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Physiological and Pathological Cardiac Remodeling in Altered Thyroid Hormone States

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Thyroid and Heart

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Abstract

The heart responds to diverse stimuli by restructuring itself. Global remodeling is regulated by changes at the tissue, cellular, interstitial, biochemical, genetic and epigenetic levels. The transition from physiological compensation to decompensation has been a target for interventional strategies. Thyroid hormones (THs) also play a critical role in guiding this structural rearrangement. A balance in TH levels (both systemic and cellular) is vital for the adaptive regulation of remodeling, with hormone imbalance leading to maladaptive changes. TH imbalance can result either primarily from changes in hormone release from the thyroid gland or secondarily from altered bioavailability at the peripheral organ level. Recent findings indicate that numerous cardiovascular diseases suffer from aberrant changes in TH-based molecular mechanisms resulting in remodeling at the cellular and organ levels. This chapter discusses mechanisms and significance of physiological and pathological cardiac remodeling processes in altered TH states.

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References

  1. Cohn JN, Ferrari R, Sharpe N. Cardiac remodeling—concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling. J Am Coll Cardiol. 2000;35(3):569–82.

    Article  CAS  PubMed  Google Scholar 

  2. Swynghedauw B. Molecular mechanisms of myocardial remodeling. Physiol Rev. 1999;79(1):215–62. https://doi.org/10.1152/physrev.1999.79.1.215.

    Article  CAS  PubMed  Google Scholar 

  3. Tham YK, Bernardo BC, Ooi JY, Weeks KL, McMullen JR. Pathophysiology of cardiac hypertrophy and heart failure: signaling pathways and novel therapeutic targets. Arch Toxicol. 2015;89(9):1401–38. https://doi.org/10.1007/s00204-015-1477-x.

    Article  CAS  PubMed  Google Scholar 

  4. Opie LH, Commerford PJ, Gersh BJ, Pfeffer MA. Controversies in ventricular remodelling. Lancet. 2006;367(9507):356–67. https://doi.org/10.1016/S0140-6736(06)68074-4.

    Article  PubMed  Google Scholar 

  5. Tamura T, Said S, Harris J, Lu W, Gerdes AM. Reverse remodeling of cardiac myocyte hypertrophy in hypertension and failure by targeting of the renin-angiotensin system. Circulation. 2000;102(2):253–9.

    Article  CAS  PubMed  Google Scholar 

  6. Kao DP, Lowes BD, Gilbert EM, Minobe W, Epperson LE, Meyer LK, et al. Therapeutic molecular phenotype of beta-blocker-associated reverse-remodeling in nonischemic dilated cardiomyopathy. Circ Cardiovasc Genet. 2015;8(2):270–83. https://doi.org/10.1161/CIRCGENETICS.114.000767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wohlschlaeger J, Schmitz KJ, Schmid C, Schmid KW, Keul P, Takeda A, et al. Reverse remodeling following insertion of left ventricular assist devices (LVAD): a review of the morphological and molecular changes. Cardiovasc Res. 2005;68(3):376–86. https://doi.org/10.1016/j.cardiores.2005.06.030.

    Article  CAS  PubMed  Google Scholar 

  8. Park JH, Negishi K, Grimm RA, Popovic Z, Stanton T, Wilkoff BL, et al. Echocardiographic predictors of reverse remodeling after cardiac resynchronization therapy and subsequent events. Circ Cardiovasc Imaging. 2013;6(6):864–72. https://doi.org/10.1161/CIRCIMAGING.112.000026.

    Article  PubMed  Google Scholar 

  9. Takeda K, Taniguchi K, Shudo Y, Kainuma S, Hamada S, Matsue H, et al. Mechanism of beneficial effects of restrictive mitral annuloplasty in patients with dilated cardiomyopathy and functional mitral regurgitation. Circulation. 2010;122(11 Suppl):S3–9. https://doi.org/10.1161/CIRCULATIONAHA.109.927855.

    Article  PubMed  Google Scholar 

  10. Stulak JM, Suri RM, Dearani JA, Burkhart HM, Sundt TM III, Enriquez-Sarano M, et al. Does early surgical intervention improve left ventricular mass regression after mitral valve repair for leaflet prolapse? J Thorac Cardiovasc Surg. 2011;141(1):122–9. https://doi.org/10.1016/j.jtcvs.2010.08.068.

    Article  PubMed  Google Scholar 

  11. Gerdes AM, Clark LC, Capasso JM. Regression of cardiac hypertrophy after closing an aortocaval fistula in rats. Am J Phys. 1995;268(6 Pt 2):H2345–51. https://doi.org/10.1152/ajpheart.1995.268.6.H2345.

    Article  CAS  Google Scholar 

  12. Wong M, Staszewsky L, Latini R, Barlera S, Volpi A, Chiang YT, et al. Valsartan benefits left ventricular structure and function in heart failure: Val-HeFT echocardiographic study. J Am Coll Cardiol. 2002;40(5):970–5.

    Article  CAS  PubMed  Google Scholar 

  13. Birks EJ, Tansley PD, Hardy J, George RS, Bowles CT, Burke M, et al. Left ventricular assist device and drug therapy for the reversal of heart failure. N Engl J Med. 2006;355(18):1873–84. https://doi.org/10.1056/NEJMoa053063.

    Article  CAS  PubMed  Google Scholar 

  14. Kramer DG, Trikalinos TA, Kent DM, Antonopoulos GV, Konstam MA, Udelson JE. Quantitative evaluation of drug or device effects on ventricular remodeling as predictors of therapeutic effects on mortality in patients with heart failure and reduced ejection fraction: a meta-analytic approach. J Am Coll Cardiol. 2010;56(5):392–406. https://doi.org/10.1016/j.jacc.2010.05.011.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Rajagopalan V, Gerdes AM. Role of thyroid hormones in ventricular remodeling. Curr Heart Fail Rep. 2015;12(2):141–9. https://doi.org/10.1007/s11897-014-0246-0.

    Article  CAS  PubMed  Google Scholar 

  16. 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(16):1781–96. https://doi.org/10.1016/j.jacc.2018.02.045.

    Article  CAS  PubMed  Google Scholar 

  17. Klein I, Danzi S. Thyroid disease and the heart. Circulation. 2007;116(15):1725–35. https://doi.org/10.1161/CIRCULATIONAHA.106.678326.

    Article  PubMed  Google Scholar 

  18. Lortet S, Zimmer HG, Rossi A. Inotropic response of the rat heart during development and regression of triiodothyronine-induced hypertrophy. J Cardiovasc Pharmacol. 1989;14(5):707–12.

    Article  CAS  PubMed  Google Scholar 

  19. Zierhut W, Zimmer HG. Differential effects of triiodothyronine on rat left and right ventricular function and the influence of metoprolol. J Mol Cell Cardiol. 1989;21(6):617–24.

    Article  CAS  PubMed  Google Scholar 

  20. Gerdes AM, Moore JA, Bishop SP. Failure of propranolol to prevent chronic hyperthyroid induced cardiac hypertrophy and multifocal cellular necrosis in the rat. Can J Cardiol. 1985;1(5):340–5.

    CAS  PubMed  Google Scholar 

  21. Weltman NY, Wang D, Redetzke RA, Gerdes AM. Longstanding hyperthyroidism is associated with normal or enhanced intrinsic cardiomyocyte function despite decline in global cardiac function. PLoS One. 2012;7(10):e46655. https://doi.org/10.1371/journal.pone.0046655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Campbell SE, Gerdes AM. Regional changes in myocyte size during the reversal of thyroid-induced cardiac hypertrophy. J Mol Cell Cardiol. 1988;20(5):379–87.

    Article  CAS  PubMed  Google Scholar 

  23. Olivieri A, Stazi MA, Mastroiacovo P, Fazzini C, Medda E, Spagnolo A, et al. A population-based study on the frequency of additional congenital malformations in infants with congenital hypothyroidism: data from the Italian Registry for Congenital Hypothyroidism (1991-1998). J Clin Endocrinol Metab. 2002;87(2):557–62. https://doi.org/10.1210/jcem.87.2.8235.

    Article  CAS  PubMed  Google Scholar 

  24. Forhead AJ, Fowden AL. Thyroid hormones in fetal growth and prepartum maturation. J Endocrinol. 2014;221(3):R87–R103. https://doi.org/10.1530/JOE-14-0025.

    Article  CAS  PubMed  Google Scholar 

  25. Liu Z, Gerdes AM. Influence of hypothyroidism and the reversal of hypothyroidism on hemodynamics and cell size in the adult rat heart. J Mol Cell Cardiol. 1990;22(12):1339–48.

    Article  CAS  PubMed  Google Scholar 

  26. Liu Y, Sherer BA, Redetzke RA, Gerdes AM. Regulation of arteriolar density in adult myocardium during low thyroid conditions. Vasc Pharmacol. 2010;52(3–4):146–50. https://doi.org/10.1016/j.vph.2009.10.003.

    Article  CAS  Google Scholar 

  27. Chen YF, Redetzke RA, Said S, Beyer AJ, Gerdes AM. Changes in left ventricular function and remodeling after myocardial infarction in hypothyroid rats. Am J Physiol Heart Circ Physiol. 2010;298(1):H259–62. https://doi.org/10.1152/ajpheart.00755.2009.

    Article  CAS  PubMed  Google Scholar 

  28. Tang YD, Kuzman JA, Said S, Anderson BE, Wang X, Gerdes AM. Low thyroid function leads to cardiac atrophy with chamber dilatation, impaired myocardial blood flow, loss of arterioles, and severe systolic dysfunction. Circulation. 2005;112(20):3122–30. https://doi.org/10.1161/CIRCULATIONAHA.105.572883.

    Article  CAS  PubMed  Google Scholar 

  29. Zhang Y, Dedkov EI, Teplitsky D, Weltman NY, Pol CJ, Rajagopalan V, et al. Both hypothyroidism and hyperthyroidism increase atrial fibrillation inducibility in rats. Circ Arrhythm Electrophysiol. 2013;6(5):952–9. https://doi.org/10.1161/CIRCEP.113.000502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jabbar A, Pingitore A, Pearce SH, Zaman A, Iervasi G, Razvi S. Thyroid hormones and cardiovascular disease. Nat Rev Cardiol. 2017;14(1):39–55. https://doi.org/10.1038/nrcardio.2016.174.

    Article  CAS  PubMed  Google Scholar 

  31. Gerdes AM. Restoration of thyroid hormone balance: a game changer in the treatment of heart failure? Am J Physiol Heart Circ Physiol. 2015;308(1):H1–10. https://doi.org/10.1152/ajpheart.00704.2014.

    Article  CAS  PubMed  Google Scholar 

  32. Gerdes AM, Iervasi G. Thyroid replacement therapy and heart failure. Circulation. 2010;122(4):385–93. https://doi.org/10.1161/CIRCULATIONAHA.109.917922.

    Article  PubMed  Google Scholar 

  33. Zhang K, Meng X, Wang W, Zheng J, An S, Wang S, et al. Prognostic value of free triiodothyronine level in patients with hypertrophic obstructive cardiomyopathy. J Clin Endocrinol Metab. 2018;103(3):1198–205. https://doi.org/10.1210/jc.2017-02386.

    Article  PubMed  Google Scholar 

  34. Wang W, Guan H, Fang W, Zhang K, Gerdes AM, Iervasi G, et al. Free triiodothyronine level correlates with myocardial injury and prognosis in idiopathic dilated cardiomyopathy: evidence from cardiac MRI and SPECT/PET imaging. Sci Rep. 2016;6:39811. https://doi.org/10.1038/srep39811.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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(5):708–13.

    Article  PubMed  Google Scholar 

  36. Rodondi N, den Elzen WP, Bauer DC, Cappola AR, Razvi S, Walsh JP, et al. Subclinical hypothyroidism and the risk of coronary heart disease and mortality. JAMA. 2010;304(12):1365–74. https://doi.org/10.1001/jama.2010.1361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Wang W, Guan H, Gerdes AM, Iervasi G, Yang Y, Tang YD. Thyroid status, cardiac function, and mortality in patients with idiopathic dilated cardiomyopathy. J Clin Endocrinol Metab. 2015;100(8):3210–8. https://doi.org/10.1210/jc.2014-4159.

    Article  CAS  PubMed  Google Scholar 

  38. Marwali EM, Boom CE, Budiwardhana N, Fakhri D, Roebiono PS, Santoso A, et al. Oral triiodothyronine for infants and children undergoing cardiopulmonary bypass. Ann Thorac Surg. 2017;104(2):688–95. https://doi.org/10.1016/j.athoracsur.2017.01.001.

    Article  PubMed  Google Scholar 

  39. Mitchell JE, Hellkamp AS, Mark DB, Anderson J, Johnson GW, Poole JE, et al. Thyroid function in heart failure and impact on mortality. JACC Heart Fail. 2013;1(1):48–55. https://doi.org/10.1016/j.jchf.2012.10.004.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Passino C, Pingitore A, Landi P, Fontana M, Zyw L, Clerico A, et al. Prognostic value of combined measurement of brain natriuretic peptide and triiodothyronine in heart failure. J Card Fail. 2009;15(1):35–40. https://doi.org/10.1016/j.cardfail.2008.08.008.

    Article  CAS  PubMed  Google Scholar 

  41. Donzelli R, Colligiani D, Kusmic C, Sabatini M, Lorenzini L, Accorroni A, et al. Effect of hypothyroidism and hyperthyroidism on tissue thyroid hormone concentrations in rat. Eur Thyroid J. 2016;5(1):27–34. https://doi.org/10.1159/000443523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Weltman NY, Ojamaa K, Savinova OV, Chen YF, Schlenker EH, Zucchi R, et al. Restoration of cardiac tissue thyroid hormone status in experimental hypothyroidism: a dose-response study in female rats. Endocrinology. 2013;154(7):2542–52. https://doi.org/10.1210/en.2012-2087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Weltman NY, Pol CJ, Zhang Y, Wang Y, Koder A, Raza S, et al. Long-term physiological T3 supplementation in hypertensive heart disease in rats. Am J Physiol Heart Circ Physiol. 2015;309(6):H1059–65. https://doi.org/10.1152/ajpheart.00431.2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Weltman NY, Ojamaa K, Schlenker EH, Chen YF, Zucchi R, Saba A, et al. Low-dose T(3) replacement restores depressed cardiac T(3) levels, preserves coronary microvasculature and attenuates cardiac dysfunction in experimental diabetes mellitus. Mol Med. 2014;20:302–12. https://doi.org/10.2119/molmed.2013.00040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. 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(2):669–79. https://doi.org/10.1210/en.2010-0431.

    Article  CAS  PubMed  Google Scholar 

  46. Klemperer JD, Ojamaa K, Klein I. Thyroid hormone therapy in cardiovascular disease. Prog Cardiovasc Dis. 1996;38(4):329–36.

    Article  CAS  PubMed  Google Scholar 

  47. 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(4):1351–8. https://doi.org/10.1210/jc.2007-2210.

    Article  CAS  PubMed  Google Scholar 

  48. 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(3):514–24. https://doi.org/10.1111/j.1582-4934.2010.01014.x.

    Article  CAS  PubMed  Google Scholar 

  49. 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(3):e0151413. https://doi.org/10.1371/journal.pone.0151413.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhang K, Tang YD, Zhang Y, Ojamaa K, Li Y, Saini AS, et al. Comparison of therapeutic triiodothyronine versus metoprolol in the treatment of myocardial infarction in rats. Thyroid. 2018;28(6):799–810. https://doi.org/10.1089/thy.2017.0544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Pantos C, Mourouzis I, Tsagoulis N, Markakis K, Galanopoulos G, Roukounakis N, et al. Thyroid hormone at supra-physiological dose optimizes cardiac geometry and improves cardiac function in rats with old myocardial infarction. J Physiol Pharmacol. 2009;60(3):49–56.

    CAS  PubMed  Google Scholar 

  52. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Pantos C, Mourouzis I, Cokkinos DV. Rebuilding the post-infarcted myocardium by activating ‘physiologic’ hypertrophic signaling pathways: the thyroid hormone paradigm. Heart Fail Rev. 2010;15(2):143–54. https://doi.org/10.1007/s10741-008-9111-0.

    Article  CAS  PubMed  Google Scholar 

  54. 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(4):308–18. https://doi.org/10.1007/s00395-008-0697-0.

    Article  CAS  PubMed  Google Scholar 

  55. Pantos C, Mourouzis I, Saranteas T, Clave 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(1):69–77. https://doi.org/10.1007/s00395-008-0758-4.

    Article  CAS  PubMed  Google Scholar 

  56. Pantos CI, Malliopoulou VA, Mourouzis IS, Karamanoli EP, Paizis IA, Steimberg N, et al. Long-term thyroxine administration protects the heart in a pattern similar to ischemic preconditioning. Thyroid. 2002;12(4):325–9. https://doi.org/10.1089/10507250252949469.

    Article  CAS  PubMed  Google Scholar 

  57. Pingitore A, Nicolini G, Kusmic C, Iervasi G, Grigolini P, Forini F. Cardioprotection and thyroid hormones. Heart Fail Rev. 2016;21(4):391–9. https://doi.org/10.1007/s10741-016-9545-8.

    Article  CAS  PubMed  Google Scholar 

  58. 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(6):H2409–15. https://doi.org/10.1152/ajpheart.00483.2005.

    Article  CAS  PubMed  Google Scholar 

  59. Yao J, Eghbali M. Decreased collagen mRNA and regression of cardiac fibrosis in the ventricular myocardium of the tight skin mouse following thyroid hormone treatment. Cardiovasc Res. 1992;26(6):603–7.

    Article  CAS  PubMed  Google Scholar 

  60. Chen WJ, Lin KH, Lee YS. Molecular characterization of myocardial fibrosis during hypothyroidism: evidence for negative regulation of the pro-alpha1(I) collagen gene expression by thyroid hormone receptor. Mol Cell Endocrinol. 2000;162(1–2):45–55.

    Article  CAS  PubMed  Google Scholar 

  61. Lee HW, Klein LE, Raser J, Eghbali-Webb M. An activator protein-1 (AP-1) response element on pro alpha1(l) collagen gene is necessary for thyroid hormone-induced inhibition of promoter activity in cardiac fibroblasts. J Mol Cell Cardiol. 1998;30(11):2495–506. https://doi.org/10.1006/jmcc.1998.0811.

    Article  CAS  PubMed  Google Scholar 

  62. Kuzman JA, Tang Y, Vogelsang KA, Said S, Anderson BE, Morkin E, et al. Thyroid hormone analog, diiodothyropropionic acid (DITPA), exerts beneficial effects on chamber and cellular remodeling in cardiomyopathic hamsters. Can J Physiol Pharmacol. 2007;85(3–4):311–8. https://doi.org/10.1139/y07-011.

    Article  CAS  PubMed  Google Scholar 

  63. 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(5):H2118–22. https://doi.org/10.1152/ajpheart.01000.2004.

    Article  CAS  PubMed  Google Scholar 

  64. Novitzky D, Cooper DK. Thyroid hormone and the stunned myocardium. J Endocrinol. 2014;223(1):R1–8. https://doi.org/10.1530/JOE-14-0389.

    Article  CAS  PubMed  Google Scholar 

  65. Files MD, Kajimoto M, O'Kelly Priddy CM, Ledee DR, Xu C, Des Rosiers C, et al. Triiodothyronine facilitates weaning from extracorporeal membrane oxygenation by improved mitochondrial substrate utilization. J Am Heart Assoc. 2014;3(2):e000680. https://doi.org/10.1161/JAHA.113.000680.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Talwar S, Bhoje A, Khadagawat R, Chaturvedi P, Sreenivas V, Makhija N, et al. Oral thyroxin supplementation in infants undergoing cardiac surgery: a double-blind placebo-controlled randomized clinical trial. J Thorac Cardiovasc Surg. 2018;156(3):1209–17.e3. https://doi.org/10.1016/j.jtcvs.2018.05.044.

    Article  CAS  PubMed  Google Scholar 

  67. Gerdes AM. Cardiomyocyte ultrastructure. Muscle: fundamental biology and mechanisms of disease, 1st ed. Elsevier Inc.; 2012.

    Google Scholar 

  68. Campbell SE, Korecky B, Rakusan K. Remodeling of myocyte dimensions in hypertrophic and atrophic rat hearts. Circ Res. 1991;68(4):984–96.

    Article  CAS  PubMed  Google Scholar 

  69. Li F, McNelis MR, Lustig K, Gerdes AM. Hyperplasia and hypertrophy of chicken cardiac myocytes during posthatching development. Am J Phys. 1997;273(2 Pt 2):R518–26. https://doi.org/10.1152/ajpregu.1997.273.2.R518.

    Article  CAS  Google Scholar 

  70. Li F, Wang X, Capasso JM, Gerdes AM. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol. 1996;28(8):1737–46. https://doi.org/10.1006/jmcc.1996.0163.

    Article  CAS  PubMed  Google Scholar 

  71. Grant C, Greene DG, Bunnell IL. Left ventricular enlargement and hypertrophy. A clinical and angiocardiographic study. Am J Med. 1965;39(6):895–904.

    Article  CAS  PubMed  Google Scholar 

  72. Grossman W, Jones D, McLaurin LP. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest. 1975;56(1):56–64. https://doi.org/10.1172/JCI108079.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Gerdes AM, Moore JA, Hines JM, Kirkland PA, Bishop SP. Regional differences in myocyte size in normal rat heart. Anat Rec. 1986;215(4):420–6. https://doi.org/10.1002/ar.1092150414.

    Article  CAS  PubMed  Google Scholar 

  74. Gerdes AM. Cardiac myocyte remodeling in hypertrophy and progression to failure. J Card Fail. 2002;8(6 Suppl):S264–8. https://doi.org/10.1054/jcaf.2002.129280.

    Article  PubMed  Google Scholar 

  75. Zimmer HG, Gerdes AM, Lortet S, Mall G. Changes in heart function and cardiac cell size in rats with chronic myocardial infarction. J Mol Cell Cardiol. 1990;22(11):1231–43.

    Article  CAS  PubMed  Google Scholar 

  76. Kajstura J, Zhang X, Liu Y, Szoke E, Cheng W, Olivetti G, et al. The cellular basis of pacing-induced dilated cardiomyopathy. Myocyte cell loss and myocyte cellular reactive hypertrophy. Circulation. 1995;92(8):2306–17.

    Article  CAS  PubMed  Google Scholar 

  77. Kramer CM, Rogers WJ, Park CS, Seibel PS, Shaffer A, Theobald TM, et al. Regional myocyte hypertrophy parallels regional myocardial dysfunction during post-infarct remodeling. J Mol Cell Cardiol. 1998;30(9):1773–8. https://doi.org/10.1006/jmcc.1998.0741.

    Article  CAS  PubMed  Google Scholar 

  78. Gerdes AM, Kellerman SE, Moore JA, Muffly KE, Clark LC, Reaves PY, et al. Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation. 1992;86(2):426–30.

    Article  CAS  PubMed  Google Scholar 

  79. Zafeiridis A, Jeevanandam V, Houser SR, Margulies KB. Regression of cellular hypertrophy after left ventricular assist device support. Circulation. 1998;98(7):656–62.

    Article  CAS  PubMed  Google Scholar 

  80. Gerdes AM. How to improve the overall quality of cardiac morphometric data. Am J Physiol Heart Circ Physiol. 2015;309(1):H9–H14. https://doi.org/10.1152/ajpheart.00232.2015.

    Article  CAS  PubMed  Google Scholar 

  81. Gerdes AM. The use of isolated myocytes to evaluate myocardial remodeling. Trends Cardiovasc Med. 1992;2(4):152–5. https://doi.org/10.1016/1050-1738(92)90023-L.

    Article  CAS  PubMed  Google Scholar 

  82. Gerdes AM, Pingitore A. Assessment of cardiomyocyte size. Manual of research techniques in cardiovascular medicine. Oxford: Wiley; 2014.

    Google Scholar 

  83. Gerdes AM, Holder MS. Cardiac myocyte structural remodeling. In: Greenberg B, editor. Cardiac remodeling mechanisms and treatment. 1st ed. Boca Raton: CRC Press; 2005.

    Google Scholar 

  84. Tamura T, Onodera T, Said S, Gerdes AM. Correlation of myocyte lengthening to chamber dilation in the spontaneously hypertensive heart failure (SHHF) rat. J Mol Cell Cardiol. 1998;30(11):2175–81. https://doi.org/10.1006/jmcc.1998.0775.

    Article  CAS  PubMed  Google Scholar 

  85. Goktepe S, Abilez OJ, Parker KK, Kuhl E. A multiscale model for eccentric and concentric cardiac growth through sarcomerogenesis. J Theor Biol. 2010;265(3):433–42. https://doi.org/10.1016/j.jtbi.2010.04.023.

    Article  PubMed  Google Scholar 

  86. Wang VY, Hussan JR, Yousefi H, Bradley CP, Hunter PJ, Nash MP. Modelling cardiac tissue growth and remodelling. J Elast. 2017;129(1–2):283–305.

    Article  Google Scholar 

  87. Li M, Iismaa SE, Naqvi N, Nicks A, Husain A, Graham RM. Thyroid hormone action in postnatal heart development. Stem Cell Res. 2014;13(3 Pt B):582–91. https://doi.org/10.1016/j.scr.2014.07.001.

    Article  CAS  PubMed  Google Scholar 

  88. Gerdes AM, Kriseman J, Bishop SP. Changes in myocardial cell size and number during the development and reversal of hyperthyroidism in neonatal rats. Lab Invest. 1983;48(5):598–602.

    CAS  PubMed  Google Scholar 

  89. Gerdes AM, Moore JA, Hines JM. Regional changes in myocyte size and number in propranolol-treated hyperthyroid rats. Lab Invest. 1987;57(6):708–13.

    CAS  PubMed  Google Scholar 

  90. Bai SL, Campbell SE, Moore JA, Morales MC, Gerdes AM. Influence of age, growth, and sex on cardiac myocyte size and number in rats. Anat Rec. 1990;226(2):207–12. https://doi.org/10.1002/ar.1092260210.

    Article  CAS  PubMed  Google Scholar 

  91. Schaub MC, Hefti MA, Harder BA, Eppenberger HM. Triiodothyronine restricts myofibrillar growth and enhances beating frequency in cultured adult rat cardiomyocytes. Basic Res Cardiol. 1998;93(5):391–5.

    Article  CAS  PubMed  Google Scholar 

  92. Shao Q, Cheng HJ, Callahan MF, Kitzman DW, Li WM, Cheng CP. Overexpression myocardial inducible nitric oxide synthase exacerbates cardiac dysfunction and beta-adrenergic desensitization in experimental hypothyroidism. Int J Cardiol. 2016;204:229–41. https://doi.org/10.1016/j.ijcard.2015.11.040.

    Article  PubMed  Google Scholar 

  93. Chen YF, Weltman NY, Li X, Youmans S, Krause D, Gerdes AM. Improvement of left ventricular remodeling after myocardial infarction with eight weeks L-thyroxine treatment in rats. J Transl Med. 2013;11:40. https://doi.org/10.1186/1479-5876-11-40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Savinova OV, Gerdes AM. Myocyte changes in heart failure. Heart Fail Clin. 2012;8(1):1–6. https://doi.org/10.1016/j.hfc.2011.08.004.

    Article  PubMed  Google Scholar 

  95. Gerdes AM, Ojamaa K. Thyroid hormone and cardioprotection. Compr Physiol. 2016;6(3):1199–219. https://doi.org/10.1002/cphy.c150012.

    Article  PubMed  Google Scholar 

  96. Re A, Nanni S, Aiello A, Granata S, Colussi C, Campostrini G, et al. Anacardic acid and thyroid hormone enhance cardiomyocytes production from undifferentiated mouse ES cells along functionally distinct pathways. Endocrine. 2016;53(3):681–8. https://doi.org/10.1007/s12020-015-0751-2.

    Article  CAS  PubMed  Google Scholar 

  97. Lee YK, Ng KM, Chan YC, Lai WH, Au KW, Ho CY, et al. Triiodothyronine promotes cardiac differentiation and maturation of embryonic stem cells via the classical genomic pathway. Mol Endocrinol. 2010;24(9):1728–36. https://doi.org/10.1210/me.2010-0032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Jackman C, Li H, Bursac N. Long-term contractile activity and thyroid hormone supplementation produce engineered rat myocardium with adult-like structure and function. Acta Biomater. 2018;78:98–110. https://doi.org/10.1016/j.actbio.2018.08.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Schwan J, Kwaczala AT, Ryan TJ, Bartulos O, Ren Y, Sewanan LR, et al. Anisotropic engineered heart tissue made from laser-cut decellularized myocardium. Sci Rep. 2016;6:32068. https://doi.org/10.1038/srep32068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Yang X, Rodriguez M, Pabon L, Fischer KA, Reinecke H, Regnier M, et al. Tri-iodo-l-thyronine promotes the maturation of human cardiomyocytes-derived from induced pluripotent stem cells. J Mol Cell Cardiol. 2014;72:296–304. https://doi.org/10.1016/j.yjmcc.2014.04.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Poon E, Keung W, Liang Y, Ramalingam R, Yan B, Zhang S, et al. Proteomic analysis of human pluripotent stem cell-derived, fetal, and adult ventricular cardiomyocytes reveals pathways crucial for cardiac metabolism and maturation. Circ Cardiovasc Genet. 2015;8(3):427–36. https://doi.org/10.1161/CIRCGENETICS.114.000918.

    Article  CAS  PubMed  Google Scholar 

  102. Naito H, Melnychenko I, Didie M, Schneiderbanger K, Schubert P, Rosenkranz S, et al. Optimizing engineered heart tissue for therapeutic applications as surrogate heart muscle. Circulation. 2006;114(1 Suppl):I72–8. https://doi.org/10.1161/CIRCULATIONAHA.105.001560.

    Article  PubMed  Google Scholar 

  103. Birket MJ, Ribeiro MC, Kosmidis G, Ward D, Leitoguinho AR, van de Pol V, et al. Contractile defect caused by mutation in MYBPC3 revealed under conditions optimized for human PSC-cardiomyocyte function. Cell Rep. 2015;13(4):733–45. https://doi.org/10.1016/j.celrep.2015.09.025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Parikh SS, Blackwell DJ, Gomez-Hurtado N, Frisk M, Wang L, Kim K, et al. Thyroid and glucocorticoid hormones promote functional T-tubule development in human-induced pluripotent stem cell-derived cardiomyocytes. Circ Res. 2017;121(12):1323–30. https://doi.org/10.1161/CIRCRESAHA.117.311920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Burchfield JS, Xie M, Hill JA. Pathological ventricular remodeling: mechanisms: part 1 of 2. Circulation. 2013;128(4):388–400. https://doi.org/10.1161/CIRCULATIONAHA.113.001878.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Xie M, Burchfield JS, Hill JA. Pathological ventricular remodeling: therapies: part 2 of 2. Circulation. 2013;128(9):1021–30. https://doi.org/10.1161/CIRCULATIONAHA.113.001879.

    Article  PubMed  Google Scholar 

  107. Cappola TP. Molecular remodeling in human heart failure. J Am Coll Cardiol. 2008;51(2):137–8. https://doi.org/10.1016/j.jacc.2007.09.028.

    Article  PubMed  Google Scholar 

  108. Zhao M, Fajardo G, Urashima T, Spin JM, Poorfarahani S, Rajagopalan V, et al. Cardiac pressure overload hypertrophy is differentially regulated by beta-adrenergic receptor subtypes. Am J Physiol Heart Circ Physiol. 2011;301(4):H1461–70. https://doi.org/10.1152/ajpheart.00453.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Maillet M, van Berlo JH, Molkentin JD. Molecular basis of physiological heart growth: fundamental concepts and new players. Nat Rev Mol Cell Biol. 2013;14(1):38–48. https://doi.org/10.1038/nrm3495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Kellerman S, Moore JA, Zierhut W, Zimmer HG, Campbell J, Gerdes AM. Nuclear DNA content and nucleation patterns in rat cardiac myocytes from different models of cardiac hypertrophy. J Mol Cell Cardiol. 1992;24(5):497–505.

    Article  CAS  PubMed  Google Scholar 

  111. Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev. 2005;26(5):704–28. https://doi.org/10.1210/er.2003-0033.

    Article  CAS  PubMed  Google Scholar 

  112. Brent GA. Mechanisms of thyroid hormone action. J Clin Invest. 2012;122(9):3035–43. https://doi.org/10.1172/JCI60047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Edwards JG, Bahl JJ, Flink IL, Cheng SY, Morkin E. Thyroid hormone influences beta myosin heavy chain (beta MHC) expression. Biochem Biophys Res Commun. 1994;199(3):1482–8. https://doi.org/10.1006/bbrc.1994.1398.

    Article  CAS  PubMed  Google Scholar 

  114. Le Bouter S, Demolombe S, Chambellan A, Bellocq C, Aimond F, Toumaniantz G, et al. Microarray analysis reveals complex remodeling of cardiac ion channel expression with altered thyroid status: relation to cellular and integrated electrophysiology. Circ Res. 2003;92(2):234–42.

    Article  PubMed  Google Scholar 

  115. Degens H, Gilde AJ, Lindhout M, Willemsen PH, Van Der Vusse GJ, Van Bilsen M. Functional and metabolic adaptation of the heart to prolonged thyroid hormone treatment. Am J Physiol Heart Circ Physiol. 2003;284(1):H108–15. https://doi.org/10.1152/ajpheart.00282.2002.

    Article  CAS  PubMed  Google Scholar 

  116. Chen YF, Pottala JV, Weltman NY, Ge X, Savinova OV, Gerdes AM. Regulation of gene expression with thyroid hormone in rats with myocardial infarction. PLoS One. 2012;7(8):e40161. https://doi.org/10.1371/journal.pone.0040161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. 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(11):26687–705. https://doi.org/10.3390/ijms161125973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Janssen R, Zuidwijk M, Muller A, Mulders J, Oudejans CB, Simonides WS. Cardiac expression of deiodinase type 3 (Dio3) following myocardial infarction is associated with the induction of a pluripotency microRNA signature from the Dlk1-Dio3 genomic region. Endocrinology. 2013;154(6):1973–8. https://doi.org/10.1210/en.2012-2017.

    Article  CAS  PubMed  Google Scholar 

  119. Janssen R, Zuidwijk MJ, Kuster DW, Muller A, 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.

    Article  Google Scholar 

  120. Gil-Cayuela C, Rosello LE, Tarazon E, Ortega A, Sandoval J, Martinez-Dolz L, et al. Thyroid hormone biosynthesis machinery is altered in the ischemic myocardium: An epigenomic study. Int J Cardiol. 2017;243:27–33. https://doi.org/10.1016/j.ijcard.2017.05.042.

    Article  PubMed  Google Scholar 

  121. Gil-Cayuela C, Ortega A, Tarazon E, Martinez-Dolz L, Cinca J, Gonzalez-Juanatey JR, et al. Myocardium of patients with dilated cardiomyopathy presents altered expression of genes involved in thyroid hormone biosynthesis. PLoS One. 2018;13(1):e0190987. https://doi.org/10.1371/journal.pone.0190987.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. 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(1):180–7. https://doi.org/10.1016/j.yjmcc.2007.09.009.

    Article  CAS  PubMed  Google Scholar 

  123. 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(5):841–4. https://doi.org/10.1016/j.yjmcc.2005.07.019.

    Article  CAS  PubMed  Google Scholar 

  124. Kuzman JA, Vogelsang KA, Thomas TA, Gerdes AM. L-Thyroxine activates Akt signaling in the heart. J Mol Cell Cardiol. 2005;39(2):251–8. https://doi.org/10.1016/j.yjmcc.2005.03.020.

    Article  CAS  PubMed  Google Scholar 

  125. 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(1–2):173–80.

    Article  CAS  PubMed  Google Scholar 

  126. Kenessey A, Ojamaa K. Thyroid hormone stimulates protein synthesis in the cardiomyocyte by activating the Akt-mTOR and p70S6K pathways. J Biol Chem. 2006;281(30):20666–72. https://doi.org/10.1074/jbc.M512671200.

    Article  CAS  PubMed  Google Scholar 

  127. Kehat I, Davis J, Tiburcy M, Accornero F, Saba-El-Leil MK, Maillet M, et al. Extracellular signal-regulated kinases 1 and 2 regulate the balance between eccentric and concentric cardiac growth. Circ Res. 2011;108(2):176–83. https://doi.org/10.1161/CIRCRESAHA.110.231514.

    Article  CAS  PubMed  Google Scholar 

  128. Suarez J, Scott BT, Suarez-Ramirez JA, Chavira CV, Dillmann WH. Thyroid hormone inhibits ERK phosphorylation in pressure overload-induced hypertrophied mouse hearts through a receptor-mediated mechanism. Am J Physiol Cell Physiol. 2010;299(6):C1524–9. https://doi.org/10.1152/ajpcell.00168.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Pantos C, Mourouzis I, Galanopoulos G, Gavra M, Perimenis P, Spanou D, et al. Thyroid hormone receptor alpha1 downregulation in postischemic heart failure progression: the potential role of tissue hypothyroidism. Horm Metab Res. 2010;42(10):718–24. https://doi.org/10.1055/s-0030-1255035.

    Article  CAS  PubMed  Google Scholar 

  130. Adamopoulos S, Gouziouta A, Mantzouratou P, Laoutaris ID, Dritsas A, Cokkinos DV, et al. Thyroid hormone signalling is altered in response to physical training in patients with end-stage heart failure and mechanical assist devices: potential physiological consequences? Interact Cardiovasc Thorac Surg. 2013;17(4):664–8. https://doi.org/10.1093/icvts/ivt294.

    Article  PubMed  PubMed Central  Google Scholar 

  131. Wang B, Ouyang J, Xia Z. Effects of triiodo-thyronine on angiotensin-induced cardiomyocyte hypertrophy: reversal of increased beta-myosin heavy chain gene expression. Can J Physiol Pharmacol. 2006;84(8–9):935–41. https://doi.org/10.1139/y06-043.

    Article  CAS  PubMed  Google Scholar 

  132. Barreto-Chaves ML, Carrillo-Sepulveda MA, Carneiro-Ramos MS, Gomes DA, Diniz GP. The crosstalk between thyroid hormones and the renin-angiotensin system. Vasc Pharmacol. 2010;52(3–4):166–70. https://doi.org/10.1016/j.vph.2009.10.009.

    Article  CAS  Google Scholar 

  133. Montalvo D, Perez-Trevino P, Madrazo-Aguirre K, Gonzalez-Mondellini FA, Miranda-Roblero HO, Ramonfaur-Gracia D, et al. Underlying mechanism of the contractile dysfunction in atrophied ventricular myocytes from a murine model of hypothyroidism. Cell Calcium. 2018;72:26–38. https://doi.org/10.1016/j.ceca.2018.01.005.

    Article  CAS  PubMed  Google Scholar 

  134. Ojamaa K, Kenessey A, Shenoy R, Klein I. Thyroid hormone metabolism and cardiac gene expression after acute myocardial infarction in the rat. Am J Physiol Endocrinol Metab. 2000;279(6):E1319–24. https://doi.org/10.1152/ajpendo.2000.279.6.E1319.

    Article  CAS  PubMed  Google Scholar 

  135. 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 miR30a/p53 axis. Endocrinology. 2014;155(11):4581–90. https://doi.org/10.1210/en.2014-1106.

    Article  CAS  PubMed  Google Scholar 

  136. 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.

    Article  Google Scholar 

  137. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Quan X, Ji Y, Zhang C, Guo X, Zhang Y, Jia S, et al. Circulating MiR-146a may be a potential biomarker of coronary heart disease in patients with subclinical hypothyroidism. Cell Physiol Biochem. 2018;45(1):226–36. https://doi.org/10.1159/000486769.

    Article  CAS  PubMed  Google Scholar 

  139. Diniz GP, Lino CA, Moreno CR, Senger N, Barreto-Chaves MLM. MicroRNA-1 overexpression blunts cardiomyocyte hypertrophy elicited by thyroid hormone. J Cell Physiol. 2017;232(12):3360–8. https://doi.org/10.1002/jcp.25781.

    Article  CAS  PubMed  Google Scholar 

  140. Janssen R, Muller A, Simonides WS. Cardiac thyroid hormone metabolism and heart failure. Eur Thyroid J. 2017;6(3):130–7. https://doi.org/10.1159/000469708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Kruger M, Sachse C, Zimmermann WH, Eschenhagen T, Klede S, Linke WA. Thyroid hormone regulates developmental titin isoform transitions via the phosphatidylinositol-3-kinase/AKT pathway. Circ Res. 2008;102(4):439–47. https://doi.org/10.1161/CIRCRESAHA.107.162719.

    Article  CAS  PubMed  Google Scholar 

  142. Ghose Roy S, Mishra S, Ghosh G, Bandyopadhyay A. Thyroid hormone induces myocardial matrix degradation by activating matrix metalloproteinase-1. Matrix Biol. 2007;26(4):269–79. https://doi.org/10.1016/j.matbio.2006.12.005.

    Article  CAS  PubMed  Google Scholar 

  143. Yao J, Eghbali M. Decreased collagen gene expression and absence of fibrosis in thyroid hormone-induced myocardial hypertrophy. Response of cardiac fibroblasts to thyroid hormone in vitro. Circ Res. 1992;71(4):831–9.

    Article  CAS  PubMed  Google Scholar 

  144. Ledee D, Portman MA, Kajimoto M, Isern N, Olson AK. Thyroid hormone reverses aging-induced myocardial fatty acid oxidation defects and improves the response to acutely increased afterload. PLoS One. 2013;8(6):e65532. https://doi.org/10.1371/journal.pone.0065532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Olson AK, Bouchard B, Ning XH, Isern N, Rosiers CD, Portman MA. Triiodothyronine increases myocardial function and pyruvate entry into the citric acid cycle after reperfusion in a model of infant cardiopulmonary bypass. Am J Physiol Heart Circ Physiol. 2012;302(5):H1086–93. https://doi.org/10.1152/ajpheart.00959.2011.

    Article  CAS  PubMed  Google Scholar 

  146. Kajimoto M, Ledee DR, Xu C, Kajimoto H, Isern NG, Portman MA. Triiodothyronine activates lactate oxidation without impairing fatty acid oxidation and improves weaning from extracorporeal membrane oxygenation. Circ J. 2014;78(12):2867–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Shi ST, Wu XX, Hao W, Wang X, Miao HT, Zhen L, et al. Triiodo-L-thyronine promotes the maturation of cardiomyocytes derived from rat bone marrow mesenchymal stem cells. J Cardiovasc Pharmacol. 2016;67(5):388–93. https://doi.org/10.1097/FJC.0000000000000363.

    Article  CAS  PubMed  Google Scholar 

  148. Ivashchenko CY, Pipes GC, Lozinskaya IM, Lin Z, Xiaoping X, Needle S, et al. Human-induced pluripotent stem cell-derived cardiomyocytes exhibit temporal changes in phenotype. Am J Physiol Heart Circ Physiol. 2013;305(6):H913–22. https://doi.org/10.1152/ajpheart.00819.2012.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. New York Institute of Technology, College of Osteopathic Medicine at A-State, Jonesboro, AR, USA

    Viswanathan Rajagopalan

  2. NYITCOM College of Osteopathic Medicine Biomedical Sciences Department, Old Westbury, NY, USA

    A. Martin Gerdes

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  1. Institute of Clinical Physiology (IFC) National Research Council (CNR), Pisa, Italy

    Giorgio Iervasi

  2. Institute of Clinical Physiology (IFC) National Research Council (CNR), Pisa, Italy

    Alessandro Pingitore

  3. NYITCOM College of Osteopathic Medicine Biomedical Sciences Department, Old Westbury, NY, USA

    A.Martin Gerdes

  4. Institute of Clinical and Translational Medicine, Newcastle University/Queen Elizabeth Hospital, Newcastle upon Tyne, UK

    Salman Razvi

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Rajagopalan, V., Gerdes, A.M. (2020). Physiological and Pathological Cardiac Remodeling in Altered Thyroid Hormone States. In: Iervasi, G., Pingitore, A., Gerdes, A., Razvi, S. (eds) Thyroid and Heart . Springer, Cham. https://doi.org/10.1007/978-3-030-36871-5_11

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