Thioredoxin-1 is required for the cardioprotecive effect of sildenafil against ischaemia/reperfusion injury and mitochondrial dysfunction in mice

References

• World Health Organization. What are cardiovascular diseases? In: Mendis S, Puska P and Norrving B, editors. Global Atlas on cardiovascular diseases prevention and control. Geneva (Switzerland): World Health Organization in collaboration with the World Heart Federation and the World Stroke Organization; 2011. Chapter 1.
   Google Scholar
• Jennings RB, Sommers HM, Smyth GA. Myocardial necrosis induced by temporary occlusion of a coronary artery in the dog. Arch Pathol. 1960;70:68–78.
   PubMedGoogle Scholar
• Cadenas S. ROS and redox signaling in myocardial ischemia-reperfusion injury and cardioprotection. Free Radic Biol Med. 2018;117:76–89.
   PubMed Web of Science ®Google Scholar
• Darley-Usmar V. The powerhouse takes control of the cell; the role of mitochondria in signal transduction. Free Radic Biol Med. 2004;37(6):753–754.
   PubMed Web of Science ®Google Scholar
• Boveris A, Oshino N, Chance B. The cellular production of hydrogen peroxide. Biochem J. 1972;128(3):617–630.
   PubMed Web of Science ®Google Scholar
• Liu T, O’Rourke B. Regulation of mitochondrial Ca2+ and its effects on energetics and redox balance in normal and failing heart. J Bioenerg Biomembr. 2009;41(2):127–132.
   PubMed Web of Science ®Google Scholar
• Aon MA, Cortassa S, Marbán E, et al. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J Biol Chem. 2003;278(45):44735–44744.
   PubMed Web of Science ®Google Scholar
• Slodzinski MK, Aon MA, O'Rourke B. Glutathione oxidation as a trigger of mitochondrial depolarization and oscillation in intact hearts. J Mol Cell Cardiol. 2008;45(5):650–660.
   PubMed Web of Science ®Google Scholar
• Halestrap AP, McStay GP, Clarke SJ. The permeability transition pore complex: another view. Biochimie. 2002;84(2–3):153–166.
   PubMed Web of Science ®Google Scholar
• Gomez L, Li B, Mewton N, et al. Inhibition of mitochondrial permeability transition pore opening: translation to patients. Cardiovasc Res. 2009;83(2):226–233.
   PubMed Web of Science ®Google Scholar
• Mahmood DF, Abderrazak A, El Hadri K, et al. The thioredoxin system as a therapeutic target in human health and disease. Antioxid Redox Signal. 2013;19(11):1266–1303.
   PubMed Web of Science ®Google Scholar
• Adluri RS, Thirunavukkarasu M, Zhan L, et al. Thioredoxin 1 enhances neovascularization and reduces ventricular remodeling during chronic myocardial infarction: a study using thioredoxin 1 transgenic mice. J Mol Cell Cardiol. 2011;50(1):239–247.
   PubMed Web of Science ®Google Scholar
• D’Annunzio V, Perez V, Mazo T, et al. Loss of myocardial protection against myocardial infarction in middle-aged transgenic mice overexpressing cardiac thioredoxin-1. Oncotarget. 2016;7(11):11889–11898.
   PubMedGoogle Scholar
• Yoshioka J, Lee RT. Thioredoxin-interacting protein and myocardial mitochondrial function in ischemia-reperfusion injury. Trends Cardiovasc Med. 2014;24(2):75–80.
   PubMed Web of Science ®Google Scholar
• Perez V, D'Annunzio V, Valdez LB, et al. Thioredoxin-1 attenuates ventricular and mitochondrial postischemic dysfunction in the stunned myocardium of transgenic mice. Antioxid Redox Signal. 2016;25(2):78–88.
   PubMed Web of Science ®Google Scholar
• D’Annunzio V, Perez V, Boveris A, et al. Role of thioredoxin-1 in ischemic preconditioning, postconditioning and aged ischemic hearts. Pharmacol Res. 2016;109:24–31.
   PubMed Web of Science ®Google Scholar
• Mazo TD, D'Annunzio V, Zaobornyj T, et al. High-fat diet abolishes the cardioprotective effects of ischemic postconditioning in murine models despite increased thioredoxin-1 levels. Mol Cell Biochem. 2019;452(1–2):153–166.
   PubMed Web of Science ®Google Scholar
• Ignarro LJ, Buga GM, Wood KS, et al. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA. 1987;84(24):9265–9269.
   PubMed Web of Science ®Google Scholar
• Boolell M, Allen MJ, Ballard SA, et al. Sildenafil: an orally active type 5 cyclic GMP-specific phosphodiesterase inhibitor for the treatment of penile erectile dysfunction. Int J Impot Res. 1996;8(2):47–52.
   PubMedGoogle Scholar
• Ockaili R, Salloum F, Hawkins J, et al. Sildenafil (Viagra) induces powerful cardioprotective effect via opening of mitochondrial K(ATP) channels in rabbits. Am J Physiol Heart Circ Physiol. 2002;283(3):H1263–H1269.
   PubMed Web of Science ®Google Scholar
• Du Toit EF, Rossouw E, Salie R, et al. Effect of sildenafil on reperfusion function, infarct size, and cyclic nucleotide levels in the isolated rat heart model. Cardiovasc Drugs Ther. 2005;19(1):23–31.
   PubMed Web of Science ®Google Scholar
• Vidavalur R, Penumathsa SV, Zhan L, et al. Sildenafil induces angiogenic response in human coronary arteriolar endothelial cells through the expression of thioredoxin, hemeoxygenase and vascular endothelial growth factor. Vascul Pharmacol. 2006;45(2):91–95.
   PubMed Web of Science ®Google Scholar
• Koneru S, Varma Penumathsa S, Thirunavukkarasu M, et al. Sildenafil-mediated neovascularization and protection against myocardial ischaemia reperfusion injury in rats: role of VEGF/angiopoietin-1. J Cell Mol Med. 2008;12(6B):2651–2664.
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Yang G, Hong C, et al. Inhibition of endogenous thioredoxin in the heart increases oxidative stress and cardiac hypertrophy. J Clin Invest. 2003;112(9):1395–1406.
   PubMed Web of Science ®Google Scholar
• Ascah A, Khairallah M, Daussin F, et al. Stress-induced opening of the permeability transition pore in the dystrophin-deficient heart is attenuated by acute treatment with sildenafil. Am J Physiol Heart Circ Physiol. 2011;300(1):H144–H153.
   PubMed Web of Science ®Google Scholar
• Boveris A, Costa LE, Cadenas E, et al. Regulation of mitochondrial respiration by adenosine diphosphate, oxygen, and nitric oxide. Meth Enzymol. 1999;301:188–198.
   PubMed Web of Science ®Google Scholar
• Chen Q, Vazquez EJ, Moghaddas S, et al. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem. 2003;278(38):36027–36031.
   PubMed Web of Science ®Google Scholar
• Squellerio I, Caruso D, Porro B, et al. Direct glutathione quantification in human blood by LC–MS/MS: comparison with HPLC with electrochemical detection. J Pharm Biomed Anal. 2012;71:111–118.
   PubMed Web of Science ®Google Scholar
• Holmgren A, Björnstedt M. Thioredoxin and thioredoxin reductase. Meth Enzymol. 1995;252:199–208.
   PubMed Web of Science ®Google Scholar
• Aboutabl ME, Raafat M, Maklad YA, et al. Sildenafil augments the beneficial hemodynamic and histopathological effects of amlodipine in nitric oxide-deficient hypertensive rats: role of nitric oxide-cyclic GMP pathway. Pharmacol Res. 2008;57(6):456–463.
   PubMed Web of Science ®Google Scholar
• Sánchez-Villamil JP, D’Annunzio V, Finocchietto P, et al. Cardiac-specific overexpression of thioredoxin 1 attenuates mitochondrial and myocardial dysfunction in septic mice. Int J Biochem Cell Biol. 2016;81(B):323–334.
   PubMedGoogle Scholar
• Das A, Xi L, Kukreja RC. Phosphodiesterase-5 inhibitor sildenafil preconditions adult cardiac myocytes against necrosis and apoptosis. Essential role of nitric oxide signaling. J Biol Chem. 2005;280(13):12944–12955.
   PubMed Web of Science ®Google Scholar
• Koka S, Das A, Salloum FN, et al. Phosphodiesterase-5 inhibitor tadalafil attenuates oxidative stress and protects against myocardial ischemia/reperfusion injury in type 2 diabetic mice. Free Radic Biol Med. 2013;60:80–88.
   PubMed Web of Science ®Google Scholar
• Burwell LS, Nadtochiy SM, Brookes PS. Cardioprotection by metabolic shut-down and gradual wake-up. J Mol Cell Cardiol. 2009;46(6):804–810.
   PubMed Web of Science ®Google Scholar
• Halestrap AP. A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection. Biochm Soc Trans. 2010;38(4):841–860.
   PubMedGoogle Scholar
• Keinan N, Tyomkin D, Shoshan-Barmatz V. Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol Cell Biol. 2010;30(24):5698–5709.
   PubMed Web of Science ®Google Scholar
• Liao Z, Liu D, Tang L, et al. Long-term oral resveratrol intake provides nutritional preconditioning against myocardial ischemia/reperfusion injury: involvement of VDAC1 downregulation. Mol Nutr Food Res. 2015;59(3):454–464.
   PubMed Web of Science ®Google Scholar
• Ago T, Yeh I, Yamamoto M, et al. Thioredoxin1 upregulates mitochondrial proteins related to oxidative phosphorylation and TCA cycle in the heart. Antioxid Redox Signal. 2006;8(9–10):1635–1650.
   PubMed Web of Science ®Google Scholar
• Cohen MV, Yang XM, Neumann T, et al. Favorable remodeling enhances recovery of regional myocardial function in the weeks after infarction in ischemically preconditioned hearts. Circulation. 2000;102(5):579–583.
   PubMed Web of Science ®Google Scholar
• Mount PF, Kemp BE, Power DA. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol. 2007;42(2):271–279.
   PubMed Web of Science ®Google Scholar
• Connelly KA, Advani A, Advani SL, et al. Impaired cardiac anti-oxidant activity in diabetes: human and correlative experimental studies. Acta Diabetol. 2014;51(5):771–782.
   PubMed Web of Science ®Google Scholar