Thyroid hormones and skeletal muscle—new insights and potential implications (original) (raw)
Simonides, W. S. & van Hardeveld, C. Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid18, 205–216 (2008). CASPubMed Google Scholar
Schiaffino, S. & Reggiani, C. Fiber types in mammalian skeletal muscles. Physiol. Rev.91, 1447–1531 (2011). CASPubMed Google Scholar
Murphy, R. M., Larkins, N. T., Mollica, J. P., Beard, N. A. & Lamb, G. D. Calsequestrin content and SERCA determine normal and maximal Ca2+ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. J. Physiol.587, 443–460 (2009). CASPubMed Google Scholar
Novák, P. & Soukup, T. Calsequestrin distribution, structure and function, its role in normal and pathological situations and the effect of thyroid hormones. Physiol. Res.60, 439–452 (2011). PubMed Google Scholar
Bianco, A. C., Salvatore, D., Gereben, B., Berry, M. J. & Larsen, P. R. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev.23, 38–89 (2002). CASPubMed Google Scholar
Gereben, B. et al. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr. Rev.29, 898–938 (2008). CASPubMedPubMed Central Google Scholar
Croteau, W., Davey, J. C., Galton, V. A. & St Germain, D. L. Cloning of the mammalian type II iodothyronine deiodinase. A selenoprotein differentially expressed and regulated in human and rat brain and other tissues. J. Clin. Invest.98, 405–417 (1996). CASPubMedPubMed Central Google Scholar
Salvatore, D., Bartha, T., Harney, J. W. & Larsen, P. R. Molecular biological and biochemical characterization of the human type 2 selenodeiodinase. Endocrinology137, 3308–3315 (1996). CASPubMed Google Scholar
Peeters, R. P. et al. Reduced activation and increased inactivation of thyroid hormone in tissues of critically ill patients. J. Clin. Endocrinol. Metab.88, 3202–3211 (2003). CASPubMed Google Scholar
Brack, A. S. & Rando, T. A. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell10, 504–514 (2012). CASPubMedPubMed Central Google Scholar
Yin, H., Price, F. & Rudnicki, M. A. Satellite cells and the muscle stem cell niche. Physiol. Rev.93, 23–67 (2013). CASPubMedPubMed Central Google Scholar
Relaix, F. & Zammit, P. S. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development139, 2845–2856 (2012). CASPubMed Google Scholar
Yu, F. et al. Effects of thyroid hormone receptor gene disruption on myosin isoform expression in mouse skeletal muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol.278, R1545–R1554 (2000). CASPubMed Google Scholar
Mebis, L. et al. Expression of thyroid hormone transporters during critical illness. Eur. J. Endocrinol.161, 243–250 (2009). CASPubMed Google Scholar
Friesema, E. C. et al. Effective cellular uptake and efflux of thyroid hormone by human monocarboxylate transporter 10. Mol. Endocrinol.22, 1357–1369 (2008). CASPubMedPubMed Central Google Scholar
Marsili, A. et al. Type 2 iodothyronine deiodinase levels are higher in slow-twitch than fast-twitch mouse skeletal muscle and are increased in hypothyroidism. Endocrinology151, 5952–5960 (2010). CASPubMedPubMed Central Google Scholar
Marsili, A. et al. Type II iodothyronine deiodinase provides intracellular 3,5,3′-triiodothyronine to normal and regenerating mouse skeletal muscle. Am. J. Physiol. Endocrinol. Metab.301, E818–E824 (2011). CASPubMedPubMed Central Google Scholar
Dentice, M. et al. The FoxO3/type 2 deiodinase pathway is required for normal mouse myogenesis and muscle regeneration. J. Clin. Invest.120, 4021–4030 (2010). CASPubMedPubMed Central Google Scholar
Hosoi, Y. et al. Expression and regulation of type II iodothyronine deiodinase in cultured human skeletal muscle cells. J. Clin. Endocrinol. Metab.84, 3293–3300 (1999). CASPubMed Google Scholar
Maia, A. L., Kim, B. W., Huang, S. A., Harney, J. W. & Larsen, P. R. Type 2 iodothyronine deiodinase is the major source of plasma T3 in euthyroid humans. J. Clin. Invest.115, 2524–2533 (2005). CASPubMedPubMed Central Google Scholar
Grozovsky, R. et al. Type 2 deiodinase expression is induced by peroxisomal proliferator-activated receptor-gamma agonists in skeletal myocytes. Endocrinology150, 1976–1983 (2009). CASPubMed Google Scholar
Mebis, L., Langouche, L., Visser, T. J. & Van den Berghe, G. The type II iodothyronine deiodinase is up-regulated in skeletal muscle during prolonged critical illness. J. Clin. Endocrinol. Metab.92, 3330–3333 (2007). CASPubMed Google Scholar
Heemstra, K. A. et al. Type 2 iodothyronine deiodinase in skeletal muscle: effects of hypothyroidism and fasting. J. Clin. Endocrinol. Metab.94, 2144–2150 (2009). CASPubMed Google Scholar
Steinsapir, J., Harney, J. & Larsen, P. R. Type 2 iodothyronine deiodinase in rat pituitary tumor cells is inactivated in proteasomes. J. Clin. Invest.102, 1895–1899 (1998). CASPubMedPubMed Central Google Scholar
Mills, I., Barge, R. M., Silva, J. E. & Larsen, P. R. Insulin stimulation of iodothyronine 5′-deiodinase in rat brown adipocytes. Biochem. Biophys. Res. Commun.143, 81–86 (1987). CASPubMed Google Scholar
Silva, J. E. & Larsen, P. R. Hormonal regulation of iodothyronine 5′-deiodinase in rat brown adipose tissue. Am. J. Physiol.251, E639–E643 (1986). CASPubMed Google Scholar
Boelen, A., Kwakkel, J., Wiersinga, W. M. & Fliers, E. Chronic local inflammation in mice results in decreased TRH and type 3 deiodinase mRNA expression in the hypothalamic paraventricular nucleus independently of diminished food intake. J. Endocrinol.191, 707–714 (2006). CASPubMed Google Scholar
Peeters, R. P. et al. Serum 3,3′,5′-triiodothyronine (rT3) and 3,5,3′-triiodothyronine/rT3 are prognostic markers in critically ill patients and are associated with postmortem tissue deiodinase activities. J. Clin. Endocrinol. Metab.90, 4559–4565 (2005). CASPubMed Google Scholar
Yen, P. M. Physiological and molecular basis of thyroid hormone action. Physiol. Rev.81, 1097–1142 (2001). CASPubMed Google Scholar
Simonides, W. S. et al. Characterization of the promoter of the rat sarcoplasmic endoplasmic reticulum Ca2+-ATPase 1 gene and analysis of thyroid hormone responsiveness. J. Biol. Chem.271, 32048–32056 (1996). CASPubMed Google Scholar
Hartong, R. et al. Delineation of three different thyroid hormone-response elements in promoter of rat sarcoplasmic reticulum Ca2+ATPase gene. Demonstration that retinoid X receptor binds 5′ to thyroid hormone receptor in response element 1. J. Biol. Chem.269, 13021–13029 (1994). CASPubMed Google Scholar
Solanes, G. et al. Thyroid hormones directly activate the expression of the human and mouse uncoupling protein-3 genes through a thyroid response element in the proximal promoter region. Biochem. J.386, 505–513 (2005). CASPubMedPubMed Central Google Scholar
Zorzano, A., Palacin, M. & Guma, A. Mechanisms regulating GLUT4 glucose transporter expression and glucose transport in skeletal muscle. Acta Physiol. Scand.183, 43–58 (2005). CASPubMed Google Scholar
Desvergne, B., Petty, K. J. & Nikodem, V. M. Functional characterization and receptor binding studies of the malic enzyme thyroid hormone response element. J. Biol. Chem.266, 1008–1013 (1991). CASPubMed Google Scholar
Dümmler, K., Müller, S. & Seitz, H. J. Regulation of adenine nucleotide translocase and glycerol 3-phosphate dehydrogenase expression by thyroid hormones in different rat tissues. Biochem. J.317 (Pt 3), 913–918 (1996). PubMedPubMed Central Google Scholar
Morkin, E. Control of cardiac myosin heavy chain gene expression. Microsc. Res. Tech.50, 522–531 (2000). CASPubMed Google Scholar
Muscat, G. E., Mynett-Johnson, L., Dowhan, D., Downes, M. & Griggs, R. Activation of myoD gene transcription by 3,5,3′-triiodo-L-thyronine: a direct role for the thyroid hormone and retinoid X receptors. Nucleic Acids Res.22, 583–591 (1994). CASPubMedPubMed Central Google Scholar
Downes, M., Griggs, R., Atkins, A., Olson, E. N. & Muscat, G. E. Identification of a thyroid hormone response element in the mouse myogenin gene: characterization of the thyroid hormone and retinoid X receptor heterodimeric binding site. Cell Growth Differ.4, 901–909 (1993). CASPubMed Google Scholar
Muller, A., Thelen, M. H., Zuidwijk, M. J., Simonides, W. S. & van Hardeveld, C. Expression of MyoD in cultured primary myotubes is dependent on contractile activity: correlation with phenotype-specific expression of a sarcoplasmic reticulum Ca2+-ATPase isoform. Biochem. Biophys. Res. Commun.229, 198–204 (1996). CASPubMed Google Scholar
Kraus, B. & Pette, D. Quantification of MyoD, myogenin, MRF4 and Id-1 by reverse-transcriptase polymerase chain reaction in rat muscles—effects of hypothyroidism and chronic low-frequency stimulation. Eur. J. Biochem.247, 98–106 (1997). CASPubMed Google Scholar
Wheeler, M. T., Snyder, E. C., Patterson, M. N. & Swoap, S. J. An E-box within the MHC IIB gene is bound by MyoD and is required for gene expression in fast muscle. Am. J. Physiol.276, C1069–C1078 (1999). CASPubMed Google Scholar
Allen, D. L., Sartorius, C. A., Sycuro, L. K. & Leinwand, L. A. Different pathways regulate expression of the skeletal myosin heavy chain genes. J. Biol. Chem.276, 43524–43533 (2001). CASPubMed Google Scholar
Weitzel, J. M., Iwen, K. A. & Seitz, H. J. Regulation of mitochondrial biogenesis by thyroid hormone. Exp. Physiol.88, 121–128 (2003). CASPubMed Google Scholar
Irrcher, I., Adhihetty, P. J., Joseph, A. M., Ljubicic, V. & Hood, D. A. Regulation of mitochondrial biogenesis in muscle by endurance exercise. Sports Med.33, 783–793 (2003). PubMed Google Scholar
Psarra, A. M., Solakidi, S. & Sekeris, C. E. The mitochondrion as a primary site of action of steroid and thyroid hormones: presence and action of steroid and thyroid hormone receptors in mitochondria of animal cells. Mol. Cell Endocrinol.246, 21–33 (2006). CASPubMed Google Scholar
Muscat, G. E., Downes, M. & Dowhan, D. H. Regulation of vertebrate muscle differentiation by thyroid hormone: the role of the myoD gene family. Bioessays17, 211–218 (1995). CASPubMed Google Scholar
White, R. B., Bierinx, A. S., Gnocchi, V. F. & Zammit, P. S. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev. Biol.10, 21 (2010). PubMedPubMed Central Google Scholar
Braverman, L. E. & Cooper, D. S. Werner & Ingbar's The Thyroid: A Fundamental and Clinical Text, 10th edn (Lippincott, Williams & Wilkins, Philadelphia, 2012). Google Scholar
de Lange, P. et al. Uncoupling protein-3 is a molecular determinant for the regulation of resting metabolic rate by thyroid hormone. Endocrinology142, 3414–3420 (2001). CASPubMed Google Scholar
Silva, J. E. Thermogenic mechanisms and their hormonal regulation. Physiol. Rev.86, 435–464 (2006). CASPubMed Google Scholar
Visser, W. E. et al. Physiological thyroid hormone levels regulate numerous skeletal muscle transcripts. J. Clin. Endocrinol. Metab.94, 3487–3496 (2009). CASPubMed Google Scholar
Clement, K. et al. In vivo regulation of human skeletal muscle gene expression by thyroid hormone. Genome Res.12, 281–291 (2002). CASPubMedPubMed Central Google Scholar
Lebon, V. et al. Effect of triiodothyronine on mitochondrial energy coupling in human skeletal muscle. J. Clin. Invest.108, 733–737 (2001). CASPubMedPubMed Central Google Scholar
Mitchell, C. S. et al. Resistance to thyroid hormone is associated with raised energy expenditure, muscle mitochondrial uncoupling, and hyperphagia. J. Clin. Invest.120, 1345–1354 (2010). CASPubMedPubMed Central Google Scholar
Johannsen, D. L. et al. Effect of short-term thyroxine administration on energy metabolism and mitochondrial efficiency in humans. PLoS ONE7, e40837 (2012). CASPubMedPubMed Central Google Scholar
Queiroz, M. S., Shao, Y. & Ismail-Beigi, F. Effect of thyroid hormone on uncoupling protein-3 mRNA expression in rat heart and skeletal muscle. Thyroid14, 177–185 (2004). PubMed Google Scholar
Ramadan, W., Marsili, A., Larsen, P. R., Zavacki, A. M. & Silva, J. E. 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. Endocrinology152, 3093–102 (2011). CASPubMedPubMed Central Google Scholar
van Marken Lichtenbelt, W. D. et al. Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med.360, 1500–1508 (2009). CASPubMed Google Scholar
Cypess, A. M. et al. Cold but not sympathomimetics activates human brown adipose tissue in vivo. Proc. Natl Acad. Sci. USA109, 10001–10005 (2012). CASPubMedPubMed Central Google Scholar
van der Lans, A. A. et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J. Clin. Invest.123, 3395–3403 (2013). CASPubMedPubMed Central Google Scholar
Wu, J. et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell150, 366–376 (2012). CASPubMedPubMed Central Google Scholar
Boström, P. et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature481, 463–468 (2012). PubMedPubMed Central Google Scholar
Chidakel, A., Mentuccia, D. & Celi, F. S. Peripheral metabolism of thyroid hormone and glucose homeostasis. Thyroid15, 899–903 (2005). CASPubMed Google Scholar
Klieverik, L. P. et al. Thyroid hormone effects on whole-body energy homeostasis and tissue-specific fatty acid uptake in vivo. Endocrinology150, 5639–5648 (2009). CASPubMed Google Scholar
Harrison, S. A., Buxton, J. M., Clancy, B. M. & Czech, M. P. Insulin regulation of hexose transport in mouse 3T3-L1 cells expressing the human HepG2 glucose transporter. J. Biol. Chem.265, 20106–20116 (1990). CASPubMed Google Scholar
Marsili, A. et al. Mice with a targeted deletion of the type 2 deiodinase are insulin resistant and susceptible to diet induced obesity. PLoS ONE6, e20832 (2011). CASPubMedPubMed Central Google Scholar
Mentuccia, D. et al. Association between a novel variant of the human type 2 deiodinase gene Thr92Ala and insulin resistance: evidence of interaction with the Trp64Arg variant of the β-3-adrenergic receptor. Diabetes51, 880–883 (2002). CASPubMed Google Scholar
Canani, L. H. et al. The type 2 deiodinase A/G. (Thr92Ala) polymorphism is associated with decreased enzyme velocity and increased insulin resistance in patients with type 2 diabetes mellitus. J. Clin. Endocrinol. Metab.90, 3472–3478 (2005). CASPubMed Google Scholar
Meulenbelt, I. et al. Identification of DIO2 as a new susceptibility locus for symptomatic osteoarthritis. Hum. Mol. Genet.17, 1867–1875 (2008). CASPubMed Google Scholar
Heemstra, K. A. et al. Thr92Ala polymorphism in the type 2 deiodinase is not associated with T4 dose in athyroid patients or patients with Hashimoto thyroiditis. Clin. Endocrinol. (Oxf.)71, 279–283 (2009). CAS Google Scholar
Charge, S. B. & Rudnicki, M. A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev.84, 209–238 (2004). CASPubMed Google Scholar
Schultz, E. & McCormick, K. M. Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol.123, 213–257 (1994). CASPubMed Google Scholar
Yablonka-Reuveni, Z. Development and postnatal regulation of adult myoblasts. Microsc. Res. Tech.30, 366–380 (1995). CASPubMedPubMed Central Google Scholar
Olson, E. N. Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol.154, 261–272 (1992). CASPubMed Google Scholar
Rudnicki, M. A. & Jaenisch, R. The MyoD family of transcription factors and skeletal myogenesis. Bioessays17, 203–209 (1995). CASPubMed Google Scholar
Brunet, A. et al. Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell96, 857–868 (1999). CASPubMed Google Scholar
Bois, P. R., Brochard, V. F., Salin-Cantegrel, A. V., Cleveland, J. L. & Grosveld, G. C. FoxO1a-cyclic GMP-dependent kinase I interactions orchestrate myoblast fusion. Mol. Cell Biol.25, 7645–7656 (2005). CASPubMedPubMed Central Google Scholar
Gross, D. N., van den Heuvel, A. P. & Birnbaum, M. J. The role of FoxO in the regulation of metabolism. Oncogene27, 2320–2336 (2008). CASPubMed Google Scholar
Mammucari, C., Schiaffino, S. & Sandri, M. Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy4, 524–526 (2008). CASPubMed Google Scholar
Zhao, J. et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab.6, 472–483 (2007). CASPubMed Google Scholar
Hu, P., Geles, K. G., Paik, J. H., DePinho, R. A. & Tjian, R. Codependent activators direct myoblast-specific MyoD transcription. Dev. Cell15, 534–546 (2008). CASPubMedPubMed Central Google Scholar
Dentice, M. et al. Type 3 deiodinase is highly expressed in proliferating myoblasts and during the early phase of muscle regeneration. Presented at the 35th Annual Meeting of the European Thyroid Association (Krakow, Poland, 2011).
Koenig, M., Monaco, A. P. & Kunkel, L. M. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell53, 219–228 (1988). CASPubMed Google Scholar
Partridge, T. Pathophysiology of muscular dystrophy. Br. J. Hosp. Med.49, 26–36 (1993). CASPubMed Google Scholar
England, S. B. et al. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature343, 180–182 (1990). CASPubMed Google Scholar
Anderson, J. E., Liu, L. & Kardami, E. The effects of hyperthyroidism on muscular dystrophy in the mdx mouse: greater dystrophy in cardiac and soleus muscle. Muscle Nerve17, 64–73 (1994). CASPubMed Google Scholar
McIntosh, L. M. & Anderson, J. E. Hypothyroidism prolongs and increases mdx muscle precursor proliferation and delays myotube formation in normal and dystrophic limb muscle. Biochem. Cell Biol.73, 181–190 (1995). CASPubMed Google Scholar
Pernitsky, A. N., McIntosh, L. M. & Anderson, J. E. Hyperthyroidism impairs early repair in normal but not dystrophic mdx mouse tibialis anterior muscle. An in vivo study. Biochem. Cell Biol.74, 315–324 (1996). CASPubMed Google Scholar