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TH Metabolism in Ischemia/Reperfusion Models

  • Claudia KusmicEmail author
  • Serena L’Abbate
Chapter
  • 41 Downloads

Abstract

Clinical evidence has shown that the two major outcomes of thyroid disease, namely, hypothyroidism and hyperthyroidism, cause evident alterations in haemodynamics and cardiac function. Moreover, even subclinical conditions of thyroid dysfunction represent higher risk for cardiovascular disease (CVD). On the other hand, clinical observations have also highlighted that CVD such as acute infarction and heart failure are associated with reduced T3 state, even in the absence of overt thyroid disorders in about 15–30% of cases. For a long time, the hypothesis underlying these observations has been that peripheral reduction of T4 conversion to T3 or inactivation to rT3 could be an adaptive response of myocardial tissue to reduce metabolic demands under stressful conditions. However, clinical evidence has proven that a persistent low T3 condition may have adverse cardiac prognostic outcomes. Moreover, a few clinical trials have shown that the replacement of homeostatic doses of thyroid hormones have a positive role in ameliorating the severity of CVD. These findings paved the way to explore new therapeutic strategies in the field of CVD and to investigate the cellular and molecular basis of such potential cardioprotective effects of thyroid hormones through experimental studies. The examination of individual cell pathways and more complex high-throughput analyses have currently provided a broader picture of T3 action during acute infarction and in the postischemic setting. It includes genomic and non-genomic mechanisms of action and crosstalk between T3 and specific miRNAs for the post-translational regulation of a wide range of genes involved in many cellular processes. Mitochondria, whose cellular functions are pleiotropic and go well beyond the mere regulation of bioenergetics, have also emerged as a pivotal target of T3 action.

Keywords

Ischemia/reperfusion Cardiovascular disease Thyroid hormones Low T3 state Cardioprotection Animal models 

References

  1. 1.
    Vaughan DE, Pfeffer MA. Angiotensin converting enzyme inhibitors and cardiovascular remodelling. Cardiovasc Res. 1994;28:159–65.PubMedCrossRefGoogle Scholar
  2. 2.
    Friberg L, Werner S, Eggertsen G, Ahnve S. Rapid down-regulation of thyroid hormones in acute myocardial infarction: is it cardioprotective in patients with angina? Arch Intern Med. 2002;162:1388–94.PubMedCrossRefGoogle Scholar
  3. 3.
    Iervasi G, Pingitore A, Landi P, Raciti M, Ripoli A, Scarlattini M, et al. Low-T3 syndrome: a strong prognostic predictor of death in patients with heart disease. Circulation. 2003;107:708–13.PubMedCrossRefGoogle Scholar
  4. 4.
    Olivares EL, Marassi MP, Fortunato RS, da Silva AC, Costa-e-Sousa RH, Araújo IG, et al. Thyroid function disturbance and type 3 iodothyronine deiodinase induction after myocardial infarction in rats a time course study. Endocrinology. 2007;148:4786–92.PubMedCrossRefGoogle Scholar
  5. 5.
    Pol CJ, Muller A, Zuidwijk MJ, van Deel ED, Kaptein E, Saba A, et al. Left-ventricular remodeling after myocardial infarction is associated with a cardiomyocyte-specific hypothyroid condition. Endocrinology. 2011;152:669–79.PubMedCrossRefGoogle Scholar
  6. 6.
    Forini F, Kusmic C, Nicolini G, Mariani L, Zucchi R, Matteucci M, et al. Triiodothyronine prevents cardiac ischemia/reperfusion mitochondrial impairment and cell loss by regulating miR30/p53 axis. Endocrinology. 2014;155:4581–90.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Kimur T, Kotajima N, Kanda T, Kuwabara A, Fukumura Y, Kobayashi I. Correlation of circulating interleukin-10 with thyroid hormone in acute myocardial infarction. Res Commun Mol Pathol Pharmacol. 2001;110:53–8.PubMedGoogle Scholar
  8. 8.
    Pingitore A, Iervasi G, Barison A, Prontera C, Pratali L, Emdin M, et al. Early activation of an altered thyroid hormone profile in asymptomatic or mildly symptomatic idiopathic left ventricular dysfunction. J Card Fail. 2006;7:520–6.CrossRefGoogle Scholar
  9. 9.
    Razvi S, Ingoe L, Keeka G, Oates C, McMillan C, Weaver JU. The beneficial effect of L-thyroxine on cardiovascular risk factors, endothelial function, and quality of life in subclinical hypothyroidism: randomized, crossover trial. J Clin Endocrinol Metab. 2007;92:1715–23.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Pingitore A, Galli E, Barison A, Iervasi A, Scarlattini M, Nucci D, et al. Acute effects of triiodothyronine (T3) replacement therapy in patients with chronic heart failure and low- T3 syndrome: a randomized, placebo-controlled study. J Clin Endocrinol Metab. 2008;93:1351–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Gerdes AM, Iervasi G. Thyroid replacement therapy and heart failure. Circulation. 2010;122:385–93.PubMedCrossRefGoogle Scholar
  12. 12.
    Pingitore A, Chen Y, Gerdes AM, Iervasi G. Acute myocardial infarction and thyroid function: new pathophysiological and therapeutic perspectives. Ann Med. 2012;44:745–57.PubMedCrossRefGoogle Scholar
  13. 13.
    Forini F, Lionetti V, Ardehali H, Pucci A, Cecchetti F, Ghanefar M, et al. Early long-term L-T3 replacement rescues mitochondria and prevents ischemic cardiac remodelling in rats. J Cell Mol Med. 2011;15:514–24.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Forini F, Ucciferri N, Kusmic C, Nicolini G, Cecchettini A, Rocchiccioli S, et al. Low T3 state is correlated with cardiac mitochondrial impairments after ischemia reperfusion injury: evidence from a proteomic approach. Int J Mol Sci. 2015;16:26687–705.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Nicolini G, Forini F, Kusmic C, Pitto L, Mariani L, Iervasi G. Early and short-term triiodothyronine supplementation prevents adverse post-ischemic cardiac remodeling: role of transforming growth factor-β1 and anti-fibrotic miRNA signaling. Mol Med. 2016;21:900–11.PubMedCrossRefGoogle Scholar
  16. 16.
    Forini F, Nicolini G, Kusmic C, D'Aurizio R, Rizzo M, Baumgart M, et al. Integrative analysis of differentially expressed genes and miRNAs predicts complex T3-mediated protective circuits in a rat model of cardiac ischemia reperfusion. Sci Rep. 2018;8:13870.  https://doi.org/10.1038/s41598-018-32237-0.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Bassett JH, Harvey CB, Williams GR. Mechanisms of thyroid hormone receptor-specific nuclear and extra nuclear actions. Mol Cell Endocrinol. 2003;213:1–11.PubMedCrossRefGoogle Scholar
  18. 18.
    Yen PM, Ando S, Feng X, Liu Y, Maruvada P, Xia X. Thyroid hormone action at the cellular, genomic and target gene levels. Mol Cell Endocrinol. 2006;246:121–7.PubMedCrossRefGoogle Scholar
  19. 19.
    Wiersinga WM. The role of thyroid hormone nuclear receptors in the heart: evidence from pharmacological approaches. Heart Fail Rev. 2010;15:121–4.PubMedCrossRefGoogle Scholar
  20. 20.
    Ortiga-Carvalho TM, Sidhaye AR, Wondisford FE. Thyroid hormone receptors and resistance to thyroid hormone disorders. Nat Rev Endocrinol. 2014;10:582–91.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Anyetei-Anum CS, Roggero VR, Allison LA. Thyroid hormone receptor localization in target tissues. J Endocrinol. 2018;237:R19–34.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Pantos C, Mourouzis I. Thyroid hormone receptor α1 as a novel therapeutic target for tissue repair. Ann Transl Med. 2018;6:254.  https://doi.org/10.21037/atm.2018.06.12.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Morkin E. Regulation of myosin heavy chains in the heart. Circulation. 1993;87:1451–60.PubMedCrossRefGoogle Scholar
  24. 24.
    Hartong R, Wang N, Kurokawa R, Lazar MA, Glass CK, Apriletti JW, et al. Delineation of three different thyroid response elements in promoter of rat sarcoplasmic reticulum Ca2+ATPase gene: demonstration that retinoid X receptor binds 5′ to thyroid hormone receptor in response element 1. J Biol Chem. 1994;269:13021–9.PubMedGoogle Scholar
  25. 25.
    Kaasik A, Paju K, Vetter R, Seppet EK. Thyroid hormones increase the contractility but suppress the effects of β-adrenergic agonist by decreasing phospholamban expression in rat atria. Cardiovasc Res. 1997;35:106–12.PubMedCrossRefGoogle Scholar
  26. 26.
    Holt E, Sjaastad I, Lunde PK, Christensen G, Sejersted OM. Thyroid hormone control of contraction and the Ca2+-ATPase/phospholamban complex in adult rat ventricular myocytes. J Mol Cell Cardiol. 1999;31:645–56.PubMedCrossRefGoogle Scholar
  27. 27.
    Razvi S, Jabbar A, Pingitore A, Danzi S, Biondi B, Klein I, et al. Thyroid hormones and cardiovascular function and diseases. J Am Coll Cardiol. 2018;71:1781–96.PubMedCrossRefGoogle Scholar
  28. 28.
    Forini F, Nicolini G, Iervasi G. Mitochondria as key targets of cardioprotection in cardiac ischemic disease: role of thyroid hormone triiodothyronine. Int J Mol Sci. 2015;16:6312–36.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Zhang D, Li Y, Liu S, Wang YC, Guo F, Zhai Q, et al. MicroRNA and thyroid hormone signaling in cardiac and skeletal muscle. Cell Biosci. 2017;7:14.  https://doi.org/10.1186/s13578-017-0141-y.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Singh BK, Sinha RA, Yen PM. Novel transcriptional mechanisms for regulating metabolism by thyroid hormone. Int J Mol Sci. 2018;19:E3284.  https://doi.org/10.3390/ijms19103284.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Davis PJ, Davis FB. Nongenomic actions of thyroid hormone on the heart. Thyroid. 2002;12:459–66.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Hiroi Y, Kim H-H, Ying H, Furuya F, Huang Z, Simoncini T, et al. Rapid nongenomic actions of thyroid hormone. Proc Natl Acad Sci U S A. 2006;103:14104–9.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Davis PJ, Leonard JL, Davis FB. Mechanisms of nongenomic actions of thyroid hormone. Front Neuroendocrinol. 2008;29:211–8.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Davis PJ, Goglia F, Leonard JL. Nongenomic actions of thyroid hormone. Nat Rev Endocrinol. 2016;12:111–21.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Kuiper GG, Kester MH, Peeters RP, Visser TJ. Biochemical mechanisms of thyroid hormone deiodination. Thyroid. 2005;15:787–98.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Gereben B, Zavacki AM, Ribich S, Kim BW, Huang SA, Simonides WS, et al. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr Rev. 2008;29:898–938.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Little AG. A review of the peripheral levels of regulation by thyroid hormone. J Comp Physiol B. 2016;186:677–88.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Louzada RA, Carvalho DP. Similarities and differences in the peripheral actions of thyroid hormones and their metabolites. Front Endocrinol. 2018;9:394.  https://doi.org/10.3389/fendo.2018.00394.CrossRefGoogle Scholar
  39. 39.
    Friesema EC, Kuiper GG, Jansen J, Visser TJ, Kester MH. Thyroid hormone transport by the human monocarboxylate transporter 8 and its rate-limiting role in intracellular metabolism. Mol Endocrinol. 2006;20:2761–72.PubMedCrossRefGoogle Scholar
  40. 40.
    Wajner SM, Maia AL. New insights toward the acute non-thyroidal illness syndrome. Front Endocrinol. 2012;3:8.  https://doi.org/10.3389/fendo.2012.00008.CrossRefGoogle Scholar
  41. 41.
    Wajner SM, Goemann IM, Bueno AL, Larsen PR, Maia AL. IL-6 promotes nonthyroidal illness syndrome by blocking thyroxine activation while promoting thyroid hormone inactivation in human cells. J Clin Invest. 2011;121:1834–45.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Peeters RP, Wouters PJ, van Toor H, Kaptein E, Visser TJ, Van den Berghe G. Serum 3,3′,5′-triiodothyronine (rT3) and 3,5,3′-triiodothyronine/rT3 are prognostic markers in critically ill patients and are associated with postmortem tissue deiodinase activities. J Clin Endocrinol Metab. 2005;90:4559–65.PubMedCrossRefGoogle Scholar
  43. 43.
    Rodriguez-Perez A, Palos-Paz F, Kaptein E, Visser TJ, Dominguez-Gerpe L, Alvarez-Escudero J, et al. Identification of molecular mechanisms related to nonthyroidal illness syndrome in skeletal muscle and adipose tissue from patients with septic shock. Clin Endocrinol. 2008;68:821–7.CrossRefGoogle Scholar
  44. 44.
    Lehnen TE, Santos MV, Lima A, Maia AL, Wajner SM. N-acetylcysteine prevents low T3 syndrome and attenuates cardiac dysfunction in a male rat model of myocardial infarction. Endocrinology. 2017;158:1502–10.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Moreno M, de Lange P, Lombardi A, Silvestri E, Lanni A, Goglia F. Metabolic effects of thyroid hormone derivatives. Thyroid. 2008;18:239–53.PubMedCrossRefGoogle Scholar
  46. 46.
    Goglia F. The effects of 3,5-diiodothyronine on energy balance. Front Physiol. 2015;5:528.  https://doi.org/10.3389/fphys.2014.00528.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Accorroni A, Saponaro F, Zucchi R. Tissue thyroid hormones and thyronamines. Heart Fail Rev. 2016;21:373–90.PubMedCrossRefGoogle Scholar
  48. 48.
    Moreno M, Giacco A, Di Munno C, Goglia F. Direct and rapid effects of 3,5-diiodo-L-thyronine (T2). Mol Cell Endocrinol. 2017;458:121–6.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Scanlan TS, Suchland KL, Hart ME, Chiellini G, Huang Y, Kruzich PJ, et al. 3-Iodothyronamine is an endogenous and rapid-acting derivative of thyroid hormone. Nat Med. 2004;10:638–42.PubMedCrossRefGoogle Scholar
  50. 50.
    Rutigliano G, Zucchi R. Cardiac actions of thyroid hormone metabolites. Mol Cell Endocrinol. 2017;458:76–81.PubMedCrossRefGoogle Scholar
  51. 51.
    Biondi B, Palmieri EA, Lombardi G, Fazio S. Effects of thyroid hormone on cardiac function: the relative importance of heart rate, loading conditions, and myocardial contractility in the regulation of cardiac performance in human hyperthyroidism. J Clin Endocrinol Metab. 2002;87:968–74.PubMedCrossRefGoogle Scholar
  52. 52.
    Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocrine Rev. 2005;26:704–28.CrossRefGoogle Scholar
  53. 53.
    Klein I, Danzi S. Thyroid disease and the heart. Circulation. 2007;116:1725–35.PubMedCrossRefGoogle Scholar
  54. 54.
    Jabbar A, Pingitore A, Pearce SH, Zaman A, Iervasi G, Razvi S. Thyroid hormones and cardiovascular disease. Nat Rev Cardiol. 2017;14:39–55.PubMedCrossRefGoogle Scholar
  55. 55.
    Biondi B, Cooper DS. Subclinical hyperthyroidism. N Engl J Med. 2018;379:1485–6.PubMedGoogle Scholar
  56. 56.
    Völzke H. Hyperthyroidism and mortality. J Am Coll Cardiol. 2007;49:2228–9.PubMedCrossRefGoogle Scholar
  57. 57.
    Collet TH, Gussekloo J, Bauer DC, den Elzen WP, Cappola AR, Balmer P, et al. Subclinical hyperthyroidism and the risk of coronary heart disease and mortality. Arch Intern Med. 2012;172:799–809.PubMedCrossRefGoogle Scholar
  58. 58.
    Klein I, Danzi S. Thyroid disease and the heart. Curr Probl Cardiol. 2016;41:65–92.PubMedCrossRefGoogle Scholar
  59. 59.
    Robuschi G, Medici D, Fesani F, Barboso G, Montermini M, d’Amato L, et al. Cardiopulmonary bypass: a low T4 and T3 syndrome with blunted thyrotropin (TSH) response to thyrotropin-releasing hormone (TRH). Horm Res. 1986;23:151–8.PubMedCrossRefGoogle Scholar
  60. 60.
    Holland FW, Brown PS Jr, Weintraub BD, Clark RE. Cardiopulmonary bypass and thyroid function: a “euthyroid sick syndrome”. Ann Thorac Surg. 1991;52:46–50.PubMedCrossRefGoogle Scholar
  61. 61.
    Cerillo AG, Storti S, Kallushi E, Haxhiademi D, Miceli A, Murzi M, et al. The low triiodothyronine syndrome: a strong predictor of low cardiac output and death in patients undergoing coronary artery bypass grafting. Ann Thorac Surg. 2014;97:2089–95.PubMedCrossRefGoogle Scholar
  62. 62.
    Klemperer JD, Klein I, Gomez M, Helm RE, Ojamaa K, Thosmas SJ, et al. Thyroid hormone treatment after coronary-artery bypass surgery. N Engl J Med. 1995;333:1522–7.PubMedCrossRefGoogle Scholar
  63. 63.
    Klemperer JD, Klein IL, Ojamaa K, Helm RE, Gomez M, Isom OW, et al. Triiodothyronine therapy lowers the incidence of atrial fibrillation after cardiac operations. Ann Thorac Surg. 1996;61:1323–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Schmidt-Ott UM, Ascheim DD. Thyroid hormone and heart failure. Curr Heart Fail Rep. 2006;3:114–9.PubMedCrossRefGoogle Scholar
  65. 65.
    Pingitore A, Landi P, Taddei MC, Ripoli A, L’Abbate A, Iervasi G. Triiodothyronine levels for risk stratification of patients with chronic heart failure. Am J Med. 2005;118:132–6.PubMedCrossRefGoogle Scholar
  66. 66.
    Lymvaios I, Mourouzis I, Cokkinos DV, Dimopoulus MA, Toumanidis ST, Pantos C. Thyroid hormone and recovery of cardiac function in patients with acute myocardial infarction: a strong association? Eur J Endocrinol. 2011;165:107–14.PubMedCrossRefGoogle Scholar
  67. 67.
    Chang X, Zhang S, Zhang M, Wang H, Fan C, Gu Y, et al. Free triiodothyronine and global registry of acute coronary events risk score on predicting long-term major adverse cardiac events in STEMI patients undergoing primary PCI. Lipids Health Dis. 2018;17:234.  https://doi.org/10.1186/s12944-018-0881-7.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Frangogiannis NG. Pathophysiology of myocardial infarction. Compr Physiol. 2015;5:1841–75.PubMedCrossRefGoogle Scholar
  69. 69.
    Frangogiannis NG. Cell biological mechanisms in regulation of the post-infarction inflammatory response. Curr Opin Physiol. 2018;1:7–13.PubMedCrossRefGoogle Scholar
  70. 70.
    Baines CP. The mitochondrial permeability transition pore and ischemia-reperfusion injury. Basic Res Cardiol. 2009;104:181–8.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Baines CP. The cardiac mitochondrion: nexus of stress. Annu Rev Physiol. 2010;72:61–80.PubMedCrossRefGoogle Scholar
  72. 72.
    Galluzzi L, Kepp O, Kroemer G. Mitochondria: master regulators of danger signaling. Nat Rev Mol Cell Biol. 2012;13:780–8.PubMedCrossRefGoogle Scholar
  73. 73.
    Khalife WI, Tang YD, Kuzman JA, Thomas TA, Anderson BE, Said S, et al. Treatment of subclinical hypothyroidism reverses ischemia and prevents myocyte loss and progressive LV dysfunction in hamsters with dilated cardiomyopathy. Am J Physiol Heart Circ Physiol. 2005;289:H2409–15.PubMedCrossRefGoogle Scholar
  74. 74.
    Thomas TA, Kuzman JA, Anderson BE, Andersen SM, Schlenker EH, Holder MS, et al. Thyroid hormones induce unique and potentially beneficial changes in cardiac myocyte shape in hypertensive rats near heart failure. Am J Physiol Heart Circ Physiol. 2005;288:H2118–22.PubMedCrossRefGoogle Scholar
  75. 75.
    Chen YF, Kobayashi S, Chen J, Redetzke RA, Said S, Liang Q, et al. Short term triiodo-L-thyronine treatment inhibits cardiac myocyte apoptosis in border area after myocardial infarction in rats. J Mol Cell Cardiol. 2008;44:180–7.PubMedCrossRefGoogle Scholar
  76. 76.
    Pantos C, Mourouzis I, Markakis K, Tsagoulis N, Panagiotou M, Cokkinos DV. Long-term thyroid hormone administration reshapes left ventricular chamber and improves cardiac function after myocardial infarction in rats. Basic Res Cardiol. 2008;103:308–18.PubMedCrossRefGoogle Scholar
  77. 77.
    Pantos C, Malliopoulou V, Paizis I, Moraitis P, Mourouzis I, Tzeis S, et al. Thyroid hormone and cardioprotection: study of p38 MAPK and JNKs during ischaemia and at reperfusion in isolated rat heart. Mol Cell Biochem. 2003;242:173–80.PubMedCrossRefGoogle Scholar
  78. 78.
    Kuzman JA, Gerdes AM, Kobayashi S, Liang Q. Thyroid hormone activates Akt and prevents serum starvation-induced cell death in neonatal rat cardiomyocytes. J Mol Cell Cardiol. 2005;39:841–4.PubMedCrossRefGoogle Scholar
  79. 79.
    Pantos C, Mourouzis I, Saranteas T, Clavé G, Ligeret H, Noack-Fraissignes P, et al. Thyroid hormone improves postischaemic recovery of function while limiting apoptosis: a new therapeutic approach to support hemodynamics in the setting of ischaemia-reperfusion? Basic Res Cardiol. 2009;104:69–77.PubMedCrossRefGoogle Scholar
  80. 80.
    Pantos C, Mourouzis I, Markakis K, Dimopoulos A, Xinaris C, Kokkinos AD, et al. Thyroid hormone attenuates cardiac remodeling and improves hemodynamics early after acute myocardial infarction in rats. Eur J Cardiothorac Surg. 2007;32:333–9.PubMedCrossRefGoogle Scholar
  81. 81.
    Rajagopalan V, Zhang Y, Ojamaa K, Chen YF, Pingitore A, Pol CJ, et al. Safe oral triiodo-L-thyronine therapy protects from post-infarct cardiac dysfunction and arrhythmias without cardiovascular adverse effects. PLoS One. 2016;11:e0151413.  https://doi.org/10.1371/journal.pone.0151413.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Rajagopalan V, Zhang Y, Pol C, Costello C, Seitter S, Lehto A, et al. Modified low-dose triiodo-L-thyronine therapy safely improves function following myocardial ischemia-reperfusion injury. Front Physiol. 2017;8:225.  https://doi.org/10.3389/fphys.2017.00225.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Henderson KK, Danzi S, Paul JT, Leya G, Klein I, Samarel AM. Physiological replacement of T3 improves left ventricular function in an animal model of myocardial infarction-induced congestive heart failure. Circ Heart Fail. 2009;2:243–52.PubMedCrossRefGoogle Scholar
  84. 84.
    De Castro AL, Fernandes RO, Ortiz VD, Campos C, Bonetto JHP, Fernandes TRG, et al. Thyroid hormones improve cardiac function and decrease expression of pro-apoptotic proteins in the heart of rats 14 days after infarction. Apoptosis. 2016;21:184–94.PubMedCrossRefGoogle Scholar
  85. 85.
    Chen J, Ortmeier SB, Savinova OV, Nareddy VB, Beyer AJ, Wang D, et al. Thyroid hormone induces sprouting angiogenesis in adult heart of hypothyroid mice through the PDGF-Akt pathway. J Cell Mol Med. 2012;16:2726–35.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Mourouzis I, Mantzouratou P, Galanopoulos G, Kostakou E, Roukounakis N, Kokkinos AD, et al. Dose-dependent effects of thyroid hormone on post-ischemic cardiac performance: potential involvement of Akt and ERK signalings. Mol Cell Biochem. 2012;363:235–43.PubMedCrossRefGoogle Scholar
  87. 87.
    Ghose Roy S, Mishra S, Ghosh G, Bandyopadhyay A. Thyroid hormone induces myocardial matrix degradation by activating matrix metalloproteinase-1. Matrix Biol. 2007;26:269–79.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Janssen R, Zuidwijk MJ, Kuster DW, Muller, Simonides WS. Thyroid hormone-regulated cardiac microRNAs are predicted to suppress pathological hypertrophic signaling. Front Endocrinol. 2014;5:171.  https://doi.org/10.3389/fendo.2014.00171.CrossRefGoogle Scholar
  89. 89.
    Janssen R, Zuidwijk MJ, Muller A, van Mil A, Dirkx E, Oudejans CB, et al. MicroRNA 214 is a potential regulator of thyroid hormone levels in the mouse heart following myocardial infarction, by targeting the thyroid-hormone-inactivating enzyme deiodinase type III. Front Endocrinol. 2016;7:22.  https://doi.org/10.3389/fendo.2016.00022.CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Institute of Clinical PhysiologyCNRPisaItaly

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