Home The key roles of thyroid hormone in mitochondrial regulation, at interface of human health and disease
Article
Licensed
Unlicensed Requires Authentication

The key roles of thyroid hormone in mitochondrial regulation, at interface of human health and disease

  • Serena Sagliocchi , Federica Restolfer , Alessandro Cossidente and Monica Dentice EMAIL logo
Published/Copyright: July 19, 2024
Journal of Basic and Clinical Physiology and Pharmacology
From the journal Journal of Basic and Clinical Physiology and Pharmacology Volume 35 Issue 4-5

Abstract

Mitochondria are highly plastic and dynamic organelles long known as the powerhouse of cellular bioenergetics, but also endowed with a critical role in stress responses and homeostasis maintenance, supporting and integrating activities across multifaced cellular processes. As a such, mitochondria dysfunctions are leading causes of a wide range of diseases and pathologies. Thyroid hormones (THs) are endocrine regulators of cellular metabolism, regulating intracellular nutrients fueling of sugars, amino acids and fatty acids. For instance, THs regulate the balance between the anabolism and catabolism of all the macro-molecules, influencing energy homeostasis during different nutritional conditions. Noteworthy, not only most of the TH-dependent metabolic modulations act via the mitochondria, but also THs have been proved to regulate the mitochondrial biosynthesis, dynamics and function. The significance of such an interplay is different in the context of specific tissues and strongly impacts on cellular homeostasis. Thus, a comprehensive understanding of THs-dependent mitochondrial functions and dynamics is required to develop more precise strategies for targeting mitochondrial function. Herein, we describe the mechanisms of TH-dependent metabolic regulation with a focus on mitochondrial action, in different tissue contexts, thus providing new insights for targeted modulation of mitochondrial dynamics.

Keywords: thyroid hormone; metabolism; mitochondria
Corresponding author: Monica Dentice, Department of Clinical Medicine and Surgery, University of Naples “Federico II”, 80131, Naples, Italy, E-mail:

Funding source: Fondazione Telethon

Award Identifier / Grant number: GMR22T1020

Funding source: Ministero dell’Istruzione, dell’Università e della Ricerca

Award Identifier / Grant number: 2022HB54P9

Funding source: Associazione Italiana per la Ricerca sul Cancro

Award Identifier / Grant number: IG 29242

  1. Research ethics: Not applicable.

  2. Informed consent: Not applicable.

  3. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  4. Competing interests: Authors state no conflict of interest.

  5. Research funding: This work was supported by grants from AIRC to M.D. (IG 29242), by Telethon to M.D. (GMR22T1020) and by a PRIN-2022 grant from MIUR awarded to M.D. (2022HB54P9).

  6. Data availability: Not applicable.

References

1. Brent, GA. Mechanisms of thyroid hormone action. J Clin Invest 2012;122:3035–43. https://doi.org/10.1172/JCI60047 [Epub 2012 Sep 4].Search in Google Scholar PubMed PubMed Central

2. Cheng, SY, Leonard, JL, Davis, PJ. Molecular aspects of thyroid hormone actions. Endocr Rev 2010;31:139–70. https://doi.org/10.1210/er.2009-0007 [Epub 2010 Jan 5].Search in Google Scholar PubMed PubMed Central

3. Cicatiello, AG, Di Girolamo, D, Dentice, M. Metabolic effects of the intracellular regulation of thyroid hormone: old players, new concepts. Front Endocrinol 2018;9:474. https://doi.org/10.3389/fendo.2018.00474.Search in Google Scholar PubMed PubMed Central

4. Nappi, A, Murolo, M, Cicatiello, AG, Sagliocchi, S, Di Cicco, E, Raia, M, et al.. Thyroid hormone receptor isoforms alpha and beta play convergent roles in muscle physiology and metabolic regulation. Metabolites 2022;12:405. https://doi.org/10.3390/metabo12050405.Search in Google Scholar PubMed PubMed Central

5. Nappi, A, Murolo, M, Sagliocchi, S, Miro, C, Cicatiello, AG, Di Cicco, E, et al.. Selective inhibition of genomic and non-genomic effects of thyroid hormone regulates muscle cell differentiation and metabolic behavior. Int J Mol Sci 2021;22:7175. https://doi.org/10.3390/ijms22137175.Search in Google Scholar PubMed PubMed Central

6. Hönes, 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:E11323–32. https://doi.org/10.1073/pnas.1706801115 [Epub 2017 Dec 11].Search in Google Scholar PubMed PubMed Central

7. Köhrle, J. The deiodinase family: selenoenzymes regulating thyroid hormone availability and action. Cell Mol Life Sci 2000;57:1853–63. https://doi.org/10.1007/PL00000667.Search in Google Scholar PubMed PubMed Central

8. Dentice, M, Marsili, A, Zavacki, A, Larsen, PR, Salvatore, D. The deiodinases and the control of intracellular thyroid hormone signaling during cellular differentiation. Biochim Biophys Acta 2013;1830:3937–45. https://doi.org/10.1016/j.bbagen.2012.05.007 [Epub 2012 May 25].Search in Google Scholar PubMed PubMed Central

9. Ambrosio, R, Damiano, V, Sibilio, A, De Stefano, MA, Avvedimento, VE, Salvatore, D, et al.. Epigenetic control of type 2 and 3 deiodinases in myogenesis: role of lysine-specific demethylase enzyme and FoxO3. Nucleic Acids Res 2013;41:3551–62. https://doi.org/10.1093/nar/gkt065 [Epub 2013 Feb 8].Search in Google Scholar PubMed PubMed Central

10. Marsili, A, Tang, D, Harney, JW, Singh, P, Zavacki, AM, Dentice, M, et al.. Type II iodothyronine deiodinase provides intracellular 3, 5, 3’-triiodothyronine to normal and regenerating mouse skeletal muscle. Am J Physiol Endocrinol Metab 2011;301:E818–24. https://doi.org/10.1152/ajpendo.00292.2011 [Epub 2011 Jul 19].Search in Google Scholar PubMed PubMed Central

11. Luongo, C, Dentice, M, Salvatore, D. Deiodinases and their intricate role in thyroid hormone homeostasis. Nat Rev Endocrinol 2019;15:479–88. https://doi.org/10.1038/s41574-019-0218-2.Search in Google Scholar PubMed

12. Chan, SY, Franklyn, JA, Pemberton, HN, Bulmer, JN, Visser, TJ, McCabe, CJ, et al.. Monocarboxylate transporter 8 expression in the human placenta: the effects of severe intrauterine growth restriction. J Endocrinol 2006;189:465–71. https://doi.org/10.1677/joe.1.06582.Search in Google Scholar PubMed PubMed Central

13. Mancino, G, Miro, C, Di Cicco, E, Dentice, M. Thyroid hormone action in epidermal development and homeostasis and its implications in the pathophysiology of the skin. J Endocrinol Invest 2021;44:1571–9. https://doi.org/10.1007/s40618-020-01492-2.Search in Google Scholar PubMed PubMed Central

14. Luongo, C, Martin, C, Vella, K, Marsili, A, Ambrosio, R, Dentice, M, et al.. The selective loss of the type 2 iodothyronine deiodinase in mouse thyrotrophs increases basal TSH but blunts the thyrotropin response to hypothyroidism. Endocrinology 2015;156:745–54. https://doi.org/10.1210/en.2014-1698 [Epub 2014 Dec 2].Search in Google Scholar PubMed PubMed Central

15. Warner, A, Mittag, J. Thyroid hormone and the central control of homeostasis. J Mol Endocrinol 2012;49:R29–35. https://doi.org/10.1530/jme-12-0068.Search in Google Scholar PubMed

16. Iwen, KA, Schröder, E, Brabant, G. Thyroid hormones and the metabolic syndrome. Eur Thyroid J 2013;2:83–92. https://doi.org/10.1159/000351249 [Epub 2013 May 28].Search in Google Scholar PubMed PubMed Central

17. Ueta, CB, Olivares, EL, Bianco, AC. Responsiveness to thyroid hormone and to ambient temperature underlies differences between brown adipose tissue and skeletal muscle thermogenesis in a mouse model of diet-induced obesity. Endocrinology 2011;152:3571–81. Erratum in: Endocrinology. 2011 Dec;152(12):5079. https://doi.org/10.1210/en.2011-1066 [Epub 2011 Jul 19].Search in Google Scholar PubMed PubMed Central

18. Fonseca, TL, Werneck-De-Castro, JP, Castillo, M, Bocco, BM, Fernandes, GW, McAninch, EA, et al.. Tissue-specific inactivation of type 2 deiodinase reveals multilevel control of fatty acid oxidation by thyroid hormone in the mouse. Diabetes 2014;63:1594–604. Erratum in: Diabetes. 2014 Aug;63(8):2895. Ferreira, Alexandre [corrected to Ferreira, Alexander R]. https://doi.org/10.2337/db13-1768 [Epub 2014 Jan 31].Search in Google Scholar PubMed PubMed Central

19. Fox, CS, Pencina, MJ, D’Agostino, RB, Murabito, JM, Seely, EW, Pearce, EN, et al.. Relations of thyroid function to body weight: cross-sectional and longitudinal observations in a community-based sample. Arch Intern Med 2008;168:587–92. https://doi.org/10.1001/archinte.168.6.587.Search in Google Scholar PubMed

20. Oppenheimer, JH, Schwartz, HL, Lane, JT, Thompson, MP. Functional relationship of thyroid hormone-induced lipogenesis, lipolysis, and thermogenesis in the rat. J Clin Invest 1991;87:125–32. https://doi.org/10.1172/JCI114961.Search in Google Scholar PubMed PubMed Central

21. Müller, MJ, Seitz, HJ. Thyroid hormone action on intermediary metabolism. Klin Wochenschr 1984;62:97–102. https://doi.org/10.1007/BF01738699.Search in Google Scholar PubMed

22. López, M, Alvarez, CV, Nogueiras, R, Diéguez, C. Energy balance regulation by thyroid hormones at central level. Trends Mol Med 2013;19:418–27. https://doi.org/10.1016/j.molmed.2013.04.004 [Epub 2013 May 23].Search in Google Scholar PubMed

23. Brent, GA. Clinical practice. Graves’ disease. N Engl J Med 2008;358:2594–605. https://doi.org/10.1056/NEJMcp0801880.Search in Google Scholar PubMed

24. Brent, GA. Hypothyroidism and thyroiditis. In: Melmed, SP, Larsen, PR, Kronenberg, HM, editors. Williams textbook of endocrinology. Philadelphia, PA: Elsevier; 2012.Search in Google Scholar

25. Silva, JE. Thermogenic mechanisms and their hormonal regulation. Physiol Rev 2006;86:435–64. https://doi.org/10.1152/physrev.00009.2005.Search in Google Scholar PubMed

26. Hafner, RP, Nobes, CD, McGown, AD, Brand, MD. Altered relationship between protonmotive force and respiration rate in non-phosphorylating liver mitochondria isolated from rats of different thyroid hormone status. Eur J Biochem 1988;178:511–8. https://doi.org/10.1111/j.1432-1033.1988.tb14477.x.Search in Google Scholar PubMed

27. Yehuda-Shnaidman, E, Kalderon, B, Azazmeh, N, Bar-Tana, J. Gating of the mitochondrial permeability transition pore by thyroid hormone. Faseb J 2010;24:93–104. https://doi.org/10.1096/fj.09-133538.Search in Google Scholar PubMed

28. Weitzel, JM, Iwen, KA. Coordination of mitochondrial biogenesis by thyroid hormone. Mol Cell Endocrinol 2011;342:1–7. https://doi.org/10.1016/j.mce.2011.05.009.Search in Google Scholar PubMed

29. Bassett, JH, Harvey, CB, Williams, GR. Mechanisms of thyroid hormone receptor-specific nuclear and extra nuclear actions. Mol Cell Endocrinol 2003;213:1–11. https://doi.org/10.1016/j.mce.2003.10.033.Search in Google Scholar PubMed

30. Gauthier, BR, Sola-García, A, Cáliz-Molina, MÁ, Lorenzo, PI, Cobo-Vuilleumier, N, Capilla-González, V, et al.. Thyroid hormones in diabetes, cancer, and aging. Aging Cell 2020;19:e13260. https://doi.org/10.1111/acel.13260 [Epub 2020 Oct 13].Search in Google Scholar PubMed PubMed Central

31. Cappola, AR, Ladenson, PW. Hypothyroidism and atherosclerosis. J Clin Endocrinol Metab 2003;88:2438–44. https://doi.org/10.1210/jc.2003-030398.Search in Google Scholar PubMed

32. Duntas, LH. Thyroid disease and lipids. Thyroid 2002;12:287–93. https://doi.org/10.1089/10507250252949405.Search in Google Scholar PubMed

33. Gao, N, Zhang, W, Zhang, YZ, Yang, Q, Chen, SH. Carotid intima-media thickness in patients with subclinical hypothyroid- ism: a meta-analysis. Atherosclerosis 2013;227:18–25. https://doi.org/10.1016/j.atherosclerosis.2012.10.070.Search in Google Scholar PubMed

34. Sawin, CT, Bigos, ST, Land, S, Bacharach, P. The aging thyroid. Relationship between elevated serum thyrotropin level and thyroid antibodies in elderly patients. Am J Med 1985;79:591–5. https://doi.org/10.1016/0002-9343(85)90056-7.Search in Google Scholar PubMed

35. Taylor, PN, Razvi, S, Pearce, SH, Dayan, CM. Clinical review: a review of the clinical consequences of variation in thyroid function within the reference range. J Clin Endocrinol Metab 2013;98:3562–71. https://doi.org/10.1210/jc.2013-1315.Search in Google Scholar PubMed

36. Wang, F, Tan, Y, Wang, C, Zhang, X, Zhao, Y, Song, X, et al.. Thyroid-stimulating hormone levels within the reference range are associated with serum lipid profiles independent of thyroid hormones. J Clin Endocrinol Metab 2012;97:2724–31. https://doi.org/10.1210/jc.2012-1133.Search in Google Scholar PubMed

37. Biondi, B, Palmieri, EA, Lombardi, G, Fazio, S. Effects of thyroid hormone on cardiac function: the relative importance of heart rate, loading conditions, and myocardial contractility in the regulation of cardiac performance in human hyperthyroidism. J Clin Endocrinol Metab 2002;87:968–74. https://doi.org/10.1210/jcem.87.3.8302.Search in Google Scholar PubMed

38. Riaz, K, Forker, AD, Isley, WL, Hamburg, MS, McCullough, PA. Hyperthyroidism: a “curable” cause of congestive heart failure–three case reports and a review of the literature. Congest Heart Fail 2003;9:40–6. https://doi.org/10.1111/j.1527-5299.2003.01124.x.Search in Google Scholar PubMed

39. Chen, J, Sun, M, Adeyemo, A, Pirie, F, Carstensen, T, Pomilla, C, et al.. Genome-wide association study of type 2 diabetes in Africa. Diabetologia 2019;62:1204–11. https://doi.org/10.1007/s00125-019-4880-7 [Epub 2019 May 2].Search in Google Scholar PubMed PubMed Central

40. Cavallo-Perin, P, Bruno, A, Boine, L, Cassader, M, Lenti, G, Pagano, G. Insulin resistance in Graves’ disease: a quantitative in-vivo evaluation. Eur J Clin Invest 1988;18:607–13. https://doi.org/10.1111/j.1365-2362.1988.tb01275.x.Search in Google Scholar PubMed

41. Waring, AC, Rodondi, N, Harrison, S, Kanaya, AM, Simonsick, EM, Miljkovic, I, et al.. Thyroid function and prevalent and incident metabolic syndrome in older adults: the health, ageing and body composition study. Clin Endocrinol 2012;76:911–8. https://doi.org/10.1111/j.1365-2265.2011.04328.x.Search in Google Scholar PubMed PubMed Central

42. Klieverik, LP, Sauerwein, HP, Ackermans, MT, Boelen, A, Kalsbeek, A, Fliers, E. Effects of thyrotoxicosis and selective hepatic autonomic denervation on hepatic glucose metabolism in rats. Am J Physiol Endocrinol Metab 2008;294:E513–20. https://doi.org/10.1152/ajpendo.00659.2007 [Epub 2008 Jan 8].Search in Google Scholar PubMed

43. Power, O, Hallihan, A, Jakeman, P. Human insulinotropic response to oral ingestion of native and hydrolysed whey protein. Amino Acids 2009;37:333–9. https://doi.org/10.1007/s00726-008-0156-0 [Epub 2008 Aug 5].Search in Google Scholar PubMed

44. Hatting, M, Tavares, CDJ, Sharabi, K, Rines, AK, Puigserver, P. Insulin regulation of gluconeogenesis. Ann N Y Acad Sci 2018;1411:21–35. https://doi.org/10.1111/nyas.13435 [Epub 2017 Sep 3].Search in Google Scholar PubMed PubMed Central

45. Hekimsoy, Z, Oktem, IK. Serum creatine kinase levels in overt and subclinical hypothyroidism. Endocr Res 2005;31:171–5. https://doi.org/10.1080/07435800500371706.Search in Google Scholar PubMed

46. Brennan, MD, Powell, C, Kaufman, KR, Sun, PC, Bahn, RS, Nair, KS. The impact of overt and subclinical hyperthyroidism on skeletal muscle. Thyroid 2006;16:375–80. https://doi.org/10.1089/thy.2006.16.375.Search in Google Scholar PubMed

47. Ledda-Columbano, GM, Perra, A, Loi, R, Shinozuka, H, Columbano, A. Cell proliferation induced by triiodothyronine in rat liver is associated with nodule regression and reduction of hepatocellular carcinomas. Cancer Res 2000;60:603–9.Search in Google Scholar

48. Hassan, MM, Kaseb, A, Li, D, Patt, YZ, Vauthey, JN, Thomas, MB, et al.. Association between hypothyroidism and hepatocellular carcinoma: a case-control study in the United States. Hepatology 2009;49:1563–70. https://doi.org/10.1002/hep.22793.Search in Google Scholar PubMed PubMed Central

49. Reddy, A, Dash, C, Leerapun, A, Mettler, TA, Stadheim, LM, Lazaridis, KN, et al.. Hypothyroidism: a possible risk factor for liver cancer in patients with no known underlying cause of liver disease. Clin Gastroenterol Hepatol 2007;5:118–23. https://doi.org/10.1016/j.cgh.2006.07.011.[Epub 2006 Sep 26].Search in Google Scholar PubMed

50. García-Silva, S, Aranda, A. The thyroid hormone receptor is a suppressor of ras-mediated transcription, proliferation, and transformation. Mol Cell Biol 2004;24:7514–23. https://doi.org/10.1128/MCB.24.17.7514-7523.2004.Search in Google Scholar PubMed PubMed Central

51. Nappi, A, Miro, C, Pezone, A, Tramontano, A, Di Cicco, E, Sagliocchi, S, et al.. Loss of p53 activates thyroid hormone via type 2 deiodinase and enhances DNA damage. Nat Commun 2023;14:1244. https://doi.org/10.1038/s41467-023-36755-y.Search in Google Scholar PubMed PubMed Central

52. Sagliocchi, S, Acampora, L, Cicatiello, AG. Deiodination and tumor progression: the interplay between thyroid hormones intracellular activation and the androgen signal. J Basic Clin Physiol Pharmacol 2023;34:551–3. https://doi.org/10.1515/jbcpp-2023-0155.Search in Google Scholar PubMed

53. Miro, C, Di Cicco, E, Ambrosio, R, Mancino, G, Di Girolamo, D, Cicatiello, AG, et al.. Thyroid hormone induces progression and invasiveness of squamous cell carcinomas by promoting a ZEB-1/E-cadherin switch. Nat Commun 2019;10:5410. Erratum in: Nat Commun. 2020 Jan 8;11(1):245. https://doi.org/10.1038/s41467-019-13140-2.Search in Google Scholar PubMed PubMed Central

54. Miro, C, Nappi, A, Cicatiello, AG, Di Cicco, E, Sagliocchi, S, Murolo, M, et al.. Thyroid hormone enhances angiogenesis and the Warburg effect in squamous cell carcinomas. Cancers 2021;13:2743. https://doi.org/10.3390/cancers13112743.Search in Google Scholar PubMed PubMed Central

55. Cicatiello, AG, Ambrosio, R, Dentice, M. Thyroid hormone promotes differentiation of colon cancer stem cells. Mol Cell Endocrinol 2017;459:84–9. https://doi.org/10.1016/j.mce.2017.03.017 [Epub 2017 Mar 22].Search in Google Scholar PubMed

56. Miro, C, Di Giovanni, A, Murolo, M, Cicatiello, AG, Nappi, A, Sagliocchi, S, et al.. Thyroid hormone and androgen signals mutually interplay and enhance inflammation and tumorigenic activation of tumor microenvironment in prostate cancer. Cancer Lett 2022;532:215581. https://doi.org/10.1016/j.canlet.2022.215581 [Epub 2022 Feb 5].Search in Google Scholar PubMed

57. Torabinejad, S, Miro, C, Barone, B, Imbimbo, C, Crocetto, F, Dentice, M. The androgen-thyroid hormone crosstalk in prostate cancer and the clinical implications. Eur Thyroid J 2023;12:e220228. https://doi.org/10.1530/ETJ-22-0228.Search in Google Scholar PubMed PubMed Central

58. Weitzel, JM, Iwen, KA, Seitz, HJ. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol 2003;88:121–8. https://doi.org/10.1113/eph8802506.Search in Google Scholar PubMed

59. Psarra, AM, Sekeris, CE. Steroid and thyroid hormone receptors in mitochondria. IUBMB Life 2008;60:210–23. https://doi.org/10.1002/iub.37.Search in Google Scholar PubMed

60. Vidali, S, Knuever, J, Lerchner, J, Giesen, M, Bíró, T, Klinger, M, et al.. Hypothalamic-pituitary-thyroid axis hormones stimulate mitochondrial function and biogenesis in human hair follicles. J Invest Dermatol 2014;134:33–42. https://doi.org/10.1038/jid.2013.286 [Epub 2013 Jun 27].Search in Google Scholar PubMed

61. Sagliocchi, S, Cicatiello, AG, Di Cicco, E, Ambrosio, R, Miro, C, Di Girolamo, D, et al.. The thyroid hormone activating enzyme, type 2 deiodinase, induces myogenic differentiation by regulating mitochondrial metabolism and reducing oxidative stress. Redox Biol 2019;24:101228. https://doi.org/10.1016/j.redox.2019.101228 [Epub 2019 May 22].Search in Google Scholar PubMed PubMed Central

62. Casas, F, Rochard, P, Rodier, A, Cassar-Malek, I, Marchal-Victorion, S, Wiesner, RJ, et al.. A variant form of the nuclear triiodothyronine receptor c-ErbAα1 plays a direct role in regulation of mitochondrial RNA synthesis. Mol Cell Biol 1999;19:7913–24. https://doi.org/10.1128/mcb.19.12.7913.Search in Google Scholar PubMed PubMed Central

63. Andersson, ML, Vennström, B. Chicken thyroid hormone receptor α requires the N-terminal amino acids for exclusive nuclear localization. FEBS Lett 1997;416:291–6. https://doi.org/10.1016/s0014-5793(97)01223-4.Search in Google Scholar PubMed

64. Wrutniak, C, Cassar-Malek, I, Marchal, S, Rascle, A, Heusser, S, Keller, JM, 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;270:16347–54. https://doi.org/10.1074/jbc.270.27.16347.Search in Google Scholar PubMed

65. Salvatore, D, Simonides, WS, Dentice, M, Zavacki, AM, Larsen, PR. Thyroid hormones and skeletal muscle–new insights and potential implications. Nat Rev Endocrinol 2014;10:206–14. https://doi.org/10.1038/nrendo.2013.238 [Epub 2013 Dec 10].Search in Google Scholar PubMed PubMed Central

66. Lombardi, A, Senese, R, De Matteis, R, Busiello, RA, Cioffi, F, Goglia, F, et al.. 3,5-Diiodo-L-thyronine activates brown adipose tissue thermogenesis in hypothyroid rats. PLoS One 2015;10:e0116498. https://doi.org/10.1371/journal.pone.0116498.Search in Google Scholar PubMed PubMed Central

67. Kalderon, B, Hermesh, O, Bar-Tana, J. Mitochondrial permeability transition is induced by in vivo thyroid hormone treatment. Endocrinology 1995;136:3552–6. https://doi.org/10.1210/endo.136.8.7628392.Search in Google Scholar PubMed

68. Simonides, WS, van Hardeveld, C. Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid 2008;18:205–16. https://doi.org/10.1089/thy.2007.0256.Search in Google Scholar PubMed

69. Dentice, M, Marsili, A, Ambrosio, R, Guardiola, O, Sibilio, A, Paik, JH, et al.. The FoxO3/type 2 deiodinase pathway is required for normal mouse myogenesis and muscle regeneration. J Clin Invest 2010;120:4021–30. https://doi.org/10.1172/JCI43670. [Epub 2010 Oct 11].Search in Google Scholar PubMed PubMed Central

70. Dentice, M, Ambrosio, R, Damiano, V, Sibilio, A, Luongo, C, Guardiola, O, et al.. Intracellular inactivation of thyroid hormone is a survival mechanism for muscle stem cell proliferation and lineage progression. Cell Metabol 2014;20:1038–48. https://doi.org/10.1016/j.cmet.2014.10.009.Search in Google Scholar PubMed PubMed Central

71. Dentice, M, Salvatore, D. Deiodinases: the balance of thyroid hormone: local impact of thyroid hormone inactivation. J Endocrinol 2011;209:273–82. https://doi.org/10.1530/JOE-11-0002.Search in Google Scholar PubMed

72. Cicatiello, AG, Sagliocchi, S, Nappi, A, Di Cicco, E, Miro, C, Murolo, M, et al.. Thyroid hormone regulates glutamine metabolism and anaplerotic fluxes by inducing mitochondrial glutamate aminotransferase GPT2. Cell Rep 2022;38:110409. Erratum in: Cell Rep. 2022 Mar 22;38(12):110562. https://doi.org/10.1016/j.celrep.2022.110409.Search in Google Scholar PubMed PubMed Central

73. Mishra, P, Varuzhanyan, G, Pham, AH, Chan, DC. Mitochondrial dynamics is a distinguishing feature of skeletal muscle fiber types and regulates organellar compartmentalization. Cell Metabol 2015;22:1033–44. https://doi.org/10.1016/j.cmet.2015.09.027 [Epub 2015 Oct 22].Search in Google Scholar PubMed PubMed Central

74. Pagel-Langenickel, I, Bao, J, Joseph, JJ, Schwartz, DR, Mantell, BS, Xu, X, et al.. PGC-1alpha integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J Biol Chem 2008;283:22464–72. https://doi.org/10.1074/jbc.M800842200 [Epub 2008 Jun 25].Search in Google Scholar PubMed PubMed Central

75. Bocco, BM, Louzada, RA, Silvestre, DH, Santos, MC, Anne-Palmer, E, Rangel, IF, et al.. Thyroid hormone activation by type 2 deiodinase mediates exercise-induced peroxisome proliferator-activated receptor-γ coactivator-1α expression in skeletal muscle. J Physiol 2016;594:5255–69. https://doi.org/10.1113/JP272440 [Epub 2016 Aug 18].Search in Google Scholar PubMed PubMed Central

76. Jäger, S, Handschin, C, St-Pierre, J, Spiegelman, BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 2007;104:12017–22. https://doi.org/10.1073/pnas.0705070104 [Epub 2007 Jul 3].Search in Google Scholar PubMed PubMed Central

77. Cantó, C, Gerhart-Hines, Z, Feige, JN, Lagouge, M, Noriega, L, Milne, JC, et al.. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009;458:1056–60. https://doi.org/10.1038/nature07813.Search in Google Scholar PubMed PubMed Central

78. Irrcher, I, Ljubicic, V, Kirwan, AF, Hood, DA. AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS One 2008;3:e3614. https://doi.org/10.1371/journal.pone.0003614 [Epub 2008 Oct 31].Search in Google Scholar PubMed PubMed Central

79. Branvold, DJ, Allred, DR, Beckstead, DJ, Kim, HJ, Fillmore, N, Condon, BM, et al.. Thyroid hormone effects on LKB1, MO25, phospho-AMPK, phospho-CREB, and PGC-1alpha in rat muscle. J Appl Physiol 2008;105:1218–27. https://doi.org/10.1152/japplphysiol.00997.2007 [Epub 2008 Jul 31].Search in Google Scholar PubMed

80. de Lange, P, Senese, R, Cioffi, F, Moreno, M, Lombardi, A, Silvestri, E, et al.. Rapid activation by 3,5,3’-L-triiodothyronine of adenosine 5’-monophosphate-activated protein kinase/acetyl-coenzyme a carboxylase and at/protein kinase B signaling pathways: relation to changes in fuel metabolism and myosin heavy-chain protein content in rat gastrocnemius muscle in vivo. Endocrinology 2008;149:6462–70. https://doi.org/10.1210/en.2008-0202 [Epub 2008 Aug 14].Search in Google Scholar PubMed

81. Barbe, P, Larrouy, D, Boulanger, C, Chevillotte, E, Viguerie, N, Thalamas, C, et al.. Triiodothyronine-mediated up-regulation of UCP2 and UCP3 mRNA expression in human skeletal muscle without coordinated induction of mitochondrial respiratory chain genes. Faseb J 2001;15:13–15. https://doi.org/10.1096/fj.00-0502fje [Epub 2000 Nov 9].Search in Google Scholar PubMed

82. de Lange, P, Lanni, A, Beneduce, L, Moreno, M, Lombardi, A, Silvestri, E, et al.. Uncoupling protein-3 is a molecular determinant for the regulation of resting metabolic rate by thyroid hormone. Endocrinology 2001;142:3414–20. https://doi.org/10.1210/endo.142.8.8303.Search in Google Scholar PubMed

83. Ramadan, W, Marsili, A, Larsen, PR, Zavacki, AM, Silva, JE. Type-2 iodothyronine 5’deiodinase (D2) in skeletal muscle of C57Bl/6 mice. II. Evidence for a role of D2 in the hypermetabolism of thyroid hormone receptor alpha-deficient mice. Endocrinology 2011;152:3093–102. https://doi.org/10.1210/en.2011-0139.Search in Google Scholar PubMed PubMed Central

84. Mizushima, N, Komatsu, M. Autophagy: renovation of cells and tissues. Cell 2011;147:728–41. https://doi.org/10.1016/j.cell.2011.10.026.Search in Google Scholar PubMed

85. Grumati, P, Coletto, L, Sabatelli, P, Cescon, M, Angelin, A, Bertaggia, E, et al.. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 2010;16:1313–20. https://doi.org/10.1038/nm.2247 [Epub 2010 Oct 31].Search in Google Scholar PubMed

86. Thapaliya, S, Runkana, A, McMullen, MR, Nagy, LE, McDonald, C, Naga Prasad, SV, et al.. Alcohol-induced autophagy contributes to loss in skeletal muscle mass. Autophagy 2014;10:677–90. https://doi.org/10.4161/auto.27918 [Epub 2014 Jan 31].Search in Google Scholar PubMed PubMed Central

87. Masiero, E, Sandri, M. Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles. Autophagy 2010;6:307–9. https://doi.org/10.4161/auto.6.2.11137 [Epub 2010 Feb 6].Search in Google Scholar PubMed

88. Lesmana, R, Sinha, RA, Singh, BK, Zhou, J, Ohba, K, Wu, Y, et al.. Thyroid hormone stimulation of autophagy is essential for mitochondrial biogenesis and activity in skeletal muscle. Endocrinology 2016;157:23–38. https://doi.org/10.1210/en.2015-1632 [Epub 2015 Nov 12].Search in Google Scholar PubMed

89. Lira, VA, Okutsu, M, Zhang, M, Greene, NP, Laker, RC, Breen, DS, et al.. Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. Faseb J 2013;27:4184–93. https://doi.org/10.1096/fj.13-228486 [Epub 2013 Jun 27].Search in Google Scholar PubMed PubMed Central

90. Lo Verso, F, Carnio, S, Vainshtein, A, Sandri, M. Autophagy is not required to sustain exercise and PRKAA1/AMPK activity but is important to prevent mitochondrial damage during physical activity. Autophagy 2014;10:1883–94. https://doi.org/10.4161/auto.32154 [Epub 2014 Oct 30].Search in Google Scholar PubMed PubMed Central

91. Malik, R, Hodgson, H. The relationship between the thyroid gland and the liver. QJM 2002;95:559–69. https://doi.org/10.1093/qjmed/95.9.559.Search in Google Scholar PubMed

92. Mullur, R, Liu, YY, Brent, GA. Thyroid hormone regulation of metabolism. Physiol Rev 2014;94:355–82. https://doi.org/10.1152/physrev.00030.2013.Search in Google Scholar PubMed PubMed Central

93. Sinha, RA, Singh, BK, Zhou, J, Wu, Y, Farah, BL, Ohba, K, et al.. Thyroid hormone induction of mitochondrial activity is coupled to mitophagy via ROS-AMPK-ULK1 signaling. Autophagy 2015;11:1341–57. https://doi.org/10.1080/15548627.2015.1061849.Search in Google Scholar PubMed PubMed Central

94. Singh, R, Kaushik, S, Wang, Y, Xiang, Y, Novak, I, Komatsu, M, et al.. Autophagy regulates lipid metabolism. Nature 2009;458:1131–5. https://doi.org/10.1038/nature07976 [Epub 2009 Apr 1].Search in Google Scholar PubMed PubMed Central

95. Cioffi, F, Senese, R, Lanni, A, Goglia, F. Thyroid hormones and mitochondria: with a brief look at derivatives and analogues. Mol Cell Endocrinol 2013;379:51–61. https://doi.org/10.1016/j.mce.2013.06.006 [Epub 2013 Jun 13].Search in Google Scholar PubMed

96. Sinha, RA, Singh, BK, Yen, PM. Thyroid hormone regulation of hepatic lipid and carbohydrate metabolism. Trends Endocrinol Metab 2014;25:538–45. https://doi.org/10.1016/j.tem.2014.07.001 [Epub 2014 Aug 12].Search in Google Scholar PubMed

97. Gracia-Sancho, J, Guixé-Muntet, S, Hide, D, Bosch, J. Modulation of autophagy for the treatment of liver diseases. Expert Opin Investig Drugs 2014;23:965–77. https://doi.org/10.1517/13543784.2014.912274 [Epub 2014 Apr 21].Search in Google Scholar PubMed

98. Townsend, SA, Newsome, PN. Non-alcoholic fatty liver disease in 2016. Br Med Bull 2016;119:143–56. https://doi.org/10.1093/bmb/ldw031 [Epub 2016 Aug 19].Search in Google Scholar PubMed PubMed Central

99. Sinha, RA, Yen, PM. Thyroid hormone-mediated autophagy and mitochondrial turnover in NAFLD. Cell Biosci 2016;6:46. https://doi.org/10.1186/s13578-016-0113-7.Search in Google Scholar PubMed PubMed Central

100. Liu, YY, Brent, GA. Thyroid hormone crosstalk with nuclear receptor signaling in metabolic regulation. Trends Endocrinol Metab 2010;21:166–73. https://doi.org/10.1016/j.tem.2009.11.004 [Epub 2009 Dec 16].Search in Google Scholar PubMed PubMed Central

101. Sinha, RA, You, SH, Zhou, J, Siddique, MM, Bay, BH, Zhu, X, et al.. Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. J Clin Invest 2012;122:2428–38. https://doi.org/10.1172/JCI60580 [Epub 2012 Jun 11].Search in Google Scholar PubMed PubMed Central

102. Coppola, M, Glinni, D, Moreno, M, Cioffi, F, Silvestri, E, Goglia, F. Thyroid hormone analogues and derivatives: actions in fatty liver. World J Hepatol 2014;6:114–29. https://doi.org/10.4254/wjh.v6.i3.114.Search in Google Scholar PubMed PubMed Central

103. Videla, LA. Energy metabolism, thyroid calorigenesis, and oxidative stress: functional and cytotoxic consequences. Redox Rep 2000;5:265–75. https://doi.org/10.1179/135100000101535807.Search in Google Scholar PubMed

104. Paget, GE, Thorp, JM. An effect of thyroxin on the fine structure of the rat liver cell. Nature 1963;199:1307–8. https://doi.org/10.1038/1991307a0.Search in Google Scholar PubMed

105. Vercesi, AE, Kowaltowski, AJ, Grijalba, MT, Meinicke, AR, Castilho, RF. The role of reactive oxygen species in mitochondrial permeability transition. Biosci Rep 1997;17:43–52. https://doi.org/10.1023/a:1027335217774.10.1023/A:1027335217774Search in Google Scholar

106. Skulachev, VP. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q Rev Biophys 1996;29:169–202. https://doi.org/10.1017/s0033583500005795.Search in Google Scholar PubMed

107. Goemann, IM, Romitti, M, Meyer, ELS, Wajner, SM, Maia, AL. Role of thyroid hormones in the neoplastic process: an overview. Endocr Relat Cancer 2017;24:R367–85. https://doi.org/10.1530/ERC-17-0192.Search in Google Scholar PubMed

108. Ciavardelli, D, Bellomo, M, Crescimanno, C, Vella, V. Type 3 deiodinase: role in cancer growth, stemness, and metabolism. Front Endocrinol 2014;5:215. https://doi.org/10.3389/fendo.2014.00215.Search in Google Scholar PubMed PubMed Central

109. Bernal, J. Thyroid hormone receptors in brain development and function. Nat Clin Pract Endocrinol Metab 2007;3:249–59. https://doi.org/10.1038/ncpendmet0424.Search in Google Scholar PubMed

110. Bauer, M, London, ED, Silverman, DH, Rasgon, N, Kirchheiner, J, Whybrow, PC. Thyroid, brain and mood modulation in affective disorder: insights from molecular research and functional brain imaging. Pharmacopsychiatry 2003;36:S215–21. https://doi.org/10.1055/s-2003-45133.Search in Google Scholar PubMed

111. Murolo, M, Di Vincenzo, O, Cicatiello, AG, Scalfi, L, Dentice, M. Cardiovascular and neuronal consequences of thyroid hormones alterations in the ischemic stroke. Metabolites 2022;13:22. https://doi.org/10.3390/metabo13010022.Search in Google Scholar PubMed PubMed Central

112. Hassan, W, Noreen, H, Rehman, S, Kamal, MA, da Rocha, JBT. Association of oxidative stress with neurological disorders. Curr Neuropharmacol 2022;20:1046–72. https://doi.org/10.2174/1570159X19666211111141246.Search in Google Scholar PubMed PubMed Central

113. Liu, Y-Y, Brent, GA. Thyroid hormone and the brain: mechanisms of action in development and role in protection and promotion of recovery after brain injury. Pharmacol Ther 2018;186:176–85. https://doi.org/10.1016/j.pharmthera.2018.01.007.Search in Google Scholar PubMed PubMed Central

114. Morita, M, Ikeshima-Kataoka, H, Kreft, M, Vardjan, N, Zorec, R, Noda, M. Metabolic plasticity of astrocytes and aging of the brain. Int J Mol Sci 2019;20:941. https://doi.org/10.3390/ijms20040941.Search in Google Scholar PubMed PubMed Central

Received: 2024-06-28
Accepted: 2024-07-06
Published Online: 2024-07-19

© 2024 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Editorials
  3. Targeting Rho GTPase regulators in cancer: are we hitting the mark?
  4. The pitfalls of linear regression in physiological research
  5. Reviews
  6. Lipid profile and mortality in patients with pulmonary thromboembolism; a systematic review and meta-analysis
  7. IcoSema: unveiling the future of diabetes management from a clinical pharmacology perspective
  8. Deucravacitinib: moderate-to-severe plaque psoriasis preventable?
  9. The key roles of thyroid hormone in mitochondrial regulation, at interface of human health and disease
  10. Uncovering the coronavirus outbreak: present understanding and future research paths
  11. Effects of thyroid hormones in skeletal muscle protein turnover
  12. Original Articles
  13. Effect of high-intensity interval training vs. moderate-intensity continuous training on cardiometabolic risk factors in overweight and obese individuals
  14. Alcohol promotes liver fibrosis in high fat diet induced diabetic rats
  15. Association between aerobic performance and physiological responses in Yo-Yo intermittent recovery test level 2, and the futsal-specific intermittent endurance test in trained futsal players
  16. Oral vs. injected: which vitamin D boost works best for low levels?
  17. Effects of an 8-week intervention of anulom vilom pranayama combined with heartfulness meditation on psychological stress, autonomic function, inflammatory biomarkers, and oxidative stress in healthcare workers during COVID-19 pandemic: a randomized controlled trial
  18. Ureteral access sheaths in RIRS: a retrospective, comparative, single-center study
https://doi.org/10.1515/jbcpp-2024-0108
Keywords for this article
thyroid hormone; metabolism; mitochondria

Articles in the same Issue

  1. Frontmatter
  2. Editorials
  3. Targeting Rho GTPase regulators in cancer: are we hitting the mark?
  4. The pitfalls of linear regression in physiological research
  5. Reviews
  6. Lipid profile and mortality in patients with pulmonary thromboembolism; a systematic review and meta-analysis
  7. IcoSema: unveiling the future of diabetes management from a clinical pharmacology perspective
  8. Deucravacitinib: moderate-to-severe plaque psoriasis preventable?
  9. The key roles of thyroid hormone in mitochondrial regulation, at interface of human health and disease
  10. Uncovering the coronavirus outbreak: present understanding and future research paths
  11. Effects of thyroid hormones in skeletal muscle protein turnover
  12. Original Articles
  13. Effect of high-intensity interval training vs. moderate-intensity continuous training on cardiometabolic risk factors in overweight and obese individuals
  14. Alcohol promotes liver fibrosis in high fat diet induced diabetic rats
  15. Association between aerobic performance and physiological responses in Yo-Yo intermittent recovery test level 2, and the futsal-specific intermittent endurance test in trained futsal players
  16. Oral vs. injected: which vitamin D boost works best for low levels?
  17. Effects of an 8-week intervention of anulom vilom pranayama combined with heartfulness meditation on psychological stress, autonomic function, inflammatory biomarkers, and oxidative stress in healthcare workers during COVID-19 pandemic: a randomized controlled trial
  18. Ureteral access sheaths in RIRS: a retrospective, comparative, single-center study
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 3.11.2025 from https://www.degruyterbrill.com/document/doi/10.1515/jbcpp-2024-0108/pdf
Scroll to top button