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Thyroid Hormone and Myocardial Mitochondria

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Mitochondria and Their Role in Cardiovascular Disease

Abstract

The ability of thyroid hormone to regulate energy utilization was first recognized more than 100 years ago and is still a contemporary topic in thyroid research. To date, we still do not understand the molecular events by which thyroid hormone controls this essential function. Energy, in the form of ATP, is the currency required for life, and the mitochondrion is its principal source. This fact has made this organelle an obvious target for thyroid hormone action. In addition to providing about 90 % of the energy currency of the cell, these acquired organelles also play essential roles in cell signaling and cell survival, two other cell regulatory cascades that are possible targets for thyroid hormone action.

In addition to the action of the nuclear-localized thyroid hormone receptors on nuclear oxidative phosphorylation (OXPHOS) gene transcription, a parallel direct action of the mitochondrially localized receptors on mitochondrial transcription has been demonstrated. The coordination of transcription activation in nuclei and mitochondria by the thyroid hormone receptors is in part realized by their binding to common trans-acting elements in the two genomes.

In this chapter we will focus on the effects of thyroid hormone on mitochondrial energetics and mitochondriogenesis.

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References

  1. Horlein AJ, Naar AM, Heinzel T, et al. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature. 1995;377(6548):397–404.

    PubMed  CAS  Google Scholar 

  2. Chen JD, Evans RM. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature. 1995;377(6548):454–7.

    PubMed  CAS  Google Scholar 

  3. Potter GB, Beaudoin 3rd GM, DeRenzo CL, Zarach JM, Chen SH, Thompson CC. The hairless gene mutated in congenital hair loss disorders encodes a novel nuclear receptor corepressor. Genes Dev. 2001;15(20):2687–701.

    PubMed  CAS  Google Scholar 

  4. Dressel U, Thormeyer D, Altincicek B, et al. Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol Cell Biol. 1999;19(5):3383–94.

    PubMed  CAS  Google Scholar 

  5. Wei LN, Hu X. Receptor interacting protein 140 as a thyroid hormone-dependent, negative co-regulator for the induction of cellular retinoic acid binding protein I gene. Mol Cell Endocrinol. 2004;218(1–2):39–48.

    PubMed  CAS  Google Scholar 

  6. Zamir I, Dawson J, Lavinsky RM, Glass CK, Rosenfeld MG, Lazar MA. Cloning and characterization of a corepressor and potential component of the nuclear hormone receptor repression complex. Proc Natl Acad Sci USA. 1997;94(26):14400–5.

    PubMed  CAS  Google Scholar 

  7. Yoon HG, Chan DW, Huang ZQ, et al. Purification and functional characterization of the human N-CoR complex: the roles of HDAC3, TBL1 and TBLR1. EMBO J. 2003;22(6):1336–46.

    PubMed  CAS  Google Scholar 

  8. Reilly SM, Bhargava P, Liu S, et al. Nuclear receptor corepressor SMRT regulates mitochondrial oxidative metabolism and mediates aging-related metabolic deterioration. Cell Metab. 2010;12(6): 643–53.

    PubMed  CAS  Google Scholar 

  9. Lee JW, Ryan F, Swaffield JC, Johnston SA, Moore DD. Interaction of thyroid-hormone receptor with a conserved transcriptional mediator. Nature. 1995;374(6517):91–4.

    PubMed  CAS  Google Scholar 

  10. McKenna NJ, Lanz RB, O’Malley BW. Nuclear receptor coregulators: cellular and molecular biology. Endocr Rev. 1999;20(3): 321–44.

    PubMed  CAS  Google Scholar 

  11. McKenna NJ, O’Malley BW. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell. 2002;108(4):465–74.

    PubMed  CAS  Google Scholar 

  12. Fondell JD, Ge H, Roeder RG. Ligand induction of a transcriptionally active thyroid hormone receptor coactivator complex. Proc Natl Acad Sci USA. 1996;93(16):8329–33.

    PubMed  CAS  Google Scholar 

  13. Yuan CX, Ito M, Fondell JD, Fu ZY, Roeder RG. The TRAP220 component of a thyroid hormone receptor-associated protein (TRAP) coactivator complex interacts directly with nuclear receptors in a ligand-dependent fashion. Proc Natl Acad Sci USA. 1998;95(14):7939–44.

    PubMed  CAS  Google Scholar 

  14. Wikstrom L, Johansson C, Salto C, et al. Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor alpha 1. EMBO J. 1998;17(2):455–61.

    PubMed  CAS  Google Scholar 

  15. 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.

    PubMed  CAS  Google Scholar 

  16. Mynatt RL, Park EA, Thorngate FE, Das HK, Cook GA. Changes in carnitine palmitoyltransferase-I mRNA abundance produced by hyperthyroidism and hypothyroidism parallel changes in activity. Biochem Biophys Res Commun. 1994;201(2):932–7.

    PubMed  CAS  Google Scholar 

  17. Cook GA, Edwards TL, Jansen MS, Bahouth SW, Wilcox HG, Park EA. Differential regulation of carnitine palmitoyltransferase-I gene isoforms (CPT-I alpha and CPT-I beta) in the rat heart. J Mol Cell Cardiol. 2001;33(2):317–29.

    PubMed  CAS  Google Scholar 

  18. Petty KJ, Desvergne B, Mitsuhashi T, Nikodem VM. Identification of a thyroid hormone response element in the malic enzyme gene. J Biol Chem. 1990;265(13):7395–400.

    PubMed  CAS  Google Scholar 

  19. Dummler K, Muller S, Seitz HJ. Regulation of adenine nucleotide translocase and glycerol 3-phosphate dehydrogenase expression by thyroid hormones in different rat tissues. Biochem J. 1996;317(Pt 3):913–8.

    PubMed  Google Scholar 

  20. 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.

    PubMed  CAS  Google Scholar 

  21. Priestman DA, Donald E, Holness MJ, Sugden MC. Different mechanisms underlie the long-term regulation of pyruvate dehydrogenase kinase (PDHK) by tri-iodothyronine in heart and liver. FEBS Lett. 1997;419(1):55–7.

    PubMed  CAS  Google Scholar 

  22. Schonfeld P, Wieckowski MR, Wojtczak L. Thyroid hormone-induced expression of the ADP/ATP carrier and its effect on fatty acid-induced uncoupling of oxidative phosphorylation. FEBS Lett. 1997;416(1):19–22.

    PubMed  CAS  Google Scholar 

  23. Portman MA, Xiao Y, Qian K, Tucker RL, Parish SM, Ning XH. Thyroid hormone coordinates respiratory control maturation and adenine nucleotide translocator expression in heart in vivo. Circulation. 2000;102(11):1323–9.

    PubMed  CAS  Google Scholar 

  24. Scarpulla RC, Kilar MC, Scarpulla KM. Coordinate induction of multiple cytochrome c mRNAs in response to thyroid hormone. J Biol Chem. 1986;261(10):4660–2.

    PubMed  CAS  Google Scholar 

  25. Luciakova K, Nelson BD. Transcript levels for nuclear-encoded mammalian mitochondrial respiratory-chain components are regulated by thyroid hormone in an uncoordinated fashion. Eur J Biochem. 1992;207(1):247–51.

    PubMed  CAS  Google Scholar 

  26. Gopalakrishnan L, Scarpulla RC. Differential regulation of respiratory chain subunits by a CREB-dependent signal transduction pathway. Role of cyclic AMP in cytochrome c and COXIV gene expression. J Biol Chem. 1994;269(1):105–13.

    PubMed  CAS  Google Scholar 

  27. Araki O, Ying H, Furuya F, Zhu X, Cheng SY. Thyroid hormone receptor beta mutants: dominant negative regulators of peroxisome proliferator-activated receptor gamma action. Proc Natl Acad Sci USA. 2005;102(45):16251–6.

    PubMed  CAS  Google Scholar 

  28. Buroker NE, Young ME, Wei C, et al. The dominant negative thyroid hormone receptor beta-mutant {Delta}337T alters PPAR{alpha} signaling in heart. Am J Physiol Endocrinol Metab. 2007;292(2):E453–60.

    PubMed  CAS  Google Scholar 

  29. Hansen MK, Connolly TM. Nuclear receptors as drug targets in obesity, dyslipidemia and atherosclerosis. Curr Opin Investig Drugs. 2008;9(3):247–55.

    PubMed  CAS  Google Scholar 

  30. Hart CM. The Role of PPARgamma in pulmonary vascular disease. J Investig Med. 2008;56(2):518–21.

    PubMed  CAS  Google Scholar 

  31. Weitzel JM, Iwen KA, Seitz HJ. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol. 2003;88(1):121–8.

    PubMed  CAS  Google Scholar 

  32. Yu M, Jaradat SA, Grossman LI. Genomic organization and promoter regulation of human cytochrome c oxidase subunit VII heart/muscle isoform (COX7AH). Biochim Biophys Acta. 2002;1574(3):345–53.

    PubMed  CAS  Google Scholar 

  33. Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115–24.

    PubMed  CAS  Google Scholar 

  34. McClure TD, Young ME, Taegtmeyer H, et al. Thyroid hormone interacts with PPARalpha and PGC-1 during mitochondrial maturation in sheep heart. Am J Physiol Heart Circ Physiol. 2005;289(5):H2258–64.

    PubMed  CAS  Google Scholar 

  35. Irrcher I, Adhihetty PJ, Sheehan T, Joseph AM, Hood DA. PPARgamma coactivator-1alpha expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations. Am J Physiol Cell Physiol. 2003;284(6):C1669–77.

    PubMed  CAS  Google Scholar 

  36. Mutvei A, Kuzela S, Nelson BD. Control of mitochondrial transcription by thyroid hormone. Eur J Biochem. 1989;180(1): 235–40.

    PubMed  CAS  Google Scholar 

  37. Fisher RP, Lisowsky T, Parisi MA, Clayton DA. DNA wrapping and bending by a mitochondrial high mobility group-like transcriptional activator protein. J Biol Chem. 1992;267(5): 3358–67.

    PubMed  CAS  Google Scholar 

  38. Marin-Garcia J, Ananthakrishnan R, Goldenthal MJ. Heart mitochondrial DNA and enzyme changes during early human development. Mol Cell Biochem. 2000;210(1–2):47–52.

    PubMed  CAS  Google Scholar 

  39. Garstka HL, Facke M, Escribano JR, Wiesner RJ. Stoichiometry of mitochondrial transcripts and regulation of gene expression by mitochondrial transcription factor A. Biochem Biophys Res Commun. 1994;200(1):619–26.

    PubMed  CAS  Google Scholar 

  40. Inagaki H, Kitano S, Lin KH, Maeda S, Saito T. Inhibition of mitochondrial gene expression by antisense RNA of mitochondrial transcription factor A (mtTFA). Biochem Mol Biol Int. 1998;45(3):567–73.

    PubMed  CAS  Google Scholar 

  41. Wallace DC. Animal models for mitochondrial disease. Methods Mol Biol. 2002;197:3–54.

    PubMed  CAS  Google Scholar 

  42. Wang J, Wilhelmsson H, Graff C, et al. Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat Genet. 1999;21(1):133–7.

    PubMed  CAS  Google Scholar 

  43. Schneider JJ, Hood DA. Effect of thyroid hormone on mtHsp70 expression, mitochondrial import and processing in cardiac muscle. J Endocrinol. 2000;165(1):9–17.

    PubMed  CAS  Google Scholar 

  44. Wrutniak C, Cassar-Malek I, Marchal S, et al. A 43-kDa protein related to c-Erb A alpha 1 is located in the mitochondrial matrix of rat liver. J Biol Chem. 1995;270(27):16347–54.

    PubMed  CAS  Google Scholar 

  45. Casas F, Rochard P, Rodier A, et al. A variant form of the nuclear triiodothyronine receptor c-ErbAalpha1 plays a direct role in regulation of mitochondrial RNA synthesis. Mol Cell Biol. 1999;19(12):7913–24.

    PubMed  CAS  Google Scholar 

  46. Morrish F, Buroker NE, Ge M, 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.

    PubMed  CAS  Google Scholar 

  47. Andersson ML, Vennstrom B. Chicken thyroid hormone receptor alpha requires the N-terminal amino acids for exclusive nuclear localization. FEBS Lett. 1997;416(3):291–6.

    PubMed  CAS  Google Scholar 

  48. Casas F, Daury L, Grandemange S, et al. Endocrine regulation of mitochondrial activity: involvement of truncated RXRalpha and c-Erb Aalpha1 proteins. FASEB J. 2003;17(3):426–36.

    PubMed  CAS  Google Scholar 

  49. Enriquez JA, Fernandez-Silva P, Garrido-Perez N, Lopez-Perez MJ, Perez-Martos A, Montoya J. Direct regulation of mitochondrial RNA synthesis by thyroid hormone. Mol Cell Biol. 1999;19(1):657–70.

    PubMed  CAS  Google Scholar 

  50. Sterling K. Direct thyroid hormone activation of mitochondria: the role of adenine nucleotide translocase. Endocrinology. 1986;119(1):292–5.

    PubMed  CAS  Google Scholar 

  51. Sterling K. Direct thyroid hormone activation of mitochondria: identification of adenine nucleotide translocase (AdNT) as the hormone receptor. Trans Assoc Am Physicians. 1987;100: 284–93.

    PubMed  CAS  Google Scholar 

  52. Sterling K. Thyroid hormone action: identification of the mitochondrial thyroid hormone receptor as adenine nucleotide translocase. Thyroid. 1991;1(2):167–71.

    PubMed  CAS  Google Scholar 

  53. Sterling K, Milch PO. Thyroid hormone binding by a component of mitochondrial membrane. Proc Natl Acad Sci USA. 1975;72(8):3225–9.

    PubMed  CAS  Google Scholar 

  54. Goglia F, Torresani J, Bugli P, Barletta A, Liverini G. In vitro binding of triiodothyronine to rat liver mitochondria. Pflugers Arch. 1981;390(2):120–4.

    PubMed  CAS  Google Scholar 

  55. Hashizume K, Ichikawa K. Localization of 3,5,3′-L-triiodothyronine receptor in rat kidney mitochondrial membranes. Biochem Biophys Res Commun. 1982;106(3):920–6.

    PubMed  CAS  Google Scholar 

  56. Sterling K, Campbell GA, Brenner MA. Purification of the mitochondrial triiodothyronine (T3) receptor from rat liver. Acta Endocrinol (Copenh). 1984;105(3):391–7.

    CAS  Google Scholar 

  57. Aquila H, Misra D, Eulitz M, Klingenberg M. Complete amino acid sequence of the ADP/ATP carrier from beef heart mitochondria. Hoppe Seylers Z Physiol Chem. 1982;363(3):345–9.

    PubMed  CAS  Google Scholar 

  58. Babior BM, Creagan S, Ingbar SH, Kipnes RS. Stimulation of mitochondrial adenosine diphosphate uptake by thyroid hormones. Proc Natl Acad Sci USA. 1973;70(1):98–102.

    PubMed  CAS  Google Scholar 

  59. Protnay GI, McClendon FD, Bush JE, Braverman LE, Babior BM. The effect of physiological doses of thyroxine on carrier-mediated ADP uptake by liver mitochondria from thyroidectomized rats. Biochem Biophys Res Commun. 1973;55(1):17–21.

    PubMed  CAS  Google Scholar 

  60. 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.

    PubMed  CAS  Google Scholar 

  61. Saelim N, John LM, Wu J, et al. Nontranscriptional modulation of intracellular Ca2+ signaling by ligand stimulated thyroid hormone receptor. J Cell Biol. 2004;167(5):915–24.

    PubMed  CAS  Google Scholar 

  62. Spinks A, Burn JH. Thyroid activity and amine oxidase in the liver. Br J Pharmacol Chemother. 1952;7(1):93–8.

    PubMed  CAS  Google Scholar 

  63. Schayer RW, Wu KY, Smiley RL, Kobayashi Y. Studies on monoamine oxidase in intact animals. J Biol Chem. 1954;210(1): 259–67.

    PubMed  CAS  Google Scholar 

  64. Sourkes TL, Missala K, Bastomsky CH, Fang TY. Metabolism of monoamines and diamines in hyperthyroid and hypothyroid rats. Can J Biochem. 1977;55(8):789–95.

    PubMed  CAS  Google Scholar 

  65. Egashira T, Yamanaka Y. Changes in MAO activities in several organs of rats after administration of l-thyroxine. Jpn J Pharmacol. 1987;45(2):135–42.

    PubMed  CAS  Google Scholar 

  66. Ichikawa K, Hashizume K, Yamada T. Monoamine oxidase inhibitory modulators in rat heart cytosol: evidence for induction by thyroid hormone. Endocrinology. 1982;111(6):1803–9.

    PubMed  CAS  Google Scholar 

  67. 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.

    PubMed  CAS  Google Scholar 

  68. 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.

    PubMed  CAS  Google Scholar 

  69. Goldenthal MJ, Ananthakrishnan R, Marin-Garcia J. Nuclear-mitochondrial cross-talk in cardiomyocyte T3 signaling: a time-course analysis. J Mol Cell Cardiol. 2005;39(2):319–26.

    PubMed  CAS  Google Scholar 

  70. Sheehan TE, Kumar PA, Hood DA. Tissue-specific regulation of cytochrome c oxidase subunit expression by thyroid hormone. Am J Physiol Endocrinol Metab. 2004;286(6):E968–74.

    PubMed  CAS  Google Scholar 

  71. Wiesner RJ, Kurowski TT, Zak R. Regulation by thyroid hormone of nuclear and mitochondrial genes encoding subunits of cytochrome-c oxidase in rat liver and skeletal muscle. Mol Endocrinol. 1992;6(9):1458–67.

    PubMed  CAS  Google Scholar 

  72. Arnold S, Goglia F, Kadenbach B. 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur J Biochem. 1998;252(2): 325–30.

    PubMed  CAS  Google Scholar 

  73. Goglia F, Lanni A, Barth J, Kadenbach B. Interaction of diiodothyronines with isolated cytochrome c oxidase. FEBS Lett. 1994;346(2–3):295–8.

    PubMed  CAS  Google Scholar 

  74. Paradies G, Petrosillo G, Ruggiero FM. Cardiolipin-dependent decrease of cytochrome c oxidase activity in heart mitochondria from hypothyroid rats. Biochim Biophys Acta. 1997;1319(1):5–8.

    PubMed  CAS  Google Scholar 

  75. Iglesias T, Caubin J, Zaballos A, Bernal J, Munoz A. Identification of the mitochondrial NADH dehydrogenase subunit 3 (ND3) as a thyroid hormone regulated gene by whole genome PCR analysis. Biochem Biophys Res Commun. 1995;210(3):995–1000.

    PubMed  CAS  Google Scholar 

  76. Short KR, Nygren J, Barazzoni R, Levine J, Nair KS. T(3) increases mitochondrial ATP production in oxidative muscle despite increased expression of UCP2 and -3. Am J Physiol Endocrinol Metab. 2001;280(5):E761–9.

    PubMed  CAS  Google Scholar 

  77. Portman MA. The adenine nucleotide translocator: regulation and function during myocardial development and hypertrophy. Clin Exp Pharmacol Physiol. 2002;29(4):334–8.

    PubMed  CAS  Google Scholar 

  78. Scholz TD, TenEyck CJ, Schutte BC. Thyroid hormone regulation of the NADH shuttles in liver and cardiac mitochondria. J Mol Cell Cardiol. 2000;32(1):1–10.

    PubMed  CAS  Google Scholar 

  79. Gong DW, Bi S, Weintraub BD, Reitman M. Rat mitochondrial glycerol-3-phosphate dehydrogenase gene: multiple promoters, high levels in brown adipose tissue, and tissue-specific regulation by thyroid hormone. DNA Cell Biol. 1998;17(3):301–9.

    PubMed  CAS  Google Scholar 

  80. Paradies G, Ruggiero FM. Effect of hyperthyroidism on the transport of pyruvate in rat-heart mitochondria. Biochim Biophys Acta. 1988;935(1):79–86.

    PubMed  CAS  Google Scholar 

  81. Laughlin MR, Taylor JF, Chesnick AS, Balaban RS. Regulation of glycogen metabolism in canine myocardium: effects of insulin and epinephrine in vivo. Am J Physiol. 1992;262(6 Pt 1):E875–83.

    PubMed  CAS  Google Scholar 

  82. Drake AJ, Haines JR, Noble MI. Preferential uptake of lactate by the normal myocardium in dogs. Cardiovasc Res. 1980;14(2): 65–72.

    PubMed  CAS  Google Scholar 

  83. Trosper TL, Philipson KD. Lactate transport by cardiac sarcolemmal vesicles. Am J Physiol. 1987;252(5 Pt 1):C483–9.

    PubMed  CAS  Google Scholar 

  84. Hashimoto T, Hussien R, Brooks GA. Colocalization of MCT1, CD147, and LDH in mitochondrial inner membrane of L6 muscle cells: evidence of a mitochondrial lactate oxidation complex. Am J Physiol Endocrinol Metab. 2006;290(6):E1237–44.

    PubMed  CAS  Google Scholar 

  85. Wang Y, Tonouchi M, Miskovic D, Hatta H, Bonen A. T3 increases lactate transport and the expression of MCT4, but not MCT1, in rat skeletal muscle. Am J Physiol Endocrinol Metab. 2003;285(3): E622–8.

    PubMed  CAS  Google Scholar 

  86. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Alterations in carnitine-acylcarnitine translocase activity and in phospholipid composition in heart mitochondria from hypothyroid rats. Biochim Biophys Acta. 1997;1362(2–3):193–200.

    PubMed  CAS  Google Scholar 

  87. Daum G. Lipids of mitochondria. Biochim Biophys Acta. 1985;822(1):1–42.

    PubMed  CAS  Google Scholar 

  88. Hoch FL. Cardiolipins and biomembrane function. Biochim Biophys Acta. 1992;1113(1):71–133.

    PubMed  CAS  Google Scholar 

  89. Hostetler KY, van den Bosch H. Subcellular and submitochondrial localization of the biosynthesis of cardiolipin and related phospholipids in rat liver. Biochim Biophys Acta. 1972;260(3):380–6.

    PubMed  CAS  Google Scholar 

  90. Hatch GM. Cardiolipin biosynthesis in the isolated heart. Biochem J. 1994;297(Pt 1):201–8.

    PubMed  CAS  Google Scholar 

  91. Indiveri C, Tonazzi A, Prezioso G, Palmieri F. Kinetic characterization of the reconstituted carnitine carrier from rat liver mitochondria. Biochim Biophys Acta. 1991;1065(2):231–8.

    PubMed  CAS  Google Scholar 

  92. Paradies G, Ruggiero FM. Decreased activity of the pyruvate translocator and changes in the lipid composition in heart mitochondria from hypothyroid rats. Arch Biochem Biophys. 1989;269(2):595–602.

    PubMed  CAS  Google Scholar 

  93. Hostetler KY. Effect of thyroxine on the activity of mitochondrial cardiolipin synthase in rat liver. Biochim Biophys Acta. 1991;1086(1):139–40.

    PubMed  CAS  Google Scholar 

  94. Cao SG, Cheng P, Angel A, Hatch GM. Thyroxine stimulates phosphatidylglycerolphosphate synthase activity in rat heart mitochondria. Biochim Biophys Acta. 1995;1256(2):241–4.

    PubMed  Google Scholar 

  95. Brand MD, Pakay JL, Ocloo A, et al. The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J. 2005;392(Pt 2):353–62.

    PubMed  CAS  Google Scholar 

  96. Couplan E, del Mar Gonzalez-Barroso M, Alves-Guerra MC, Ricquier D, Goubern M, Bouillaud F. No evidence for a basal, retinoic, or superoxide-induced uncoupling activity of the uncoupling protein 2 present in spleen or lung mitochondria. J Biol Chem. 2002;277(29):26268–75.

    PubMed  CAS  Google Scholar 

  97. Cadenas S, Echtay KS, Harper JA, et al. The basal proton conductance of skeletal muscle mitochondria from transgenic mice overexpressing or lacking uncoupling protein-3. J Biol Chem. 2002;277(4):2773–8.

    PubMed  CAS  Google Scholar 

  98. Pecqueur C, Couplan E, Bouillaud F, Ricquier D. Genetic and physiological analysis of the role of uncoupling proteins in human energy homeostasis. J Mol Med (Berl). 2001;79(1):48–56.

    CAS  Google Scholar 

  99. Brand MD. The efficiency and plasticity of mitochondrial energy transduction. Biochem Soc Trans. 2005;33(Pt 5):897–904.

    PubMed  CAS  Google Scholar 

  100. Goldenthal MJ, Weiss HR, Marin-Garcia J. Bioenergetic remodeling of heart mitochondria by thyroid hormone. Mol Cell Biochem. 2004;265(1–2):97–106.

    PubMed  CAS  Google Scholar 

  101. Scarpulla RC. Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem. 2006;97(4):673–83.

    PubMed  CAS  Google Scholar 

  102. Feng X, Jiang Y, Meltzer P, Yen PM. Thyroid hormone regulation of hepatic genes in vivo detected by complementary DNA microarray. Mol Endocrinol. 2000;14(7):947–55.

    PubMed  CAS  Google Scholar 

  103. Miller LD, Park KS, Guo QM, et al. Silencing of Wnt signaling and activation of multiple metabolic pathways in response to thyroid hormone-stimulated cell proliferation. Mol Cell Biol. 2001;21(19):6626–39.

    PubMed  CAS  Google Scholar 

  104. Weitzel JM, Radtke C, Seitz HJ. Two thyroid hormone-mediated gene expression patterns in vivo identified by cDNA expression arrays in rat. Nucleic Acids Res. 2001;29(24):5148–55.

    PubMed  CAS  Google Scholar 

  105. Clement K, Viguerie N, Diehn M, et al. In vivo regulation of human skeletal muscle gene expression by thyroid hormone. Genome Res. 2002;12(2):281–91.

    PubMed  CAS  Google Scholar 

  106. Flores-Morales A, Gullberg H, Fernandez L, et al. Patterns of liver gene expression governed by TRbeta. Mol Endocrinol. 2002;16(6):1257–68.

    PubMed  CAS  Google Scholar 

  107. Denver RJ, Pavgi S, Shi YB. Thyroid hormone-dependent gene expression program for Xenopus neural development. J Biol Chem. 1997;272(13):8179–88.

    PubMed  CAS  Google Scholar 

  108. Weitzel JM, Kutz S, Radtke C, Grott S, Seitz HJ. Hormonal regulation of multiple promoters of the rat mitochondrial glycerol-3-phosphate dehydrogenase gene: identification of a complex hormone-response element in the ubiquitous promoter B. Eur J Biochem. 2001;268(14):4095–103.

    PubMed  CAS  Google Scholar 

  109. Li R, Luciakova K, Zaid A, Betina S, Fridell E, Nelson BD. Thyroid hormone activates transcription from the promoter regions of some human nuclear-encoded genes of the oxidative phosphorylation system. Mol Cell Endocrinol. 1997;128(1–2):69–75.

    PubMed  CAS  Google Scholar 

  110. Evans MJ, Scarpulla RC. Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. Characterization of upstream NRF-1, ATF, and intron Sp1 recognition sequences. J Biol Chem. 1989;264(24):14361–8.

    PubMed  CAS  Google Scholar 

  111. Zaid A, Li R, Luciakova K, Barath P, Nery S, Nelson BD. On the role of the general transcription factor Sp1 in the activation and repression of diverse mammalian oxidative phosphorylation genes. J Bioenerg Biomembr. 1999;31(2):129–35.

    PubMed  CAS  Google Scholar 

  112. Virbasius JV, Scarpulla RC. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci USA. 1994;91(4):1309–13.

    PubMed  CAS  Google Scholar 

  113. Huo L, Scarpulla RC. Mitochondrial DNA instability and peri-implantation lethality associated with targeted disruption of nuclear respiratory factor 1 in mice. Mol Cell Biol. 2001;21(2):644–54.

    PubMed  CAS  Google Scholar 

  114. Carter RS, Avadhani NG. Cloning and characterization of the mouse cytochrome c oxidase subunit IV gene. Arch Biochem Biophys. 1991;288(1):97–106.

    PubMed  CAS  Google Scholar 

  115. Virbasius JV, Scarpulla RC. Transcriptional activation through ETS domain binding sites in the cytochrome c oxidase subunit IV gene. Mol Cell Biol. 1991;11(11):5631–8.

    PubMed  CAS  Google Scholar 

  116. Virbasius JV, Virbasius CA, Scarpulla RC. Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev. 1993;7(3):380–92.

    PubMed  CAS  Google Scholar 

  117. Chung AB, Stepien G, Haraguchi Y, Li K, Wallace DC. Transcriptional control of nuclear genes for the mitochondrial muscle ADP/ATP translocator and the ATP synthase beta subunit. Multiple factors interact with the OXBOX/REBOX promoter sequences. J Biol Chem. 1992;267(29):21154–61.

    PubMed  CAS  Google Scholar 

  118. Suzuki H, Hosokawa Y, Nishikimi M, Ozawa T. Existence of common homologous elements in the transcriptional regulatory regions of human nuclear genes and mitochondrial gene for the oxidative phosphorylation system. J Biol Chem. 1991;266(4): 2333–8.

    PubMed  CAS  Google Scholar 

  119. Suzuki H, Suzuki S, Kumar S, Ozawa T. Human nuclear and mitochondrial Mt element-binding proteins to regulatory regions of the nuclear respiratory genes and to the mitochondrial promoter region. Biochem Biophys Res Commun. 1995;213(1):204–10.

    PubMed  CAS  Google Scholar 

  120. Wu Y, Delerive P, Chin WW, Burris TP. Requirement of helix 1 and the AF-2 domain of the thyroid hormone receptor for coactivation by PGC-1. J Biol Chem. 2002;277(11):8898–905.

    PubMed  CAS  Google Scholar 

  121. Knutti D, Kralli A. PGC-1, a versatile coactivator. Trends Endocrinol Metab. 2001;12(8):360–5.

    PubMed  CAS  Google Scholar 

  122. Andersson U, Scarpulla RC. Pgc-1-related coactivator, a novel, serum-inducible coactivator of nuclear respiratory factor 1-dependent transcription in mammalian cells. Mol Cell Biol. 2001;21(11): 3738–49.

    PubMed  CAS  Google Scholar 

  123. Lin J, Puigserver P, Donovan J, Tarr P, Spiegelman BM. Peroxisome proliferator-activated receptor gamma coactivator 1beta (PGC-1beta), a novel PGC-1-related transcription coactivator associated with host cell factor. J Biol Chem. 2002;277(3):1645–8.

    PubMed  CAS  Google Scholar 

  124. Kressler D, Schreiber SN, Knutti D, Kralli A. The PGC-1-related protein PERC is a selective coactivator of estrogen receptor alpha. J Biol Chem. 2002;277(16):13918–25.

    PubMed  CAS  Google Scholar 

  125. Hihi AK, Michalik L, Wahli W. PPARs: transcriptional effectors of fatty acids and their derivatives. Cell Mol Life Sci. 2002;59(5): 790–8.

    PubMed  CAS  Google Scholar 

  126. Young ME, Patil S, Ying J, et al. Uncoupling protein 3 transcription is regulated by peroxisome proliferator-activated receptor (alpha) in the adult rodent heart. FASEB J. 2001;15(3):833–45.

    PubMed  CAS  Google Scholar 

  127. Katz D, Lazar MA. Dominant negative activity of an endogenous thyroid hormone receptor variant (alpha 2) is due to competition for binding sites on target genes. J Biol Chem. 1993;268(28): 20904–10.

    PubMed  CAS  Google Scholar 

  128. Mitsuhashi T, Tennyson GE, Nikodem VM. Alternative splicing generates messages encoding rat c-erbA proteins that do not bind thyroid hormone. Proc Natl Acad Sci USA. 1988;85(16):5804–8.

    PubMed  CAS  Google Scholar 

  129. Ruggiero FM, Landriscina C, Gnoni GV, Quagliariello E. Lipid composition of liver mitochondria and microsomes in hyperthyroid rats. Lipids. 1984;19(3):171–8.

    PubMed  CAS  Google Scholar 

  130. Paradies G, Ruggiero FM. Effect of aging on the activity of the phosphate carrier and on the lipid composition in rat liver mitochondria. Arch Biochem Biophys. 1991;284(2):332–7.

    PubMed  CAS  Google Scholar 

  131. Mak IT, Shrago E, Elson CE. Effect of thyroidectomy on the kinetics of ADP-ATP translocation in liver mitochondria. Arch Biochem Biophys. 1983;226(1):317–23.

    PubMed  CAS  Google Scholar 

  132. Paradies G, Ruggiero FM, Dinoi P, Petrosillo G, Quagliariello E. Decreased cytochrome oxidase activity and changes in phospholipids in heart mitochondria from hypothyroid rats. Arch Biochem Biophys. 1993;307(1):91–5.

    PubMed  CAS  Google Scholar 

  133. Paradies G, Ruggiero FM, Dinoi P. The influence of hypothyroidism on the transport of phosphate and on the lipid composition in rat-liver mitochondria. Biochim Biophys Acta. 1991;1070(1): 180–6.

    PubMed  CAS  Google Scholar 

  134. Komiya T, Sakaguchi M, Mihara K. Cytoplasmic chaperones determine the targeting pathway of precursor proteins to mitochondria. EMBO J. 1996;15(2):399–407.

    PubMed  CAS  Google Scholar 

  135. Braun HP, Schmitz UK. The mitochondrial processing peptidase. Int J Biochem Cell Biol. 1997;29(8–9):1043–5.

    PubMed  CAS  Google Scholar 

  136. Colavecchia M, Christie LN, Kanwar YS, Hood DA. Functional consequences of thyroid hormone-induced changes in the mitochondrial protein import pathway. Am J Physiol Endocrinol Metab. 2003;284(1):E29–35.

    PubMed  CAS  Google Scholar 

  137. Craig EE, Chesley A, Hood DA. Thyroid hormone modifies mitochondrial phenotype by increasing protein import without altering degradation. Am J Physiol. 1998;275(6 Pt 1):C1508–15.

    PubMed  CAS  Google Scholar 

  138. Davis PJ, Shih A, Lin HY, Martino LJ, Davis FB. Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J Biol Chem. 2000;275(48):38032–9.

    PubMed  CAS  Google Scholar 

  139. Knutti D, Kressler D, Kralli A. Regulation of the transcriptional coactivator PGC-1 via MAPK-sensitive interaction with a repressor. Proc Natl Acad Sci USA. 2001;98(17):9713–8.

    PubMed  CAS  Google Scholar 

  140. Puigserver P, Rhee J, Lin J, et al. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Mol Cell. 2001;8(5):971–82.

    PubMed  CAS  Google Scholar 

  141. Lin HY, Davis FB, Gordinier JK, Martino LJ, Davis PJ. Thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells. Am J Physiol. 1999;276(5 Pt 1):C1014–24.

    PubMed  CAS  Google Scholar 

  142. Tanaka T, Morita H, Koide H, Kawamura K, Takatsu T. Biochemical and morphological study of cardiac hypertrophy. Effects of thyroxine on enzyme activities in the rat myocardium. Basic Res Cardiol. 1985;80(2):165–74.

    PubMed  CAS  Google Scholar 

  143. Nelson BD, Luciakova K, Li R, Betina S. The role of thyroid hormone and promoter diversity in the regulation of nuclear encoded mitochondrial proteins. Biochim Biophys Acta. 1995;1271(1): 85–91.

    PubMed  Google Scholar 

  144. Goglia F, Moreno M, Lanni A. Action of thyroid hormones at the cellular level: the mitochondrial target. FEBS Lett. 1999;452(3):115–20.

    PubMed  CAS  Google Scholar 

  145. Leung AC, McKee EE. Mitochondrial protein synthesis during thyroxine-induced cardiac hypertrophy. Am J Physiol. 1990;258(3 Pt 1):E511–8.

    PubMed  CAS  Google Scholar 

  146. Wiesner RJ, Aschenbrenner V, Ruegg JC, Zak R. Coordination of nuclear and mitochondrial gene expression during the development of cardiac hypertrophy in rats. Am J Physiol. 1994;267(1 Pt 1):C229–35.

    PubMed  CAS  Google Scholar 

  147. Ralphe JC, Bedell K, Segar JL, Scholz TD. Correlation between myocardial malate/aspartate shuttle activity and EAAT1 protein expression in hyper- and hypothyroidism. Am J Physiol Heart Circ Physiol. 2005;288(5):H2521–6.

    PubMed  CAS  Google Scholar 

  148. Hagiwara T, Tanaka K, Takai S, Maeno-Hikichi Y, Mukainaka Y, Wada K. Genomic organization, promoter analysis, and ­chromosomal localization of the gene for the mouse glial high-affinity glutamate transporter Slc1a3. Genomics. 1996;33(3): 508–15.

    PubMed  CAS  Google Scholar 

  149. Hollenberg AN, Monden T, Wondisford FE. Ligand-independent and -dependent functions of thyroid hormone receptor isoforms depend upon their distinct amino termini. J Biol Chem. 1995;270(24):14274–80.

    PubMed  CAS  Google Scholar 

  150. Kim MK, Lee JS, Chung JH. In vivo transcription factor recruitment during thyroid hormone receptor-mediated activation. Proc Natl Acad Sci USA. 1999;96(18):10092–7.

    PubMed  CAS  Google Scholar 

  151. Desai-Yajnik V, Samuels HH. The NF-kappa B and Sp1 motifs of the human immunodeficiency virus type 1 long terminal repeat function as novel thyroid hormone response elements. Mol Cell Biol. 1993;13(8):5057–69.

    PubMed  CAS  Google Scholar 

  152. Pich S, Bach D, Briones P, et al. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum Mol Genet. 2005;14(11): 1405–15.

    PubMed  CAS  Google Scholar 

  153. Bach D, Naon D, Pich S, et al. Expression of Mfn2, the Charcot-Marie-Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor alpha and interleukin-6. Diabetes. 2005;54(9):2685–93.

    PubMed  CAS  Google Scholar 

  154. Soriano FX, Liesa M, Bach D, Chan DC, Palacin M, Zorzano A. Evidence for a mitochondrial regulatory pathway defined by peroxisome proliferator-activated receptor-gamma coactivator-1 alpha, estrogen-related receptor-alpha, and mitofusin 2. Diabetes. 2006;55(6):1783–91.

    PubMed  CAS  Google Scholar 

  155. Yu T, Robotham JL, Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci USA. 2006;103(8):2653–8.

    PubMed  CAS  Google Scholar 

  156. Meeusen S, DeVay R, Block J, et al. Mitochondrial inner-­membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell. 2006;127(2):383–95.

    PubMed  CAS  Google Scholar 

  157. Song Z, Ghochani M, McCaffery JM, Frey TG, Chan DC. Mitofusins and OPA1 mediate sequential steps in mitochondrial membrane fusion. Mol Biol Cell. 2009;20(15):3525–32.

    PubMed  CAS  Google Scholar 

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Marín-García, J. (2013). Thyroid Hormone and Myocardial Mitochondria. In: Mitochondria and Their Role in Cardiovascular Disease. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-4599-9_22

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