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Thyroid Hormone Signaling Mechanisms in the Heart and Vasculature

  • Kaie OjamaaEmail author
  • Maria Alicia Carrillo-Sepulveda
Chapter
  • 33 Downloads

Abstract

Thyroid hormones regulate cardiac development, and in the adult, these hormones play key roles in cardiac growth, metabolism, and function. The complexity of thyroid hormone signaling in the cell has recently come into sharper focus with reports of functional thyroid hormone receptors localized in the cytosolic, mitochondrial, and membrane-associated compartments as well as the nucleus. Thus, categorizing thyroid hormone action as genomic or non-genomic will require revision. This review presents a broad overview of known mechanisms of action of these hormones in the heart and vasculature with a discussion of effects on cardiac function and vascular reactivity in normal and diseased settings.

Keywords

Thyroid hormones Triiodothyronine Heart Myocardium Vascular Contractility Calcium T-tubules Ion channels T3 receptors Transcription Non-genomic Genomic 

Notes

Acknowledgment

The authors declare that they have no conflicts of interest regarding the content discussed in this review article.

References

  1. 1.
    Oppenheimer JH, Schwartz HL, Surks MI, Koerner D, Dillmann WH. Nuclear receptors and the initiation of thyroid hormone action. Recent Prog Horm Res. 1976;32:529–65.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Samuels HH, Tsai JS, Casanova J. Thyroid hormone action: in vitro demonstration of putative receptors in isolated nuclei and soluble nuclear extracts. Science. 1974;184(4142):1188–91.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Sap J, Munoz A, Damm K, Goldberg Y, Ghysdael J, Leutz A, et al. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature. 1986;324(6098):635–40.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Thompson CC, Weinberger C, Lebo R, Evans RM. Identification of a novel thyroid hormone receptor expressed in the mammalian central nervous system. Science. 1987;237(4822):1610–4.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Weinberger C, Thompson CC, Ong ES, Lebo R, Gruol DJ, Evans RM. The c-erb-A gene encodes a thyroid hormone receptor. Nature. 1986;324(6098):641–6.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Evans RM, Mangelsdorf DJ. Nuclear receptors, RXR, and the big bang. Cell. 2014;157(1):255–66.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Davis FB, Cody V, Davis PJ, Borzynski LJ, Blas SD. Stimulation by thyroid hormone analogues of red blood cell Ca2+-ATPase activity in vitro. Correlations between hormone structure and biological activity in a human cell system. J Biol Chem. 1983;258(20):12373–7.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Galo MG, Unates LE, Farias RN. Effect of membrane fatty acid composition on the action of thyroid hormones on (Ca2+ + Mg2+)-adenosine triphosphatase from rat erythrocyte. J Biol Chem. 1981;256(14):7113–4.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Binah O, Rubinstein I, Gilat E. Effects of thyroid hormone on the action potential and membrane currents of Guinea pig ventricular myocytes. Pflugers Arch. 1987;409(1–2):214–6.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Segal J. Calcium is the first messenger for the action of thyroid hormone at the level of the plasma membrane: first evidence for an acute effect of thyroid hormone on calcium uptake in the heart. Endocrinology. 1990;126(5):2693–702.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Angel RC, Botta JA, Farias RN. High affinity L-triiodothyronine binding to right-side-out and inside-out vesicles from rat and human erythrocyte membrane. J Biol Chem. 1989;264(32):19143–6.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature. 2000;407(6803):538–41.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Hiroi Y, Kim HH, 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(38):14104–9.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Cao X, Kambe F, Moeller LC, Refetoff S, Seo H. Thyroid hormone induces rapid activation of Akt/protein kinase B-mammalian target of rapamycin-p70S6K cascade through phosphatidylinositol 3-kinase in human fibroblasts. Mol Endocrinol. 2005;19(1):102–12.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    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.CrossRefGoogle Scholar
  16. 16.
    Flamant F, Cheng SY, Hollenberg AN, Moeller LC, Samarut J, Wondisford FE, et al. Thyroid hormone signaling pathways: time for a more precise nomenclature. Endocrinology. 2017;158(7):2052–7.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Brent GA. Mechanisms of thyroid hormone action. J Clin Invest. 2012;122(9):3035–43.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Mendoza A, Hollenberg AN. New insights into thyroid hormone action. Pharmacol Ther. 2017;173:135–45.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Anyetei-Anum CS, Roggero VR, Allison LA. Thyroid hormone receptor localization in target tissues. J Endocrinol. 2018;237(1):R19–34.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Cheng SY, Leonard JL, Davis PJ. Molecular aspects of thyroid hormone actions. Endocr Rev. 2010;31(2):139–70.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Ito M, Roeder RG. The TRAP/SMCC/mediator complex and thyroid hormone receptor function. Trends Endocrinol Metab. 2001;12(3):127–34.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Hu X, Lazar MA. Transcriptional repression by nuclear hormone receptors. Trends Endocrinol Metab. 2000;11(1):6–10.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Singh BK, Sinha RA, Yen PM. Novel transcriptional mechanisms for regulating metabolism by thyroid hormone. Int J Mol Sci. 2018;19(10):E3284.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Singh BK, Sinha RA, Ohba K, Yen PM. Role of thyroid hormone in hepatic gene regulation, chromatin remodeling, and autophagy. Mol Cell Endocrinol. 2017;458:160–8.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Flamant F, Gauthier K. Thyroid hormone receptors: the challenge of elucidating isotype-specific functions and cell-specific response. Biochim Biophys Acta. 2013;1830(7):3900–7.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Gloss B, Trost S, Bluhm W, Swanson E, Clark R, Winkfein R, et al. Cardiac ion channel expression and contractile function in mice with deletion of thyroid hormone receptor alpha or beta. Endocrinology. 2001;142(2):544–50.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Johansson C, Gothe S, Forrest D, Vennstrom B, Thoren P. Cardiovascular phenotype and temperature control in mice lacking thyroid hormone receptor-beta or both alpha1 and beta. Am J Phys. 1999;276(6 Pt 2):H2006–12.Google Scholar
  28. 28.
    Wikstrom L, Johansson C, Salto C, Barlow C, Campos Barros A, Baas F, et al. Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor alpha 1. EMBO J. 1998;17(2):455–61.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Mansen A, Yu F, Forrest D, Larsson L, Vennstrom B. TRs have common and isoform-specific functions in regulation of the cardiac myosin heavy chain genes. Mol Endocrinol. 2001;15(12):2106–14.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Flamant F, Samarut J. Thyroid hormone receptors: lessons from knockout and knock-in mutant mice. Trends Endocrinol Metab. 2003;14(2):85–90.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Stoykov I, Zandieh-Doulabi B, Moorman AF, Christoffels V, Wiersinga WM, Bakker O. Expression pattern and ontogenesis of thyroid hormone receptor isoforms in the mouse heart. J Endocrinol. 2006;189(2):231–45.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Kalyanaraman H, Schwappacher R, Joshua J, Zhuang S, Scott BT, Klos M, et al. Nongenomic thyroid hormone signaling occurs through a plasma membrane-localized receptor. Sci Signal. 2014;7(326):ra48.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Cioffi F, Senese R, Lanni A, Goglia F. Thyroid hormones and mitochondria: with a brief look at derivatives and analogues. Mol Cell Endocrinol. 2013;379(1–2):51–61.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Wrutniak-Cabello C, Casas F, Cabello G. Thyroid hormone action in mitochondria. J Mol Endocrinol. 2001;26(1):67–77.CrossRefGoogle Scholar
  35. 35.
    Kinugawa K, Yonekura K, Ribeiro RC, Eto Y, Aoyagi T, Baxter JD, et al. Regulation of thyroid hormone receptor isoforms in physiological and pathological cardiac hypertrophy. Circ Res. 2001;89(7):591–8.CrossRefGoogle Scholar
  36. 36.
    Kinugawa K, Minobe WA, Wood WM, Ridgway EC, Baxter JD, Ribeiro RC, et al. Signaling pathways responsible for fetal gene induction in the failing human heart: evidence for altered thyroid hormone receptor gene expression. Circulation. 2001;103(8):1089–94.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    d'Amati G, di Gioia CR, Mentuccia D, Pistilli D, Proietti-Pannunzi L, Miraldi F, et al. Increased expression of thyroid hormone receptor isoforms in end-stage human congestive heart failure. J Clin Endocrinol Metab. 2001;86(5):2080–4.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Modesti PA, Marchetta M, Gamberi T, Lucchese G, Maccherini M, Chiavarelli M, et al. Reduced expression of thyroid hormone receptors and beta-adrenergic receptors in human failing cardiomyocytes. Biochem Pharmacol. 2008;75(4):900–6.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Belke DD, Gloss B, Swanson EA, Dillmann WH. Adeno-associated virus-mediated expression of thyroid hormone receptor isoforms-alpha1 and -beta1 improves contractile function in pressure overload-induced cardiac hypertrophy. Endocrinology. 2007;148(6):2870–7.CrossRefGoogle Scholar
  40. 40.
    Makino A, Suarez J, Wang H, Belke DD, Scott BT, Dillmann WH. Thyroid hormone receptor-beta is associated with coronary angiogenesis during pathological cardiac hypertrophy. Endocrinology. 2009;150(4):2008–15.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Suarez J, Wang H, Scott BT, Ling H, Makino A, Swanson E, et al. In vivo selective expression of thyroid hormone receptor alpha1 in endothelial cells attenuates myocardial injury in experimental myocardial infarction in mice. Am J Physiol Regul Integr Comp Physiol. 2014;307(3):R340–6.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Friberg L, Drvota V, Bjelak AH, Eggertsen G, Ahnve S. Association between increased levels of reverse triiodothyronine and mortality after acute myocardial infarction. Am J Med. 2001;111(9):699–703.CrossRefGoogle Scholar
  43. 43.
    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(12):1388–94.CrossRefGoogle Scholar
  44. 44.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Kalofoutis C, Mourouzis I, Galanopoulos G, Dimopoulos A, Perimenis P, Spanou D, et al. Thyroid hormone can favorably remodel the diabetic myocardium after acute myocardial infarction. Mol Cell Biochem. 2010;345(1–2):161–9.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Lymvaios I, Mourouzis I, Cokkinos DV, Dimopoulos 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(1):107–14.CrossRefGoogle Scholar
  47. 47.
    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(1–2):235–43.CrossRefGoogle Scholar
  48. 48.
    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.CrossRefGoogle Scholar
  49. 49.
    Mourouzis I, Giagourta I, Galanopoulos G, Mantzouratou P, Kostakou E, Kokkinos AD, et al. Thyroid hormone improves the mechanical performance of the post-infarcted diabetic myocardium: a response associated with up-regulation of Akt/mTOR and AMPK activation. Metabolism. 2013;62(10):1387–93.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    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.CrossRefGoogle Scholar
  51. 51.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Nicolini G, Pitto L, Kusmic C, Balzan S, Sabatino L, Iervasi G, et al. New insights into mechanisms of cardioprotection mediated by thyroid hormones. J Thyroid Res. 2013;2013:264387.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Pantos C, Mourouzis I. Translating thyroid hormone effects into clinical practice: the relevance of thyroid hormone receptor alpha1 in cardiac repair. Heart Fail Rev. 2015;20(3):273–82.PubMedCrossRefPubMedCentralGoogle 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(1):39–55.CrossRefGoogle Scholar
  55. 55.
    Gerdes AM, Ojamaa K. Thyroid Hormone and Cardioprotection. Compr Physiol. 2016;6(3):1199–219.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Subramanian KS, Dziedzic RC, Nelson HN, Stern ME, Roggero VR, Bondzi C, et al. Multiple exportins influence thyroid hormone receptor localization. Mol Cell Endocrinol. 2015;411:86–96.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Davis PJ, Davis FB, Lin HY. Promotion by thyroid hormone of cytoplasm-to-nucleus shuttling of thyroid hormone receptors. Steroids. 2008;73(9–10):1013–7.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Baumann CT, Maruvada P, Hager GL, Yen PM. Nuclear cytoplasmic shuttling by thyroid hormone receptors. Multiple protein interactions are required for nuclear retention. J Biol Chem. 2001;276(14):11237–45.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Kinugawa K, Long CS, Bristow MR. Expression of TR isoforms in failing human heart. J Clin Endocrinol Metab. 2001;86(10):5089–90.CrossRefGoogle Scholar
  60. 60.
    Wang X, Li S. Protein mislocalization: mechanisms, functions and clinical applications in cancer. Biochim Biophys Acta. 2014;1846(1):13–25.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Bonamy GM, Allison LA. Oncogenic conversion of the thyroid hormone receptor by altered nuclear transport. Nucl Recept Signal. 2006;4:e008.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Mavinakere MS, Powers JM, Subramanian KS, Roggero VR, Allison LA. Multiple novel signals mediate thyroid hormone receptor nuclear import and export. J Biol Chem. 2012;287(37):31280–97.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Zhang J, Roggero VR, Allison LA. Nuclear import and export of the thyroid hormone receptor. Vitam Horm. 2018;106:45–66.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Kinugawa K, Jeong MY, Bristow MR, Long CS. Thyroid hormone induces cardiac myocyte hypertrophy in a thyroid hormone receptor alpha1-specific manner that requires TAK1 and p38 mitogen-activated protein kinase. Mol Endocrinol. 2005;19(6):1618–28.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Pascual A, Aranda A. Thyroid hormone receptors, cell growth and differentiation. Biochim Biophys Acta. 2013;1830(7):3908–16.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Davis PJ, Lin HY, Tang HY, Davis FB, Mousa SA. Adjunctive input to the nuclear thyroid hormone receptor from the cell surface receptor for the hormone. Thyroid. 2013;23(12):1503–9.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Liu YY, Brent GA. Posttranslational modification of thyroid hormone nuclear receptor by sumoylation. Methods Mol Biol. 2018;1801:47–59.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Liu YY, Brent GA. Posttranslational modification of thyroid hormone nuclear receptor by phosphorylation. Methods Mol Biol. 1801;2018:39–46.Google Scholar
  69. 69.
    Lin HY, Zhang S, West BL, Tang HY, Passaretti T, Davis FB, et al. Identification of the putative MAP kinase docking site in the thyroid hormone receptor-beta1 DNA-binding domain: functional consequences of mutations at the docking site. Biochemistry. 2003;42(24):7571–9.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Sugawara A, Yen PM, Apriletti JW, Ribeiro RC, Sacks DB, Baxter JD, et al. Phosphorylation selectively increases triiodothyronine receptor homodimer binding to DNA. J Biol Chem. 1994;269(1):433–7.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Bhat MK, Ashizawa K, Cheng SY. Phosphorylation enhances the target gene sequence-dependent dimerization of thyroid hormone receptor with retinoid X receptor. Proc Natl Acad Sci U S A. 1994;91(17):7927–31.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Le NT, Martin JF, Fujiwara K, Abe JI. Sub-cellular localization specific SUMOylation in the heart. Biochim Biophys Acta Mol basis Dis. 2017;1863(8):2041–55.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Liu YY, Kogai T, Schultz JJ, Mody K, Brent GA. Thyroid hormone receptor isoform-specific modification by small ubiquitin-like modifier (SUMO) modulates thyroid hormone-dependent gene regulation. J Biol Chem. 2012;287(43):36499–508.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Liu YY, Ayers S, Milanesi A, Teng X, Rabi S, Akiba Y, et al. Thyroid hormone receptor sumoylation is required for preadipocyte differentiation and proliferation. J Biol Chem. 2015;290(12):7402–15.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Weitzel JM. Impaired repressor function in SUMOylation-defective thyroid hormone receptor isoforms. Eur Thyroid J. 2016;5(3):152–63.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Morkin E, Banerjee SK, Stern LZ. Biochemical and histochemical evidence for stimulation of myosin ATPase activity in thyrotoxic rabbit heart. FEBS Lett. 1977;79(2):357–60.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Morkin E, Edwards JG, Tsika RW, Bahl JJ, Flink IL. Regulation of human cardiac myosin heavy chain gene expression by thyroid hormone. Adv Exp Med Biol. 1991;308:143–7.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Balkman C, Ojamaa K, Klein I. Time course of the in vivo effects of thyroid hormone on cardiac gene expression. Endocrinology. 1992;130(4):2001–6.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Everett AW, Clark WA, Chizzonite RA, Zak R. Change in synthesis rates of alpha- and beta-myosin heavy chains in rabbit heart after treatment with thyroid hormone. J Biol Chem. 1983;258(4):2421–5.PubMedPubMedCentralGoogle Scholar
  80. 80.
    Markham BE, Bahl JJ, Gustafson TA, Morkin E. Interaction of a protein factor within a thyroid hormone-sensitive region of rat alpha-myosin heavy chain gene. J Biol Chem. 1987;262(26):12856–62.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Ojamaa K, Klein I. Thyroid hormone regulation of alpha-myosin heavy chain promoter activity assessed by in vivo DNA transfer in rat heart. Biochem Biophys Res Commun. 1991;179(3):1269–75.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Gulick J, Subramaniam A, Neumann J, Robbins J. Isolation and characterization of the mouse cardiac myosin heavy chain genes. J Biol Chem. 1991;266(14):9180–5.PubMedPubMedCentralGoogle Scholar
  83. 83.
    van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell. 2009;17(5):662–73.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007;316(5824):575–9.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Izumo S, Lompre AM, Matsuoka R, Koren G, Schwartz K, Nadal-Ginard B, et al. Myosin heavy chain messenger RNA and protein isoform transitions during cardiac hypertrophy. Interaction between hemodynamic and thyroid hormone-induced signals. J Clin Invest. 1987;79(3):970–7.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Lowes BD, Minobe W, Abraham WT, Rizeq MN, Bohlmeyer TJ, Quaife RA, et al. Changes in gene expression in the intact human heart. Downregulation of alpha-myosin heavy chain in hypertrophied, failing ventricular myocardium. J Clin Invest. 1997;100(9):2315–24.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Ojamaa K, Klemperer JD, MacGilvray SS, Klein I, Samarel A. Thyroid hormone and hemodynamic regulation of beta-myosin heavy chain promoter in the heart. Endocrinology. 1996;137(3):802–8.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Miyata S, Minobe W, Bristow MR, Leinwand LA. Myosin heavy chain isoform expression in the failing and nonfailing human heart. Circ Res. 2000;86(4):386–90.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Klein I, Ojamaa K. Thyroid hormone and the cardiovascular system. N Engl J Med. 2001;344(7):501–9.CrossRefGoogle Scholar
  90. 90.
    Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415(6868):198–205.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Bluhm WF, Kranias EG, Dillmann WH, Meyer M. Phospholamban: a major determinant of the cardiac force-frequency relationship. Am J Physiol Heart Circ Physiol. 2000;278(1):H249–55.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Kranias EG, Hajjar RJ. Modulation of cardiac contractility by the phospholamban/SERCA2a regulatome. Circ Res. 2012;110(12):1646–60.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Kiss E, Jakab G, Kranias EG, Edes I. Thyroid hormone-induced alterations in phospholamban protein expression. Regulatory effects on sarcoplasmic reticulum Ca2+ transport and myocardial relaxation. Circ Res. 1994;75(2):245–51.CrossRefGoogle Scholar
  94. 94.
    Moriscot AS, Sayen MR, Hartong R, Wu P, Dillmann WH. Transcription of the rat sarcoplasmic reticulum Ca2+ adenosine triphosphatase gene is increased by 3,5,3′-triiodothyronine receptor isoform-specific interactions with the myocyte-specific enhancer factor-2a. Endocrinology. 1997;138(1):26–32.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Reed TD, Babu GJ, Ji Y, Zilberman A, Ver Heyen M, Wuytack F, et al. The expression of SR calcium transport ATPase and the Na(+)/Ca(2+)Exchanger are antithetically regulated during mouse cardiac development and in hypo/hyperthyroidism. J Mol Cell Cardiol. 2000;32(3):453–64.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Shenoy R, Klein I, Ojamaa K. Differential regulation of SR calcium transporters by thyroid hormone in rat atria and ventricles. Am J Physiol Heart Circ Physiol. 2001;281(4):H1690–6.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Studer R, Reinecke H, Bilger J, Eschenhagen T, Bohm M, Hasenfuss G, et al. Gene expression of the cardiac Na(+)-Ca2+ exchanger in end-stage human heart failure. Circ Res. 1994;75(3):443–53.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Weisser-Thomas J, Kubo H, Hefner CA, Gaughan JP, BS MG, Ross R, et al. The Na+/Ca2+ exchanger/SR Ca2+ ATPase transport capacity regulates the contractility of normal and hypertrophied feline ventricular myocytes. J Card Fail. 2005;11(5):380–7.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Wassen FW, Schiel AE, Kuiper GG, Kaptein E, Bakker O, Visser TJ, et al. Induction of thyroid hormone-degrading deiodinase in cardiac hypertrophy and failure. Endocrinology. 2002;143(7):2812–5.CrossRefGoogle Scholar
  100. 100.
    Wassen FW, Klootwijk W, Kaptein E, Duncker DJ, Visser TJ, Kuiper GG. Characteristics and thyroid state-dependent regulation of iodothyronine deiodinases in pigs. Endocrinology. 2004;145(9):4251–63.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    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.CrossRefGoogle Scholar
  102. 102.
    Simonides WS, Mulcahey MA, Redout EM, Muller A, Zuidwijk MJ, Visser TJ, et al. Hypoxia-inducible factor induces local thyroid hormone inactivation during hypoxic-ischemic disease in rats. J Clin Invest. 2008;118(3):975–83.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Visser WE, Friesema EC, Visser TJ. Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol Endocrinol. 2011;25(1):1–14.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Haghighi K, Bidwell P, Kranias EG. Phospholamban interactome in cardiac contractility and survival: a new vision of an old friend. J Mol Cell Cardiol. 2014;77:160–7.PubMedCrossRefGoogle Scholar
  105. 105.
    Bahouth SW, Cui X, Beauchamp MJ, Park EA. Thyroid hormone induces beta1-adrenergic receptor gene transcription through a direct repeat separated by five nucleotides. J Mol Cell Cardiol. 1997;29(12):3223–37.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Bristow MR, Minobe WA, Raynolds MV, Port JD, Rasmussen R, Ray PE, et al. Reduced beta 1 receptor messenger RNA abundance in the failing human heart. J Clin Invest. 1993;92(6):2737–45.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Engelhardt S, Bohm M, Erdmann E, Lohse MJ. Analysis of beta-adrenergic receptor mRNA levels in human ventricular biopsy specimens by quantitative polymerase chain reactions: progressive reduction of beta 1-adrenergic receptor mRNA in heart failure. J Am Coll Cardiol. 1996;27(1):146–54.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Hong T, Shaw RM. Cardiac T-tubule microanatomy and function. Physiol Rev. 2017;97(1):227–52.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Hong T, Yang H, Zhang SS, Cho HC, Kalashnikova M, Sun B, et al. Cardiac BIN1 folds T-tubule membrane, controlling ion flux and limiting arrhythmia. Nat Med. 2014;20(6):624–32.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Hong TT, Smyth JW, Gao D, Chu KY, Vogan JM, Fong TS, et al. BIN1 localizes the L-type calcium channel to cardiac T-tubules. PLoS Biol. 2010;8(2):e1000312.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Hong TT, Smyth JW, Chu KY, Vogan JM, Fong TS, Jensen BC, et al. BIN1 is reduced and Cav1.2 trafficking is impaired in human failing cardiomyocytes. Heart Rhythm. 2012;9(5):812–20.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Hong TT, Cogswell R, James CA, Kang G, Pullinger CR, Malloy MJ, et al. Plasma BIN1 correlates with heart failure and predicts arrhythmia in patients with arrhythmogenic right ventricular cardiomyopathy. Heart Rhythm. 2012;9(6):961–7.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Caldwell JL, Smith CE, Taylor RF, Kitmitto A, Eisner DA, Dibb KM, et al. Dependence of cardiac transverse tubules on the BAR domain protein amphiphysin II (BIN-1). Circ Res. 2014;115(12):986–96.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Lyon AR, MacLeod KT, Zhang Y, Garcia E, Kanda GK, Lab MJ, et al. Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart. Proc Natl Acad Sci U S A. 2009;106(16):6854–9.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Seidel T, Navankasattusas S, Ahmad A, Diakos NA, Xu WD, Tristani-Firouzi M, et al. Sheet-like remodeling of the transverse tubular system in human heart failure impairs excitation-contraction coupling and functional recovery by mechanical unloading. Circulation. 2017;135(17):1632–45.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Zhou K, Hong T. Cardiac BIN1 (cBIN1) is a regulator of cardiac contractile function and an emerging biomarker of heart muscle health. Sci China Life Sci. 2017;60(3):257–63.PubMedCrossRefPubMedCentralGoogle Scholar
  117. 117.
    An S, Gilani N, Huang Y, Muncan A, Zhang Y, Tang YD, Gerdes AM, Ojamaa K. Adverse transverse-tubule remodeling in a rat model of heart failure is attenuated with low-dose triiodothyronine treatment. Mol Med. 2019;25(1):53–66.Google Scholar
  118. 118.
    Wechsler-Reya R, Sakamuro D, Zhang J, Duhadaway J, Prendergast GC. Structural analysis of the human BIN1 gene. Evidence for tissue-specific transcriptional regulation and alternate RNA splicing. J Biol Chem. 1997;272(50):31453–8.PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Knudsen N, Laurberg P, Rasmussen LB, Bulow I, Perrild H, Ovesen L, et al. Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population. J Clin Endocrinol Metab. 2005;90(7):4019–24.PubMedCrossRefPubMedCentralGoogle Scholar
  120. 120.
    Iwen KA, Schroder E, Brabant G. Thyroid hormones and the metabolic syndrome. Eur Thyroid J. 2013;2(2):83–92.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Mullur R, Liu YY, Brent GA. Thyroid hormone regulation of metabolism. Physiol Rev. 2014;94(2):​355–82.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Portman MA. Thyroid hormone regulation of heart metabolism. Thyroid. 2008;18(2):217–25.PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Sack MN, Rader TA, Park S, Bastin J, McCune SA, Kelly DP. Fatty acid oxidation enzyme gene expression is downregulated in the failing heart. Circulation. 1996;94(11):2837–42.PubMedCrossRefPubMedCentralGoogle Scholar
  124. 124.
    Osorio JC, Stanley WC, Linke A, Castellari M, Diep QN, Panchal AR, et al. Impaired myocardial fatty acid oxidation and reduced protein expression of retinoid X receptor-alpha in pacing-induced heart failure. Circulation. 2002;106(5):606–12.PubMedCrossRefPubMedCentralGoogle Scholar
  125. 125.
    Lei B, Lionetti V, Young ME, Chandler MP, d'Agostino C, Kang E, et al. Paradoxical downregulation of the glucose oxidation pathway despite enhanced flux in severe heart failure. J Mol Cell Cardiol. 2004;36(4):567–76.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Liu Q, Clanachan AS, Lopaschuk GD. Acute effects of triiodothyronine on glucose and fatty acid metabolism during reperfusion of ischemic rat hearts. Am J Phys. 1998;275(3 Pt 1):E392–9.Google Scholar
  127. 127.
    Hyyti OM, Ning XH, Buroker NE, Ge M, Portman MA. Thyroid hormone controls myocardial substrate metabolism through nuclear receptor-mediated and rapid posttranscriptional mechanisms. Am J Physiol Endocrinol Metab. 2006;290(2):E372–9.CrossRefGoogle Scholar
  128. 128.
    Hyyti OM, Portman MA. Molecular mechanisms of cross-talk between thyroid hormone and peroxisome proliferator activated receptors: focus on the heart. Cardiovasc Drugs Ther. 2006;20(6):463–9.CrossRefGoogle Scholar
  129. 129.
    Krueger JJ, Ning XH, Argo BM, Hyyti O, Portman MA. Triidothyronine and epinephrine rapidly modify myocardial substrate selection: a (13)C isotopomer analysis. Am J Physiol Endocrinol Metab. 2001;281(5):E983–90.CrossRefGoogle Scholar
  130. 130.
    Sugden MC, Langdown ML, Harris RA, Holness MJ. Expression and regulation of pyruvate dehydrogenase kinase isoforms in the developing rat heart and in adulthood: role of thyroid hormone status and lipid supply. Biochem J. 2000;352(Pt 3):731–8.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Jansen MS, Cook GA, Song S, Park EA. Thyroid hormone regulates carnitine palmitoyltransferase Ialpha gene expression through elements in the promoter and first intron. J Biol Chem. 2000;275(45):34989–97.CrossRefGoogle Scholar
  132. 132.
    Park EA, Song S, Olive M, Roesler WJ. CCAAT-enhancer-binding protein alpha (C/EBP alpha) is required for the thyroid hormone but not the retinoic acid induction of phosphoenolpyruvate carboxykinase (PEPCK) gene transcription. Biochem J. 1997;322(Pt 1):343–9.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Attia RR, Connnaughton S, Boone LR, Wang F, Elam MB, Ness GC, et al. Regulation of pyruvate dehydrogenase kinase 4 (PDK4) by thyroid hormone: role of the peroxisome proliferator-activated receptor gamma coactivator (PGC-1 alpha). J Biol Chem. 2010;285(4):2375–85.PubMedCrossRefPubMedCentralGoogle Scholar
  134. 134.
    Sadana P, Park EA. Characterization of the transactivation domain in the peroxisome-proliferator-activated receptor gamma co-activator (PGC-1). Biochem J. 2007;403(3):511–8.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Sadana P, Zhang Y, Song S, Cook GA, Elam MB, Park EA. Regulation of carnitine palmitoyltransferase I (CPT-Ialpha) gene expression by the peroxisome proliferator activated receptor gamma coactivator (PGC-1) isoforms. Mol Cell Endocrinol. 2007;267(1–2):6–16.PubMedCrossRefPubMedCentralGoogle Scholar
  136. 136.
    Portman MA, Qian K, Krueger J, Ning XH. Direct action of T3 on phosphorylation potential in the sheep heart in vivo. Am J Physiol Heart Circ Physiol. 2005;288(5):H2484–90.PubMedCrossRefPubMedCentralGoogle Scholar
  137. 137.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Kajimoto M, Priddy CM, Ledee DR, Xu C, Isern N, Olson AK, et al. Effects of continuous triiodothyronine infusion on the tricarboxylic acid cycle in the normal immature swine heart under extracorporeal membrane oxygenation in vivo. Am J Physiol Heart Circ Physiol. 2014;306(8):H1164–70.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Kates AM, Herrero P, Dence C, Soto P, Srinivasan M, Delano DG, et al. Impact of aging on substrate metabolism by the human heart. J Am Coll Cardiol. 2003;41(2):293–9.PubMedCrossRefGoogle Scholar
  141. 141.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Kolwicz SC Jr, Purohit S, Tian R. Cardiac metabolism and its interactions with contraction, growth, and survival of cardiomyocytes. Circ Res. 2013;113(5):603–16.CrossRefGoogle Scholar
  143. 143.
    Marin-Garcia J. Thyroid hormone and myocardial mitochondrial biogenesis. Vasc Pharmacol. 2010;52(3–4):120–30.CrossRefGoogle Scholar
  144. 144.
    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(3):6312–36.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Harper ME, Seifert EL. Thyroid hormone effects on mitochondrial energetics. Thyroid. 2008;18(2):145–56.PubMedCrossRefPubMedCentralGoogle Scholar
  146. 146.
    Dorn GW 2nd. Apoptotic and non-apoptotic programmed cardiomyocyte death in ventricular remodelling. Cardiovasc Res. 2009;81(3):465–73.PubMedCrossRefPubMedCentralGoogle Scholar
  147. 147.
    Marin-Garcia J, Goldenthal MJ. Mitochondrial centrality in heart failure. Heart Fail Rev. 2008;13(2):137–50.PubMedCrossRefPubMedCentralGoogle Scholar
  148. 148.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Morrish F, Buroker NE, Ge M, Ning XH, Lopez-Guisa J, Hockenbery D, et al. Thyroid hormone receptor isoforms localize to cardiac mitochondrial matrix with potential for binding to receptor elements on mtDNA. Mitochondrion. 2006;6(3):143–8.CrossRefGoogle Scholar
  150. 150.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Janssen R, Zuidwijk MJ, Kuster DW, Muller A, Simonides WS. Thyroid hormone-regulated cardiac microRNAs are predicted to suppress pathological hypertrophic signaling. Front Endocrinol (Lausanne). 2014;5:171.Google Scholar
  152. 152.
    Psarra AM, Sekeris CE. Steroid and thyroid hormone receptors in mitochondria. IUBMB Life. 2008;60(4):210–23.PubMedCrossRefPubMedCentralGoogle Scholar
  153. 153.
    Saelim N, Holstein D, Chocron ES, Camacho P, Lechleiter JD. Inhibition of apoptotic potency by ligand stimulated thyroid hormone receptors located in mitochondria. Apoptosis. 2007;12(10):1781–94.PubMedCrossRefGoogle Scholar
  154. 154.
    Storey NM, Gentile S, Ullah H, Russo A, Muessel M, Erxleben C, et al. Rapid signaling at the plasma membrane by a nuclear receptor for thyroid hormone. Proc Natl Acad Sci U S A. 2006;103(13):5197–201.PubMedPubMedCentralCrossRefGoogle Scholar
  155. 155.
    Moeller LC, Cao X, Dumitrescu AM, Seo H, Refetoff S. Thyroid hormone mediated changes in gene expression can be initiated by cytosolic action of the thyroid hormone receptor beta through the phosphatidylinositol 3-kinase pathway. Nucl Recept Signal. 2006;4:e020.PubMedPubMedCentralCrossRefGoogle Scholar
  156. 156.
    Moeller LC, Dumitrescu AM, Refetoff S. Cytosolic action of thyroid hormone leads to induction of hypoxia-inducible factor-1alpha and glycolytic genes. Mol Endocrinol. 2005;19(12):2955–63.PubMedCrossRefGoogle Scholar
  157. 157.
    Martin NP, Marron Fernandez de Velasco E, Mizuno F, Scappini EL, Gloss B, Erxleben C, et al. A rapid cytoplasmic mechanism for PI3 kinase regulation by the nuclear thyroid hormone receptor, TRbeta, and genetic evidence for its role in the maturation of mouse hippocampal synapses in vivo. Endocrinology. 2014;155(9):3713–24.PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Ojamaa K. Signaling mechanisms in thyroid hormone-induced cardiac hypertrophy. Vasc Pharmacol. 2010;52(3–4):113–9.CrossRefGoogle Scholar
  159. 159.
    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.PubMedCrossRefGoogle Scholar
  160. 160.
    Levin ER. Plasma membrane estrogen receptors. Trends Endocrinol Metab. 2009;20(10):477–82.PubMedPubMedCentralCrossRefGoogle Scholar
  161. 161.
    Kapitola J, Vilimovska D. Inhibition of the early circulatory effects of triiodothyronine in rats by propranolol. Physiol Bohemoslov. 1981;30(4):347–51.PubMedGoogle Scholar
  162. 162.
    Vargas F, Moreno JM, Rodriguez-Gomez I, Wangensteen R, Osuna A, Alvarez-Guerra M, et al. Vascular and renal function in experimental thyroid disorders. Eur J Endocrinol. 2006;154(2):197–212.CrossRefGoogle Scholar
  163. 163.
    Napoli R, Biondi B, Guardasole V, Matarazzo M, Pardo F, Angelini V, et al. Impact of hyperthyroidism and its correction on vascular reactivity in humans. Circulation. 2001;104(25):3076–80.PubMedCrossRefGoogle Scholar
  164. 164.
    Klemperer JD, Zelano J, Helm RE, Berman K, Ojamaa K, Klein I, et al. Triiodothyronine improves left ventricular function without oxygen wasting effects after global hypothermic ischemia. J Thorac Cardiovasc Surg. 1995;109(3):457–65.PubMedCrossRefGoogle Scholar
  165. 165.
    Colantuoni A, Marchiafava PL, Lapi D, Forini FS, Iervasi G. Effects of tetraiodothyronine and triiodothyronine on hamster cheek pouch microcirculation. Am J Physiol Heart Circ Physiol. 2005;288(4):H1931–6.PubMedCrossRefGoogle Scholar
  166. 166.
    Park KW, Dai HB, Ojamaa K, Lowenstein E, Klein I, Sellke FW. The direct vasomotor effect of thyroid hormones on rat skeletal muscle resistance arteries. Anesth Analg. 1997;85(4):734–8.PubMedCrossRefGoogle Scholar
  167. 167.
    Ojamaa K, Balkman C, Klein IL. Acute effects of triiodothyronine on arterial smooth muscle cells. Ann Thorac Surg. 1993;56(1 Suppl):S61–6. discussion S6–7.PubMedCrossRefGoogle Scholar
  168. 168.
    Ojamaa K, Klemperer JD, Klein I. Acute effects of thyroid hormone on vascular smooth muscle. Thyroid. 1996;6(5):505–12.CrossRefGoogle Scholar
  169. 169.
    Carrillo-Sepulveda MA, Ceravolo GS, Fortes ZB, Carvalho MH, Tostes RC, Laurindo FR, et al. Thyroid hormone stimulates NO production via activation of the PI3K/Akt pathway in vascular myocytes. Cardiovasc Res. 2010;85(3):560–70.PubMedCrossRefGoogle Scholar
  170. 170.
    Samuel S, Zhang K, Tang YD, Gerdes AM, Carrillo-Sepulveda MA. Triiodothyronine potentiates vasorelaxation via PKG/VASP signaling in vascular smooth muscle cells. Cell Physiol Biochem. 2017;41(5):1894–904.PubMedCrossRefGoogle Scholar
  171. 171.
    Makino A, Wang H, Scott BT, Yuan JX, Dillmann WH. Thyroid hormone receptor-alpha and vascular function. Am J Physiol Cell Physiol. 2012;302(9):C1346–52.PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Karch R, Neumann F, Ullrich R, Neumuller J, Podesser BK, Neumann M, et al. The spatial pattern of coronary capillaries in patients with dilated, ischemic, or inflammatory cardiomyopathy. Cardiovasc Pathol. 2005;14(3):135–44.PubMedCrossRefGoogle Scholar
  173. 173.
    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.CrossRefGoogle Scholar
  174. 174.
    Weltman NY, Ojamaa K, Schlenker EH, Chen YF, Zucchi R, Saba A, et al. Low-dose T3 replacement restores depressed cardiac T3 levels, preserves coronary microvasculature, and attenuates cardiac dysfunction in experimental diabetes mellitus. Mol Med. 2014;20:302–12.PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Savinova OV, Liu Y, Aasen GA, Mao K, Weltman NY, Nedich BL, et al. Thyroid hormone promotes remodeling of coronary resistance vessels. PLoS One. 2011;6(9):e25054.PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    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(11):2726–35.PubMedPubMedCentralCrossRefGoogle Scholar
  177. 177.
    Davis FB, Mousa SA, O'Connor L, Mohamed S, Lin HY, Cao HJ, et al. Proangiogenic action of thyroid hormone is fibroblast growth factor-dependent and is initiated at the cell surface. Circ Res. 2004;94(11):1500–6.PubMedCrossRefPubMedCentralGoogle Scholar
  178. 178.
    Davis PJ, Davis FB, Mousa SA. Thyroid hormone-induced angiogenesis. Curr Cardiol Rev. 2009;5(1):12–6.PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    Bergh JJ, Lin HY, Lansing L, Mohamed SN, Davis FB, Mousa S, et al. Integrin alphaVbeta3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology. 2005;146(7):2864–71.PubMedCrossRefPubMedCentralGoogle Scholar
  180. 180.
    Mousa SA, Davis FB, Mohamed S, Davis PJ, Feng X. Pro-angiogenesis action of thyroid hormone and analogs in a three-dimensional in vitro microvascular endothelial sprouting model. Int Angiol. 2006;25(4):407–13.PubMedPubMedCentralGoogle Scholar
  181. 181.
    Liu X, Zheng N, Shi YN, Yuan J, Li L. Thyroid hormone induced angiogenesis through the integrin alphavbeta3/protein kinase D/histone deacetylase 5 signaling pathway. J Mol Endocrinol. 2014;52(3):245–54.PubMedCrossRefPubMedCentralGoogle Scholar
  182. 182.
    Light P, Shimoni Y, Harbison S, Giles W, French RJ. Hypothyroidism decreases the ATP sensitivity of KATP channels from rat heart. J Membr Biol. 1998;162(3):217–23.PubMedCrossRefPubMedCentralGoogle Scholar
  183. 183.
    Shimoni Y, Severson DL. Thyroid status and potassium currents in rat ventricular myocytes. Am J Phys. 1995;268(2 Pt 2):H576–83.Google Scholar
  184. 184.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    Yalcin Y, Carman D, Shao Y, Ismail-Beigi F, Klein I, Ojamaa K. Regulation of Na/K-ATPase gene expression by thyroid hormone and hyperkalemia in the heart. Thyroid. 1999;9(1):53–9.PubMedCrossRefPubMedCentralGoogle Scholar
  186. 186.
    Liu B, Huang F, Gick G. Regulation of Na,K-ATPase beta 1 mRNA content by thyroid hormone in neonatal rat cardiac myocytes. Cell Mol Biol Res. 1993;39(3):221–9.PubMedPubMedCentralGoogle Scholar
  187. 187.
    Shimoni Y, Fiset C, Clark RB, Dixon JE, McKinnon D, Giles WR. Thyroid hormone regulates postnatal expression of transient K+ channel isoforms in rat ventricle. J Physiol. 1997;500(Pt 1):65–73.PubMedPubMedCentralCrossRefGoogle Scholar
  188. 188.
    Wickenden AD, Kaprielian R, Parker TG, Jones OT, Backx PH. Effects of development and thyroid hormone on K+ currents and K+ channel gene expression in rat ventricle. J Physiol. 1997;504(Pt 2):271–86.PubMedPubMedCentralCrossRefGoogle Scholar
  189. 189.
    Ojamaa K, Sabet A, Kenessey A, Shenoy R, Klein I. Regulation of rat cardiac Kv1.5 gene expression by thyroid hormone is rapid and chamber specific. Endocrinology. 1999;140(7):3170–6.PubMedCrossRefPubMedCentralGoogle Scholar
  190. 190.
    Craelius W, Green WL, Harris DR. Acute effects of thyroid hormone on sodium currents in neonatal myocytes. Biosci Rep. 1990;10(3):309–15.PubMedCrossRefPubMedCentralGoogle Scholar
  191. 191.
    Dudley SC Jr, Baumgarten CM. Bursting of cardiac sodium channels after acute exposure to 3,5,3′-triiodo-L-thyronine. Circ Res. 1993;73(2):301–13.PubMedCrossRefPubMedCentralGoogle Scholar
  192. 192.
    Harris DR, Green WL, Craelius W. Acute thyroid hormone promotes slow inactivation of sodium current in neonatal cardiac myocytes. Biochim Biophys Acta. 1991;1095(2):175–81.PubMedCrossRefPubMedCentralGoogle Scholar
  193. 193.
    Sakaguchi Y, Cui G, Sen L. Acute effects of thyroid hormone on inward rectifier potassium channel currents in Guinea pig ventricular myocytes. Endocrinology. 1996;137(11):4744–51.PubMedCrossRefPubMedCentralGoogle Scholar
  194. 194.
    Sen L, Sakaguchi Y. Cui G. G protein modulates thyroid hormone-induced Na(+) channel activation in ventricular myocytes. Am J Physiol Heart Circ Physiol. 2002;283(5):H2119–29.PubMedCrossRefPubMedCentralGoogle Scholar
  195. 195.
    Sun ZQ, Ojamaa K, Coetzee WA, Artman M, Klein I. Effects of thyroid hormone on action potential and repolarizing currents in rat ventricular myocytes. Am J Physiol Endocrinol Metab. 2000;278(2):E302–7.PubMedCrossRefPubMedCentralGoogle Scholar
  196. 196.
    Sun ZQ, Ojamaa K, Nakamura TY, Artman M, Klein I, Coetzee WA. Thyroid hormone increases pacemaker activity in rat neonatal atrial myocytes. J Mol Cell Cardiol. 2001;33(4):811–24.PubMedCrossRefPubMedCentralGoogle Scholar
  197. 197.
    Wang YG, Dedkova EN, Fiening JP, Ojamaa K, Blatter LA, Lipsius SL. Acute exposure to thyroid hormone increases Na+ current and intracellular Ca2+ in cat atrial myocytes. J Physiol. 2003;546(Pt 2):491–9.CrossRefGoogle Scholar
  198. 198.
    Watanabe H, Washizuka T, Komura S, Yoshida T, Hosaka Y, Hatada K, et al. Genomic and non-genomic regulation of L-type calcium channels in rat ventricle by thyroid hormone. Endocr Res. 2005;31(1):59–70.PubMedCrossRefPubMedCentralGoogle Scholar
  199. 199.
    Lopez-Crisosto C, Pennanen C, Vasquez-Trincado C, Morales PE, Bravo-Sagua R, Quest AFG, et al. Sarcoplasmic reticulum–mitochondria communication in cardiovascular pathophysiology. Nat Rev Cardiol. 2017;14:342.PubMedCrossRefPubMedCentralGoogle Scholar
  200. 200.
    Luongo TS, Lambert JP, Gross P, Nwokedi M, Lombardi AA, Shanmughapriya S, et al. The mitochondrial Na(+)/Ca(2+) exchanger is essential for Ca(2+) homeostasis and viability. Nature. 2017;545(7652):93–7.PubMedPubMedCentralCrossRefGoogle Scholar
  201. 201.
    Morales PE, Torres G, Sotomayor-Flores C, Pena-Oyarzun D, Rivera-Mejias P, Paredes F, et al. GLP-1 promotes mitochondrial metabolism in vascular smooth muscle cells by enhancing endoplasmic reticulum-mitochondria coupling. Biochem Biophys Res Commun. 2014;446(1):410–6.PubMedCrossRefPubMedCentralGoogle Scholar
  202. 202.
    Drago I, De Stefani D, Rizzuto R, Pozzan T. Mitochondrial Ca2+ uptake contributes to buffering cytoplasmic Ca2+ peaks in cardiomyocytes. Proc Natl Acad Sci U S A. 2012;109(32):12986–91.PubMedPubMedCentralCrossRefGoogle Scholar
  203. 203.
    Saelim N, John LM, Wu J, Park JS, Bai Y, Camacho P, et al. Nontranscriptional modulation of intracellular Ca2+ signaling by ligand stimulated thyroid hormone receptor. J Cell Biol. 2004;167(5):915–24.PubMedPubMedCentralCrossRefGoogle Scholar
  204. 204.
    Mansen A, Tiselius C, Sand P, Fauconnier J, Westerblad H, Rydqvist B, et al. Thyroid hormone receptor alpha can control action potential duration in mouse ventricular myocytes through the KCNE1 ion channel subunit. Acta Physiol (Oxf). 2010;198(2):133–42.CrossRefGoogle Scholar
  205. 205.
    Johansson C, Koopmann R, Vennstrom B, Benndorf K. Accelerated inactivation of voltage-dependent K+ outward current in cardiomyocytes from thyroid hormone receptor alpha1-deficient mice. J Cardiovasc Electrophysiol. 2002;13(1):44–50.PubMedCrossRefPubMedCentralGoogle Scholar
  206. 206.
    Hones GS, Rakov H, Logan J, Liao XH, Werbenko E, Pollard AS, et al. Noncanonical thyroid hormone signaling mediates cardiometabolic effects in vivo. Proc Natl Acad Sci U S A. 2017;114(52):E11323–E32.PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    Macchia PE, Takeuchi Y, Kawai T, Cua K, Gauthier K, Chassande O, et al. Increased sensitivity to thyroid hormone in mice with complete deficiency of thyroid hormone receptor alpha. Proc Natl Acad Sci U S A. 2001;98(1):349–54.PubMedPubMedCentralGoogle Scholar
  208. 208.
    Gassanov N, Er F, Endres-Becker J, Wolny M, Schramm C, Hoppe UC. Distinct regulation of cardiac I(f) current via thyroid receptors alpha1 and beta1. Pflugers Arch. 2009;458(6):1061–8.PubMedCrossRefPubMedCentralGoogle Scholar
  209. 209.
    Gassanov N, Er F, Michels G, Zagidullin N, Brandt MC, Hoppe UC. Divergent regulation of cardiac KCND3 potassium channel expression by the thyroid hormone receptors alpha1 and beta1. J Physiol. 2009;587(Pt 6):1319–29.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biomedical SciencesNew York Institute of Technology College of Osteopathic MedicineOld WestburyUSA

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