S, Oikawa S (2018) Proteomics analysis identified peroxiredoxin 2 involved in early-phase left ventricular impairment in hamsters with cardiomyopathy. PLoS ONE 13:e0192624. https://doi.org/10.1371/journal.pone.0192624

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  130. 130.

    Lacerda D, Ortiz V, Turck P, Campos-Carraro C, Zimmer A, Teixeira R, Bianchi S, de Castro AL, Schenkel PC, Bello-Klein A, Bassani VL, da Rosa Araujo AS (2018) Stilbenoid pterostilbene complexed with cyclodextrin preserves left ventricular function after myocardial infarction in rats: possible involvement of thiol proteins and modulation of phosphorylated GSK-3beta. Free Radic Res 52:988–999. https://doi.org/10.1080/10715762.2018.1506115

    CAS  Article  PubMed  Google Scholar 

  131. 131.

    Lacerda D, Turck P, Campos-Carraro C, Hickmann A, Ortiz V, Bianchi S, Bello-Klein A, de Castro AL, Bassani VL, Araujo A (2020) Pterostilbene improves cardiac function in a rat model of right heart failure through modulation of calcium handling proteins and oxidative stress. Appl Physiol Nutr Metab 45:987–995. https://doi.org/10.1139/apnm-2019-0864

    CAS  Article  PubMed  Google Scholar 

  132. 132.

    Lee YJ (2020) Knockout mouse models for peroxiredoxins. Antioxidants (Basel). https://doi.org/10.3390/antiox9020182

    Article  PubMed  PubMed Central  Google Scholar 

  133. 133.

    Leng Y, Wu Y, Lei S, Zhou B, Qiu Z, Wang K, Xia Z (2018) Inhibition of HDAC6 activity alleviates myocardial ischemia/reperfusion injury in diabetic rats: potential role of peroxiredoxin 1 acetylation and redox regulation. Oxid Med Cell Longev 2018:9494052. https://doi.org/10.1155/2018/9494052

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  134. 134.

    Lennon SL, Quindry J, Hamilton KL, French J, Staib J, Mehta JL, Powers SK (2004) Loss of exercise-induced cardioprotection after cessation of exercise. J Appl Physiol (1985) 96:1299–1305. https://doi.org/10.1152/japplphysiol.00920.2003

    Article  Google Scholar 

  135. 135.

    Leu JI, Murphy ME, George DL (2020) Functional interplay among thiol-based redox signaling, metabolism, and ferroptosis unveiled by a genetic variant of TP53. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.2009943117

    Article  PubMed  PubMed Central  Google Scholar 

  136. 136.

    Li H, Xu C, Li Q, Gao X, Sugano E, Tomita H, Yang L, Shi S (2017) Thioredoxin 2 offers protection against mitochondrial oxidative stress in H9c2 cells and against myocardial hypertrophy induced by hyperglycemia. Int J Mol Sci. https://doi.org/10.3390/ijms18091958

    Article  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Li Y, Ren M, Wang X, Cui X, Zhao H, Zhao C, Zhou J, Guo Y, Hu Y, Yan C, Berk B, Wang J (2017) Glutaredoxin 1 mediates the protective effect of steady laminar flow on endothelial cells against oxidative stress-induced apoptosis via inhibiting Bim. Sci Rep 7:15539. https://doi.org/10.1038/s41598-017-15672-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  138. 138.

    Li Y, Xiang Y, Zhang S, Wang Y, Yang J, Liu W, Xue F (2017) Intramyocardial injection of thioredoxin 2-expressing lentivirus alleviates myocardial ischemia-reperfusion injury in rats. Am J Transl Res 9:4428–4439

    CAS  PubMed  PubMed Central  Google Scholar 

  139. 139.

    Li YR, Zhu H, Danelisen I (2020) Role of peroxiredoxins in protecting against cardiovascular and related disorders. Cardiovasc Toxicol 20:448–453. https://doi.org/10.1007/s12012-020-09588-0

    CAS  Article  PubMed  Google Scholar 

  140. 140.

    Li YY, Xiang Y, Zhang S, Wang Y, Yang J, Liu W, Xue FT (2017) Thioredoxin-2 protects against oxygen-glucose deprivation/reperfusion injury by inhibiting autophagy and apoptosis in H9c2 cardiomyocytes. Am J Transl Res 9:1471–1482

    CAS  PubMed  PubMed Central  Google Scholar 

  141. 141.

    Liang LM, Liu Y, Cheng CY, Liu L, Li KL, Li ZL, Liu WJ, Zhang ZH, Huang ZH (2018) Sanguis draconis flavones promotes ischemic tolerance by targeting Prx-6 in myocardial ischemia and reperfusion injury. Int J Clin Exp Med 11:13024–13032

    CAS  Google Scholar 

  142. 142.

    Lillig CH, Berndt C (2013) Glutaredoxins in thiol/disulfide exchange. Antioxid Redox Signal 18:1654–1665. https://doi.org/10.1089/ars.2012.5007

    CAS  Article  PubMed  Google Scholar 

  143. 143.

    Lillig CH, Berndt C, Holmgren A (2008) Glutaredoxin systems. Biochim Biophys Acta 1780:1304–1317. https://doi.org/10.1016/j.bbagen.2008.06.003

    CAS  Article  PubMed  Google Scholar 

  144. 144.

    Liu CC, Fry NA, Hamilton EJ, Chia KK, Garcia A, Karimi Galougahi K, Figtree GA, Clarke RJ, Bundgaard H, Rasmussen HH (2013) Redox-dependent regulation of the Na(+)-K(+) pump: new twists to an old target for treatment of heart failure. J Mol Cell Cardiol 61:94–101. https://doi.org/10.1016/j.yjmcc.2013.05.013

    CAS  Article  PubMed  Google Scholar 

  145. 145.

    Liu F, Su H, Liu B, Mei Y, Ke Q, Sun X, Tan W (2020) STVNa attenuates isoproterenol-induced cardiac hypertrophy response through the HDAC4 and Prdx2/ROS/Trx1 pathways. Int J Mol Sci. https://doi.org/10.3390/ijms21020682

    Article  PubMed  PubMed Central  Google Scholar 

  146. 146.

    Liu X, Liu K, Li C, Cai J, Huang L, Chen H, Wang H, Zou J, Liu M, Wang K, Tan S, Zhang H (2019) Heat-shock protein B1 upholds the cytoplasm reduced state to inhibit activation of the Hippo pathway in H9c2 cells. J Cell Physiol 234:5117–5133. https://doi.org/10.1002/jcp.27322

    CAS  Article  PubMed  Google Scholar 

  147. 147.

    Liu X, Wang L, Cai J, Liu K, Liu M, Wang H, Zhang H (2019) N-acetylcysteine alleviates H2O2-induced damage via regulating the redox status of intracellular antioxidants in H9c2 cells. Int J Mol Med 43:199–208. https://doi.org/10.3892/ijmm.2018.3962

    CAS  Article  PubMed  Google Scholar 

  148. 148.

    Lorenzo O, Ramirez E, Picatoste B, Egido J, Tunon J (2013) Alteration of energy substrates and ROS production in diabetic cardiomyopathy. Mediators Inflamm 2013:461967. https://doi.org/10.1155/2013/461967

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  149. 149.

    Lu J, Holmgren A (2014) The thioredoxin antioxidant system. Free Radic Biol Med 66:75–87. https://doi.org/10.1016/j.freeradbiomed.2013.07.036

    CAS  Article  PubMed  Google Scholar 

  150. 150.

    Lundberg M, Johansson C, Chandra J, Enoksson M, Jacobsson G, Ljung J, Johansson M, Holmgren A (2001) Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J Biol Chem 276:26269–26275. https://doi.org/10.1074/jbc.M011605200

    CAS  Article  PubMed  Google Scholar 

  151. 151.

    Mahal Z, Fujikawa K, Matsuo H, Zahid HM, Koike M, Misumi M, Kaneko T, Mashimo T, Ohara H, Nabika T (2019) Effects of the Prdx2 depletion on blood pressure and life span in spontaneously hypertensive rats. Hypertens Res 42:610–617. https://doi.org/10.1038/s41440-019-0207-9

    CAS  Article  PubMed  Google Scholar 

  152. 152.

    Mailloux RJ (2020) Protein S-glutathionylation reactions as a global inhibitor of cell metabolism for the desensitization of hydrogen peroxide signals. Redox Biol 32:101472. https://doi.org/10.1016/j.redox.2020.101472

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  153. 153.

    Mailloux RJ, Xuan JY, McBride S, Maharsy W, Thorn S, Holterman CE, Kennedy CR, Rippstein P, deKemp R, da Silva J, Nemer M, Lou M, Harper ME (2014) Glutaredoxin-2 is required to control oxidative phosphorylation in cardiac muscle by mediating deglutathionylation reactions. J Biol Chem 289:14812–14828. https://doi.org/10.1074/jbc.M114.550574

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  154. 154.

    Matsui R, Ferran B, Oh A, Croteau D, Shao D, Han J, Pimentel DR, Bachschmid MM (2020) Redox regulation via glutaredoxin-1 and protein S-glutathionylation. Antioxid Redox Signal 32:677–700. https://doi.org/10.1089/ars.2019.7963

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  155. 155.

    Matsui R, Watanabe Y, Murdoch CE (2017) Redox regulation of ischemic limb neovascularization—what we have learned from animal studies. Redox Biol 12:1011–1019. https://doi.org/10.1016/j.redox.2017.04.040

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  156. 156.

    Matsushima S, Ide T, Yamato M, Matsusaka H, Hattori F, Ikeuchi M, Kubota T, Sunagawa K, Hasegawa Y, Kurihara T, Oikawa S, Kinugawa S, Tsutsui H (2006) Overexpression of mitochondrial peroxiredoxin-3 prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation 113:1779–1786. https://doi.org/10.1161/CIRCULATIONAHA.105.582239

    CAS  Article  PubMed  Google Scholar 

  157. 157.

    Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, Hay RT (1992) Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 20:3821–3830. https://doi.org/10.1093/nar/20.15.3821

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  158. 158.

    McBean GJ, Aslan M, Griffiths HR, Torrao RC (2015) Thiol redox homeostasis in neurodegenerative disease. Redox Biol 5:186–194. https://doi.org/10.1016/j.redox.2015.04.004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  159. 159.

    McCommis KS, McGee AM, Laughlin MH, Bowles DK, Baines CP (2011) Hypercholesterolemia increases mitochondrial oxidative stress and enhances the MPT response in the porcine myocardium: beneficial effects of chronic exercise. Am J Physiol Regul Integr Comp Physiol 301:R1250-1258. https://doi.org/10.1152/ajpregu.00841.2010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  160. 160.

    Melino G, Bernassola F, Knight RA, Corasaniti MT, Nistico G, Finazzi-Agro A (1997) S-nitrosylation regulates apoptosis. Nature 388:432–433. https://doi.org/10.1038/41237

    CAS  Article  PubMed  Google Scholar 

  161. 161.

    Meuillet EJ, Mahadevan D, Berggren M, Coon A, Powis G (2004) Thioredoxin-1 binds to the C2 domain of PTEN inhibiting PTEN’s lipid phosphatase activity and membrane binding: a mechanism for the functional loss of PTEN’s tumor suppressor activity. Arch Biochem Biophys 429:123–133. https://doi.org/10.1016/j.abb.2004.04.020

    CAS  Article  PubMed  Google Scholar 

  162. 162.

    Miyamoto M, Kishimoto C, Shioji K, Nakamura H, Toyokuni S, Nakayama Y, Kita M, Yodoi J, Sasayama S (2001) Difference in thioredoxin expression in viral myocarditis in inbred strains of mice. Jpn Circ J 65:561–564

    CAS  Article  Google Scholar 

  163. 163.

    Mochizuki A, Saso A, Zhao Q, Kubo S, Nishida N, Shimada I (2018) Balanced regulation of redox status of intracellular thioredoxin revealed by in-cell NMR. J Am Chem Soc 140:3784–3790. https://doi.org/10.1021/jacs.8b00426

    CAS  Article  PubMed  Google Scholar 

  164. 164.

    Molkentin JD, Dorn GW 2nd (2001) Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu Rev Physiol 63:391–426. https://doi.org/10.1146/annurev.physiol.63.1.391

    CAS  Article  PubMed  Google Scholar 

  165. 165.

    Murata H, Ihara Y, Nakamura H, Yodoi J, Sumikawa K, Kondo T (2003) Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J Biol Chem 278:50226–50233. https://doi.org/10.1074/jbc.M310171200

    CAS  Article  PubMed  Google Scholar 

  166. 166.

    Murdoch CE, Shuler M, Haeussler DJ, Kikuchi R, Bearelly P, Han J, Watanabe Y, Fuster JJ, Walsh K, Ho YS, Bachschmid MM, Cohen RA, Matsui R (2014) Glutaredoxin-1 up-regulation induces soluble vascular endothelial growth factor receptor 1, attenuating post-ischemia limb revascularization. J Biol Chem 289:8633–8644. https://doi.org/10.1074/jbc.M113.517219

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  167. 167.

    Murdoch CE, Zhang M, Cave AC, Shah AM (2006) NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure. Cardiovasc Res 71:208–215

    CAS  Article  Google Scholar 

  168. 168.

    Murphy E, Ardehali H, Balaban RS, DiLisa F, Dorn GW 2nd, Kitsis RN, Otsu K, Ping P, Rizzuto R, Sack MN, Wallace D, Youle RJ, American Heart Association Council on Basic Cardiovascular Sciences CoCC, Council on Functional G, Translational B (2016) Mitochondrial function, biology, and role in disease: a scientific statement from the American heart association. Circ Res 118:1960–1991. https://doi.org/10.1161/RES.0000000000000104

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  169. 169.

    Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13. https://doi.org/10.1042/BJ20081386

    CAS  Article  PubMed  Google Scholar 

  170. 170.

    Nagarajan N, Oka S, Sadoshima J (2017) Modulation of signaling mechanisms in the heart by thioredoxin 1. Free Radic Biol Med 109:125–131. https://doi.org/10.1016/j.freeradbiomed.2016.12.020

    CAS  Article  PubMed  Google Scholar 

  171. 171.

    Nagy N, Malik G, Fisher AB, Das DK (2006) Targeted disruption of peroxiredoxin 6 gene renders the heart vulnerable to ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 291:H2636-2640. https://doi.org/10.1152/ajpheart.00399.2006

    CAS  Article  PubMed  Google Scholar 

  172. 172.

    Nakamura H, Vaage J, Valen G, Padilla CA, Bjornstedt M, Holmgren A (1998) Measurements of plasma glutaredoxin and thioredoxin in healthy volunteers and during open-heart surgery. Free Radic Biol Med 24:1176–1186. https://doi.org/10.1016/s0891-5849(97)00429-2

    CAS  Article  PubMed  Google Scholar 

  173. 173.

    Nguyen TT, Stevens MV, Kohr M, Steenbergen C, Sack MN, Murphy E (2011) Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J Biol Chem 286:40184–40192. https://doi.org/10.1074/jbc.M111.243469

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  174. 174.

    Nonn L, Williams RR, Erickson RP, Powis G (2003) The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol Cell Biol 23:916–922. https://doi.org/10.1128/mcb.23.3.916-922.2003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  175. 175.

    Nordberg J, Arner ESJ (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radical Biol Med 31:1287–1312. https://doi.org/10.1016/S0891-5849(01)00724-9

    CAS  Article  Google Scholar 

  176. 176.

    Oliveira MS, Tanaka LY, Antonio EL, Brandizzi LI, Serra AJ, Dos Santos L, Krieger JE, Laurindo FRM, Tucci PJF (2020) Hyperbaric oxygenation improves redox control and reduces mortality in the acute phase of myocardial infarction in a rat model. Mol Med Rep 21:1431–1438. https://doi.org/10.3892/mmr.2020.10968

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  177. 177.

    Pain T, Yang XM, Critz SD, Yue Y, Nakano A, Liu GS, Heusch G, Cohen MV, Downey JM (2000) Opening of mitochondrial K(ATP) channels triggers the preconditioned state by generating free radicals. Circ Res 87:460–466. https://doi.org/10.1161/01.res.87.6.460

    CAS  Article  PubMed  Google Scholar 

  178. 178.

    Pan S, Berk BC (2007) Glutathiolation regulates tumor necrosis factor-alpha-induced caspase-3 cleavage and apoptosis: key role for glutaredoxin in the death pathway. Circ Res 100:213–219. https://doi.org/10.1161/01.RES.0000256089.30318.20

    CAS  Article  PubMed  Google Scholar 

  179. 179.

    Park KJ, Kim YJ, Kim J, Kim SM, Lee SY, Bae JW, Hwang KK, Kim DW, Cho MC (2012) Protective effects of peroxiredoxin on hydrogen peroxide induced oxidative stress and apoptosis in cardiomyocytes. Korean Circ J 42:23–32. https://doi.org/10.4070/kcj.2012.42.1.23

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  180. 180.

    Parker AR, Petluru PN, Nienaber VL, Badger J, Leverett BD, Jair K, Sridhar V, Logan C, Ayala PY, Kochat H, Hausheer FH (2015) Cysteine specific targeting of the functionally distinct peroxiredoxin and glutaredoxin proteins by the investigational disulfide BNP7787. Molecules 20:4928–4950. https://doi.org/10.3390/molecules20034928

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  181. 181.

    Pastore A, Piemonte F (2013) Protein glutathionylation in cardiovascular diseases. Int J Mol Sci 14:20845–20876. https://doi.org/10.3390/ijms141020845

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  182. 182.

    Penna C, Andreadou I, Aragno M, Beauloye C, Bertrand L, Lazou A, Falcao-Pires I, Bell R, Zuurbier CJ, Pagliaro P, Hausenloy DJ (2020) Effect of hyperglycaemia and diabetes on acute myocardial ischaemia-reperfusion injury and cardioprotection by ischaemic conditioning protocols. Br J Pharmacol 177:5312–5335. https://doi.org/10.1111/bph.14993

    CAS  Article  PubMed  Google Scholar 

  183. 183.

    Perez V, DAnnunzio V, Mazo T, Marchini T, Caceres L, Evelson P, Gelpi RJ (2016) Ischemic postconditioning confers cardioprotection and prevents reduction of Trx-1 in young mice, but not in middle-aged and old mice. Mol Cell Biochem 415:67–76. https://doi.org/10.1007/s11010-016-2677-2

    CAS  Article  PubMed  Google Scholar 

  184. 184.

    Perez VI, Bokov A, Van Remmen H, Mele J, Ran Q, Ikeno Y, Richardson A (2009) Is the oxidative stress theory of aging dead? Biochim Biophys Acta 1790:1005–1014. https://doi.org/10.1016/j.bbagen.2009.06.003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  185. 185.

    Peskin AV, Low FM, Paton LN, Maghzal GJ, Hampton MB, Winterbourn CC (2007) The high reactivity of peroxiredoxin 2 with H(2)O(2) is not reflected in its reaction with other oxidants and thiol reagents. J Biol Chem 282:11885–11892. https://doi.org/10.1074/jbc.M700339200

    CAS  Article  PubMed  Google Scholar 

  186. 186.

    Pimentel DR, Adachi T, Ido Y, Heibeck T, Jiang B, Lee Y, Melendez JA, Cohen RA, Colucci WS (2006) Strain-stimulated hypertrophy in cardiac myocytes is mediated by reactive oxygen species-dependent Ras S-glutathiolation. J Mol Cell Cardiol 41:613–622. https://doi.org/10.1016/j.yjmcc.2006.05.009

    CAS  Article  PubMed  Google Scholar 

  187. 187.

    Polhemus DJ, Li Z, Pattillo CB, Gojon G Sr, Gojon G Jr, Giordano T, Krum H (2015) A novel hydrogen sulfide prodrug, SG1002, promotes hydrogen sulfide and nitric oxide bioavailability in heart failure patients. Cardiovasc Ther 33:216–226. https://doi.org/10.1111/1755-5922.12128

    CAS  Article  PubMed  Google Scholar 

  188. 188.

    Powis G, Kirkpatrick DL (2007) Thioredoxin signaling as a target for cancer therapy. Curr Opin Pharmacol 7:392–397. https://doi.org/10.1016/j.coph.2007.04.003

    CAS  Article  PubMed  Google Scholar 

  189. 189.

    Powis G, Mustacich D, Coon A (2000) The role of the redox protein thioredoxin in cell growth and cancer. Free Radical Biol Med 29:312–322. https://doi.org/10.1016/S0891-5849(00)00313-0

    CAS  Article  Google Scholar 

  190. 190.

    Qanungo S, Starke DW, Pai HV, Mieyal JJ, Nieminen AL (2007) Glutathione supplementation potentiates hypoxic apoptosis by S-glutathionylation of p65-NFkappaB. J Biol Chem 282:18427–18436. https://doi.org/10.1074/jbc.M610934200

    CAS  Article  PubMed  Google Scholar 

  191. 191.

    Radyuk SN, Orr WC (2018) The multifaceted impact of peroxiredoxins on aging and disease. Antioxid Redox Signal 29:1293–1311. https://doi.org/10.1089/ars.2017.7452

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  192. 192.

    Rao Y, Chen J, Guo Y, Ji T, Xie P (2020) Rivaroxaban ameliorates angiotensin II-induced cardiac remodeling by attenuating TXNIP/Trx2 interaction in KKAy mice. Thromb Res 193:45–52. https://doi.org/10.1016/j.thromres.2020.05.030

    CAS  Article  PubMed  Google Scholar 

  193. 193.

    Reinartz M, Ding Z, Flogel U, Godecke A, Schrader J (2008) Nitrosative stress leads to protein glutathiolation, increased s-nitrosation, and up-regulation of peroxiredoxins in the heart. J Biol Chem 283:17440–17449. https://doi.org/10.1074/jbc.M800126200

    CAS  Article  PubMed  Google Scholar 

  194. 194.

    Ren X, Zou L, Zhang X, Branco V, Wang J, Carvalho C, Holmgren A, Lu J (2017) Redox signaling mediated by thioredoxin and glutathione systems in the central nervous system. Antioxid Redox Signal 27:989–1010. https://doi.org/10.1089/ars.2016.6925

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  195. 195.

    Rhee SG, Chae HZ, Kim K (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 38:1543–1552. https://doi.org/10.1016/j.freeradbiomed.2005.02.026

    CAS  Article  PubMed  Google Scholar 

  196. 196.

    Rhee SG, Kil IS (2016) Mitochondrial H2O2 signaling is controlled by the concerted action of peroxiredoxin III and sulfiredoxin: linking mitochondrial function to circadian rhythm. Free Radic Biol Med 100:73–80. https://doi.org/10.1016/j.freeradbiomed.2016.10.011

    CAS  Article  PubMed  Google Scholar 

  197. 197.

    Rhee SG, Woo HA, Kang D (2018) The role of peroxiredoxins in the transduction of H2O2 signals. Antioxid Redox Signal 28:537–557. https://doi.org/10.1089/ars.2017.7167

    CAS  Article  PubMed  Google Scholar 

  198. 198.

    Rosello-Lleti E, Tarazon E, Barderas MG, Ortega A, Otero M, Molina-Navarro MM, Lago F, Gonzalez-Juanatey JR, Salvador A, Portoles M, Rivera M (2014) Heart mitochondrial proteome study elucidates changes in cardiac energy metabolism and antioxidant PRDX3 in human dilated cardiomyopathy. PLoS ONE 9:e112971. https://doi.org/10.1371/journal.pone.0112971

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  199. 199.

    Rubartelli A, Bajetto A, Allavena G, Wollman E, Sitia R (1992) Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway. J Biol Chem 267:24161–24164

    CAS  Article  Google Scholar 

  200. 200.

    Ruddy TD, Shumak SL, Liu PP, Barnie A, Seawright SJ, McLaughlin PR, Zinman B (1988) The relationship of cardiac diastolic dysfunction to concurrent hormonal and metabolic status in type I diabetes mellitus. J Clin Endocrinol Metab 66:113–118. https://doi.org/10.1210/jcem-66-1-113

    CAS  Article  PubMed  Google Scholar 

  201. 201.

    Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17:2596–2606. https://doi.org/10.1093/emboj/17.9.2596

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  202. 202.

    Salmon AB, Richardson A, Perez VI (2010) Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging? Free Radic Biol Med 48:642–655. https://doi.org/10.1016/j.freeradbiomed.2009.12.015

    CAS  Article  PubMed  Google Scholar 

  203. 203.

    Schenkel PC, Tavares AM, Fernandes RO, Diniz GP, Ludke AR, Ribeiro MF, Araujo AS, Barreto-Chaves ML, Bello-Klein A (2012) Time course of hydrogen peroxide-thioredoxin balance and its influence on the intracellular signalling in myocardial infarction. Exp Physiol 97:741–749. https://doi.org/10.1113/expphysiol.2012.064832

    CAS  Article  PubMed  Google Scholar 

  204. 204.

    Schroder E, Brennan JP, Eaton P (2008) Cardiac peroxiredoxins undergo complex modifications during cardiac oxidant stress. Am J Physiol Heart Circ Physiol 295:H425-433. https://doi.org/10.1152/ajpheart.00017.2008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  205. 205.

    Schroder E, Ponting CP (1998) Evidence that peroxiredoxins are novel members of the thioredoxin fold superfamily. Protein Sci 7:2465–2468. https://doi.org/10.1002/pro.5560071125

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  206. 206.

    Schroder K, Zhou R, Tschopp J (2010) The NLRP3 inflammasome: a sensor for metabolic danger? Science 327:296–300. https://doi.org/10.1126/science.1184003

    CAS  Article  PubMed  Google Scholar 

  207. 207.

    Schulte J, Struck J, Bergmann A, Kohrle J (2010) Immunoluminometric assay for quantification of peroxiredoxin 4 in human serum. Clin Chim Acta 411:1258–1263. https://doi.org/10.1016/j.cca.2010.05.016

    CAS  Article  PubMed  Google Scholar 

  208. 208.

    Schulz E, Wenzel P, Munzel T, Daiber A (2014) Mitochondrial redox signaling: Interaction of mitochondrial reactive oxygen species with other sources of oxidative stress. Antioxid Redox Signal 20:308–324. https://doi.org/10.1089/ars.2012.4609

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  209. 209.

    Severson DL (2004) Diabetic cardiomyopathy: recent evidence from mouse models of type 1 and type 2 diabetes. Can J Physiol Pharmacol 82:813–823. https://doi.org/10.1139/y04-065

    CAS  Article  PubMed  Google Scholar 

  210. 210.

    Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA, Group P-P (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 350:g7647. https://doi.org/10.1136/bmj.g7647

    Article  PubMed  PubMed Central  Google Scholar 

  211. 211.

    Shang Q, Bao L, Guo H, Hao F, Luo Q, Chen J, Guo C (2017) Contribution of glutaredoxin-1 to S-glutathionylation of endothelial nitric oxide synthase for mesenteric nitric oxide generation in experimental necrotizing enterocolitis. Transl Res 188:92–105. https://doi.org/10.1016/j.trsl.2016.01.004

    CAS  Article  PubMed  Google Scholar 

  212. 212.

    Shao D, Han J, Hou X, Fry J, Behring JB, Seta F, Long MT, Roy HK, Cohen RA, Matsui R, Bachschmid MM (2017) Glutaredoxin-1 deficiency causes fatty liver and dyslipidemia by inhibiting sirtuin-1. Antioxid Redox Signal 27:313–327. https://doi.org/10.1089/ars.2016.6716

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  213. 213.

    Shao D, Oka S, Liu T, Zhai P, Ago T, Sciarretta S, Li H, Sadoshima J (2014) A redox-dependent mechanism for regulation of AMPK activation by Thioredoxin1 during energy starvation. Cell Metab 19:232–245. https://doi.org/10.1016/j.cmet.2013.12.013

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  214. 214.

    Shi S, Guo Y, Lou Y, Li Q, Cai X, Zhong X, Li H (2017) Sulfiredoxin involved in the protection of peroxiredoxins against hyperoxidation in the early hyperglycaemia. Exp Cell Res 352:273–280. https://doi.org/10.1016/j.yexcr.2017.02.015

    CAS  Article  PubMed  Google Scholar 

  215. 215.

    Shokhina AG, Kostyuk AI, Ermakova YG, Panova AS, Staroverov DB, Egorov ES, Baranov MS, van Belle GJ, Katschinski DM, Belousov VV, Bilan DS (2019) Red fluorescent redox-sensitive biosensor Grx1-roCherry. Redox Biol 21:101071. https://doi.org/10.1016/j.redox.2018.101071

    CAS  Article  PubMed  Google Scholar 

  216. 216.

    Sies H, Jones DP (2020) Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol 21:363–383. https://doi.org/10.1038/s41580-020-0230-3

    CAS  Article  PubMed  Google Scholar 

  217. 217.

    Skoko JJ, Attaran S, Neumann CA (2019) Signals getting crossed in the entanglement of redox and phosphorylation pathways: phosphorylation of peroxiredoxin proteins sparks cell signaling. Antioxidants (Basel). https://doi.org/10.3390/antiox8020029

    Article  Google Scholar 

  218. 218.

    Song JJ, Rhee JG, Suntharalingam M, Walsh SA, Spitz DR, Lee YJ (2002) Role of glutaredoxin in metabolic oxidative stress. Glutaredoxin as a sensor of oxidative stress mediated by H2O2. J Biol Chem 277:46566–46575. https://doi.org/10.1074/jbc.M206826200

    CAS  Article  PubMed  Google Scholar 

  219. 219.

    Sorescu D, Griendling KK (2002) Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest Heart Fail 8:132–140. https://doi.org/10.1111/j.1527-5299.2002.00717.x

    CAS  Article  PubMed  Google Scholar 

  220. 220.

    Stocker S, Van Laer K, Mijuskovic A, Dick TP (2018) The conundrum of hydrogen peroxide signaling and the emerging role of peroxiredoxins as redox relay hubs. Antioxid Redox Signal 28:558–573. https://doi.org/10.1089/ars.2017.7162

    CAS  Article  PubMed  Google Scholar 

  221. 221.

    Stoyanovsky DA, Tyurina YY, Tyurin VA, Anand D, Mandavia DN, Gius D, Ivanova J, Pitt B, Billiar TR, Kagan VE (2005) Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein S-nitrosothiols. J Am Chem Soc 127:15815–15823. https://doi.org/10.1021/ja0529135

    CAS  Article  PubMed  Google Scholar 

  222. 222.

    Su H, Pistolozzi M, Shi X, Sun X, Tan W (2017) Alterations in NO/ROS ratio and expression of Trx1 and Prdx2 in isoproterenol-induced cardiac hypertrophy. Acta Biochim Biophys Sin (Shanghai) 49:1022–1028. https://doi.org/10.1093/abbs/gmx102

    CAS  Article  Google Scholar 

  223. 223.

    Suh JH, Heath SH, Hagen TM (2003) Two subpopulations of mitochondria in the aging rat heart display heterogenous levels of oxidative stress. Free Radic Biol Med 35:1064–1072. https://doi.org/10.1016/s0891-5849(03)00468-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  224. 224.

    Sun J, Morgan M, Shen RF, Steenbergen C, Murphy E (2007) Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 101:1155–1163. https://doi.org/10.1161/CIRCRESAHA.107.155879

    CAS  Article  PubMed  Google Scholar 

  225. 225.

    Sun L, Ferreira JC, Mochly-Rosen D (2011) ALDH2 activator inhibits increased myocardial infarction injury by nitroglycerin tolerance. Sci Transl Med 3:107ra111. https://doi.org/10.1126/scitranslmed.3002067

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  226. 226.

    Swain L, Kesemeyer A, Meyer-Roxlau S, Vettel C, Zieseniss A, Guntsch A, Jatho A, Becker A, Nanadikar MS, Morgan B, Dennerlein S, Shah AM, El-Armouche A, Nikolaev VO, Katschinski DM (2016) Redox imaging using cardiac myocyte-specific transgenic biosensor mice. Circ Res 119:1004–1016. https://doi.org/10.1161/CIRCRESAHA.116.309551

    CAS  Article  PubMed  Google Scholar 

  227. 227.

    Swain L, Nanadikar MS, Borowik S, Zieseniss A, Katschinski DM (2018) Transgenic organisms meet redox bioimaging: one step closer to physiology. Antioxid Redox Signal 29:603–612. https://doi.org/10.1089/ars.2017.7469

    CAS  Article  PubMed  Google Scholar 

  228. 228.

    Takagi Y, Gon Y, Todaka T, Nozaki K, Nishiyama A, Sono H, Hashimoto N, Kikuchi H, Yodoi J (1998) Expression of thioredoxin is enhanced in atherosclerotic plaques and during neointima formation in rat arteries. Lab Invest 78:957–966

    CAS  PubMed  Google Scholar 

  229. 229.

    Tang C, Yin G, Huang C, Wang H, Gao J, Luo J, Zhang Z, Wang J, Hong J, Chai X (2020) Peroxiredoxin-1 ameliorates pressure overload-induced cardiac hypertrophy and fibrosis. Biomed Pharmacother 129:110357. https://doi.org/10.1016/j.biopha.2020.110357

    CAS  Article  PubMed  Google Scholar 

  230. 230.

    Tavares AMV, Araujo ASD, Llesuy S, Khaper N, Rohde LE, Clausell N, Bello-Klein A (2012) Early loss of cardiac function in acute myocardial infarction is associated with redox imbalance. Exp Clin Cardiol 17:263–267

    CAS  PubMed  PubMed Central  Google Scholar 

  231. 231.

    Tian Y, Lv W, Lu C, Zhao X, Zhang C, Song H (2019) LATS2 promotes cardiomyocyte H9C2 cells apoptosis via the Prx3-Mfn2-mitophagy pathways. J Recept Signal Transduct Res 39:470–478. https://doi.org/10.1080/10799893.2019.1701031

    CAS  Article  PubMed  Google Scholar 

  232. 232.

    Tong G, Aponte AM, Kohr MJ, Steenbergen C, Murphy E, Sun J (2014) Postconditioning leads to an increase in protein S-nitrosylation. Am J Physiol Heart Circ Physiol 306:H825-832. https://doi.org/10.1152/ajpheart.00660.2013

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  233. 233.

    Tsuchiya Y, Peak-Chew SY, Newell C, Miller-Aidoo S, Mangal S, Zhyvoloup A, Bakovic J, Malanchuk O, Pereira GC, Kotiadis V, Szabadkai G, Duchen MR, Campbell M, Cuenca SR, Vidal-Puig A, James AM, Murphy MP, Filonenko V, Skehel M, Gout I (2017) Protein CoAlation: a redox-regulated protein modification by coenzyme A in mammalian cells. Biochem J 474:2489–2508. https://doi.org/10.1042/BCJ20170129

    CAS  Article  PubMed  Google Scholar 

  234. 234.

    Tullio F, Angotti C, Perrelli MG, Penna C, Pagliaro P (2013) Redox balance and cardioprotection. Basic Res Cardiol 108:392. https://doi.org/10.1007/s00395-013-0392-7

    CAS  Article  PubMed  Google Scholar 

  235. 235.

    Turoczi T, Chang VW, Engelman RM, Maulik N, Ho YS, Das DK (2003) Thioredoxin redox signaling in the ischemic heart: an insight with transgenic mice overexpressing Trx1. J Mol Cell Cardiol 35:695–704. https://doi.org/10.1016/s0022-2828(03)00117-2

    CAS  Article  PubMed  Google Scholar 

  236. 236.

    Ueno M, Masutani H, Arai RJ, Yamauchi A, Hirota K, Sakai T, Inamoto T, Yamaoka Y, Yodoi J, Nikaido T (1999) Thioredoxin-dependent redox regulation of p53-mediated p21 activation. J Biol Chem 274:35809–35815. https://doi.org/10.1074/jbc.274.50.35809

    CAS  Article  PubMed  Google Scholar 

  237. 237.

    Ullrich V, Schildknecht S (2014) Sensing hypoxia by mitochondria: a unifying hypothesis involving s-nitrosation. Antioxid Redox Signal 20:325–338. https://doi.org/10.1089/ars.2012.4788

    CAS  Article  PubMed  Google Scholar 

  238. 238.

    Ulrich K, Jakob U (2019) The role of thiols in antioxidant systems. Free Radic Biol Med 140:14–27. https://doi.org/10.1016/j.freeradbiomed.2019.05.035

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  239. 239.

    Urata Y, Ihara Y, Murata H, Goto S, Koji T, Yodoi J, Inoue S, Kondo T (2006) 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. https://doi.org/10.1074/jbc.M601984200

    CAS  Article  PubMed  Google Scholar 

  240. 240.

    Da V, Perez V, Mazo T, Munoz MC, Dominici FP, Carreras MC, Poderoso JJ, Sadoshima J, Gelpi RJ (2016) Loss of myocardial protection against myocardial infarction in middle-aged transgenic mice overexpressing cardiac thioredoxin-1. Oncotarget 7:11889–11898. https://doi.org/10.18632/oncotarget.7726

    Article  Google Scholar 

  241. 241.

    Velu CS, Niture SK, Doneanu CE, Pattabiraman N, Srivenugopal KS (2007) Human p53 is inhibited by glutathionylation of cysteines present in the proximal DNA-binding domain during oxidative stress. Biochemistry 46:7765–7780. https://doi.org/10.1021/bi700425y

    CAS  Article  PubMed  Google Scholar 

  242. 242.

    Watanabe Y, Murdoch CE, Sano S, Ido Y, Bachschmid MM, Cohen RA, Matsui R (2016) Glutathione adducts induced by ischemia and deletion of glutaredoxin-1 stabilize HIF-1alpha and improve limb revascularization. Proc Natl Acad Sci U S A 113:6011–6016. https://doi.org/10.1073/pnas.1524198113

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  243. 243.

    Wei B, Lin Q, Ji YG, Zhao YC, Ding LN, Zhou WJ, Zhang LH, Gao CY, Zhao W (2018) Luteolin ameliorates rat myocardial ischaemia-reperfusion injury through activation of peroxiredoxin II. Br J Pharmacol 175:3315–3332. https://doi.org/10.1111/bph.14367

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  244. 244.

    Welsh SJ, Bellamy WT, Briehl MM, Powis G (2002) The redox protein thioredoxin-1 (Trx-1) increases hypoxia-inducible factor 1alpha protein expression: Trx-1 overexpression results in increased vascular endothelial growth factor production and enhanced tumor angiogenesis. Cancer Res 62:5089–5095

    CAS  PubMed  Google Scholar 

  245. 245.

    White CR, Brock TA, Chang LY, Crapo J, Briscoe P, Ku D, Bradley WA, Gianturco SH, Gore J, Freeman BA et al (1994) Superoxide and peroxynitrite in atherosclerosis. Proc Natl Acad Sci U S A 91:1044–1048. https://doi.org/10.1073/pnas.91.3.1044

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  246. 246.

    Winterbourn CC (2020) Hydrogen peroxide reactivity and specificity in thiol-based cell signalling. Biochem Soc Trans 48:745–754. https://doi.org/10.1042/BST20190049

    CAS  Article  PubMed  Google Scholar 

  247. 247.

    Winterbourn CC, Hampton MB (2008) Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45:549–561. https://doi.org/10.1016/j.freeradbiomed.2008.05.004

    CAS  Article  PubMed  Google Scholar 

  248. 248.

    Witte S, Villalba M, Bi K, Liu YH, Isakov N, Altman A (2000) Inhibition of the c-Jun N-terminal kinase/AP-1 and NF-kappa B pathways by PICOT, a novel protein kinase C-interacting protein with a thioredoxin homology domain. J Biol Chem 275:1902–1909. https://doi.org/10.1074/jbc.275.3.1902

    CAS  Article  PubMed  Google Scholar 

  249. 249.

    Wohua Z, Weiming X (2019) Glutaredoxin 2 (GRX2) deficiency exacerbates high fat diet (HFD)-induced insulin resistance, inflammation and mitochondrial dysfunction in brain injury: a mechanism involving GSK-3beta. Biomed Pharmacother 118:108940. https://doi.org/10.1016/j.biopha.2019.108940

    CAS  Article  PubMed  Google Scholar 

  250. 250.

    Wunderlich C, Flogel U, Godecke A, Heger J, Schrader J (2003) Acute inhibition of myoglobin impairs contractility and energy state of iNOS-overexpressing hearts. Circ Res 92:1352–1358. https://doi.org/10.1161/01.RES.0000079026.70629.E5

    CAS  Article  PubMed  Google Scholar 

  251. 251.

    Yagi K, Liu C, Bando T, Yokomise H, Inui K, Hitomi S, Wada H (1994) Inhibition of reperfusion injury by human thioredoxin (adult T-cell leukemia-derived factor) in canine lung transplantation. J Thorac Cardiovasc Surg 108:913–921

    CAS  Article  Google Scholar 

  252. 252.

    Yamamoto M, Yang G, Hong C, Liu J, Holle E, Yu X, Wagner T, Vatner SF, Sadoshima J (2003) Inhibition of endogenous thioredoxin in the heart increases oxidative stress and cardiac hypertrophy. J Clin Invest 112:1395–1406. https://doi.org/10.1172/JCI17700

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  253. 253.

    Yamanaka H, Maehira F, Oshiro M, Asato T, Yanagawa Y, Takei H, Nakashima Y (2000) A possible interaction of thioredoxin with VDUP1 in HeLa cells detected in a yeast two-hybrid system. Biochem Biophys Res Commun 271:796–800. https://doi.org/10.1006/bbrc.2000.2699

    CAS  Article  PubMed  Google Scholar 

  254. 254.

    Yang J, Gong Y, Liu Q, Cai J, Zhang B, Zhang Z (2018) Thioredoxin silencing-induced cardiac supercontraction occurs through endoplasmic reticulum stress and calcium overload in chicken. Metallomics 10:1667–1677. https://doi.org/10.1039/c8mt00206a

    CAS  Article  PubMed  Google Scholar 

  255. 255.

    Yin T, Hou R, Liu S, Lau WB, Wang H, Tao L (2010) Nitrative inactivation of thioredoxin-1 increases vulnerability of diabetic hearts to ischemia/reperfusion injury. J Mol Cell Cardiol 49:354–361. https://doi.org/10.1016/j.yjmcc.2010.05.002

    CAS  Article  PubMed  Google Scholar 

  256. 256.

    Yoshioka J, Chutkow WA, Lee S, Kim JB, Yan J, Tian R, Lindsey ML, Feener EP, Seidman CE, Seidman JG, Lee RT (2012) Deletion of thioredoxin-interacting protein in mice impairs mitochondrial function but protects the myocardium from ischemia-reperfusion injury. J Clin Invest 122:267–279. https://doi.org/10.1172/JCI44927

    CAS  Article  PubMed  Google Scholar 

  257. 257.

    Young A, Gardiner D, Kuksal N, Gill R, O’Brien M, Mailloux RJ (2019) Deletion of the glutaredoxin-2 gene protects mice from diet-induced weight gain, which correlates with increased mitochondrial respiration and proton leaks in skeletal muscle. Antioxid Redox Signal 31:1272–1288. https://doi.org/10.1089/ars.2018.7715

    CAS  Article  PubMed  Google Scholar 

  258. 258.

    Zhang H, Luo Y, Zhang W, He Y, Dai S, Zhang R, Huang Y, Bernatchez P, Giordano FJ, Shadel G, Sessa WC, Min W (2007) Endothelial-specific expression of mitochondrial thioredoxin improves endothelial cell function and reduces atherosclerotic lesions. Am J Pathol 170:1108–1120. https://doi.org/10.2353/ajpath.2007.060960

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  259. 259.

    Zhang Y, Park J, Han SJ, Yang SY, Yoon HJ, Park I, Woo HA, Lee SR (2020) Redox regulation of tumor suppressor PTEN in cell signaling. Redox Biol 34:101553. https://doi.org/10.1016/j.redox.2020.101553

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  260. 260.

    Zhao W, Fan GC, Zhang ZG, Bandyopadhyay A, Zhou X, Kranias EG (2009) Protection of peroxiredoxin II on oxidative stress-induced cardiomyocyte death and apoptosis. Basic Res Cardiol 104:377–389. https://doi.org/10.1007/s00395-008-0764-6

    CAS  Article  PubMed  Google Scholar 

  261. 261.

    Zhou S, Narukami T, Masuo S, Shimizu M, Fujita T, Doi Y, Kamimura Y, Takaya N (2013) NO-inducible nitrosothionein mediates NO removal in tandem with thioredoxin. Nat Chem Biol 9:657–663. https://doi.org/10.1038/nchembio.1316

    CAS  Article  PubMed  Google Scholar 

  262. 262.

    Zhou Y, Kok KH, Chun AC, Wong CM, Wu HW, Lin MC, Fung PC, Kung H, Jin DY (2000) Mouse peroxiredoxin V is a thioredoxin peroxidase that inhibits p53-induced apoptosis. Biochem Biophys Res Commun 268:921–927. https://doi.org/10.1006/bbrc.2000.2231

    CAS  Article  PubMed  Google Scholar 

  263. 263.

    Zhu WZ, Wu XF, Zhang Y, Zhou ZN (2012) Proteomic analysis of mitochondrial proteins in cardiomyocytes from rats subjected to intermittent hypoxia. Eur J Appl Physiol 112:1037–1046. https://doi.org/10.1007/s00421-011-2050-9

    CAS  Article  PubMed  Google Scholar 

  264. 264.

    Zmijewski JW, Banerjee S, Bae H, Friggeri A, Lazarowski ER, Abraham E (2010) Exposure to hydrogen peroxide induces oxidation and activation of AMP-activated protein kinase. J Biol Chem 285:33154–33164. https://doi.org/10.1074/jbc.M110.143685

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  265. 265.

    Zschauer TC, Matsushima S, Altschmied J, Shao D, Sadoshima J, Haendeler J (2013) Interacting with thioredoxin-1–disease or no disease? Antioxid Redox Signal 18:1053–1062. https://doi.org/10.1089/ars.2012.4822

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work has been supported by the EU-CARDIOPROTECTION COST (European Cooperation in Science and Technology-Action) (CA16225). I.A. acknowledges support from the European Union (ERDF) and Greek national funds through the Operational Program “Competitiveness, Entrepreneurship and Innovation”, under the call “RESEARCH – CREATE - INNOVATE” (Project code: 5048539). A.D. was supported by vascular biology research grants from the Boehringer Ingelheim Foundation for the collaborative research group ‘Novel and neglected cardiovascular risk factors: Molecular mechanisms and therapeutics’. R.S. was supported by Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) [Project number 268555672 – SFB 1213, Project B05].

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Ioanna Andreadou or Rainer Schulz.

Ethics declarations

Conflict of interest

R.S. received fees for lectures provided to Amgen, Recordati and Sanofi and grant support form Sanofi. The other authors declare that they have no conflicts of interest with the contents of this article.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Andreadou, I., Efentakis, P., Frenis, K. et al. Thiol-based redox-active proteins as cardioprotective therapeutic agents in cardiovascular diseases. Basic Res Cardiol 116, 44 (2021). https://doi.org/10.1007/s00395-021-00885-5

Download citation

Keywords

  • Thioredoxins
  • Glutaredoxins
  • Peroxiredoxins
  • Cardiac hypertrophy
  • Ischemia/reperfusion injury
  • Heart failure