Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-20T16:16:34.261Z Has data issue: false hasContentIssue false

Role of thyroid hormones in early postnatal development of skeletal muscle and its implications for undernutrition

Published online by Cambridge University Press:  09 March 2007

A. P. Harrison
Affiliation:
Department of Cellular Physiology, The Babraham Institute, CambridgeCB2 4AT
D. R. Tivey
Affiliation:
Department of Cellular Physiology, The Babraham Institute, CambridgeCB2 4AT
T. Clausen
Affiliation:
Department of Physiology, University of Aarhus, DK-8OOO Ärhus C, Denmark
C. Duchamp
Affiliation:
Department of Cellular Physiology, The Babraham Institute, CambridgeCB2 4AT
M. J. Dauncey
Affiliation:
Department of Cellular Physiology, The Babraham Institute, CambridgeCB2 4AT
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Energy intake profoundly influences many endocrine axes which in turn play a central role in development. The specific influence of a short period of mild hypothyroidism, similar to that induced by undernutrition, in regulating muscle development has been assessed in a large mammal during early postnatal life. Hypothyroidism was induced by providing methimazole and iopanoic acid in the feed of piglets between 4 and 14 d of age, and controls were pair-fed to the energy intake of their hypothyroid littermates. Thyroid status was evaluated, and myofibre differentiation and cation pump concentrations were then assessed in the following functionally distinct muscles: longissimus dorsi (l. dorsi), soleus and rhomboideus. Reductions in plasma concentrations of thyroxine (T4; 32%, P < O·Ol), triiodothyronine (T3;48%, P < 0·001), free T3, (58%, P < 0·001)and hepatic 5'-monodeiodinase (EC 1.11.1.8) activity (74%, P < 0·001) occurred with treatment. Small, although significant, increases in the proportion of type I slow-twitch oxidative fibres occurred with mild hypothyroidism, in l. dorsi (2%, P < 0·01) and soleus(7%, P < 0·01). Nuclear T3-receptor concentration in l. dorsi of hypothyroid animals compared with controls increased by 46% (P < 0·001), a response that may represent a homeostatic mechanism making muscle more sensitive to low levels of circulating thyroid hormones. Nevertheless, Na+, K+-ATPase (EC 3.6.1.37) concentration was reduced by 15–16% in all muscles (l.dorsi P< 0·05,soleusP < 0·001, rhomboideusP < 0·05), and Ca2+-ATPase (EC 3.6.1.38) concentration was significantly reduced in the two slow-twitch muscles: by 22% in rhomboideus (P < 0·001) and 23% in soleus (P < 0·05). It is concluded that during early postnatal development of large mammals a period of mild hypothyroidism, comparable with that found during undernutrition, induces changes in myofibre differentiation and a down-regulation of cation pumps in skeletal muscle. Such changes would result in slowness of movement and muscle weakness, and also reduce ATP hydrolysis with a concomitant improvement in energetic efficiency.

Type
General Nutrition
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Acheson, K. J. & Burger, A. G. (1980). A study of the relationship between thermogenesis and thyroid hormones. Journal of Clinical Endocrinology and Metabolism 51, 8489.CrossRefGoogle ScholarPubMed
Arai, M., Otsu, K., MacLennan, D. H., Alpert, N. R. & Periasamy, M. (1991). Effect of thyroid hormone on the expression of mRNA encoding sarcoplasmic reticulum proteins. Circulation Research 69, 266276.CrossRefGoogle ScholarPubMed
Brodie, C. & Sampson, S. R. (1989). Characterization of thyroid hormone effects on Na channel synthesis in cultured skeletal myotubes: role of Ca2+. Endocrinology 125, 842849.CrossRefGoogle ScholarPubMed
Brooke, M. H. & Kaiser, K. K. (1970). Three ‘myosin adenosine triphosphatase’ systems: The nature of their pH lability and sulfhydryl dependence. Journal of Histochemistry and Cytochemistry 18, 670672.CrossRefGoogle ScholarPubMed
Clausen, T., Everts, M. E. & Kjeldsen, K. (1987). Quantification of the maximum capacity for active sodium potassium transport in art skeletal muscic. Journal of Physiology 388, 163181.CrossRefGoogle Scholar
Clausen, R., van Hardeveld, C. & Everts, M. E. (1991). Significance of cation transport in control of energy metabolism and thermogenesis, Physiological Reviews 3, 733774.CrossRefGoogle Scholar
d'Albis, A. & Butler-Browne, G. (1993). The hormonal control of myosin isoform expression in skeletal muscle of mammals: a review. Basic and Applied Myology 3, 716.Google Scholar
Dauncey, M. J. (1990). Thyroid hormones and thermogenesis. Proceedings of the Nutrition Society 49, 203215.CrossRefGoogle ScholarPubMed
Dauncey, M. J., Brown, D., Hayashi, M. & Ingram, D. L. (1988). Thyroid hormone nuclear receptors in skeletal muscle as influenced by environmental temperature and energy intake. Quarterly Journal of Experimental Physiology 73, 183191.CrossRefGoogle ScholarPubMed
Dauncey, M. J. & Burton, K. A. (1989). 3H-Ouabain binding sites in porcine skeletal muscle as influenced by environmental temperature and energy intake. Pfiügers Archiv: European Journal of Physiology 414, 317323.CrossRefGoogle ScholarPubMed
Dauncey, M. J., Burton, K. A. & Morovat, A. (1991). Variations in [3H]ouabain binding of porcine skeletal muscle associated with feeding. Experimental Physiology 76, 967970.CrossRefGoogle ScholarPubMed
Dauncey, M. J., Clausen, T. & Harrison, A. P. (1994). Developmental regulation of Na+, K+- and Ca2+-ATPases in muscle. In Modern Trends in BioThermoKinetics, vol. 3, pp. 163168 [Gnaiger, E., Gellerich, F. N. and Wyss, M. editors]. Innsbruck: Innsbruck University Press.Google Scholar
Dauncey, M. J. & Gilmour, R. S. (1996). Regulatory factors in the control of muscle development. Proceedings of the Nutrition Society 55, 543559.CrossRefGoogle ScholarPubMed
Dauncey, M. J. & Harrison, A. P. (1996). Developmental regulation of cation pumps in skeletal and cardiac muscle. Acta Physiologica Scandinavica 156, 313323.CrossRefGoogle ScholarPubMed
Dauncey, M. J. & Ingram, D. L. (1988). Influence of environmental temperature and energy intake on skeletal musle respiratory enzymes and morphology. European Journal of Applied Physiology 58, 239244.CrossRefGoogle Scholar
Dauncey, M. J. & Morovat, A. (1993). Investigation of mechanisms mediating the increase in plasma concentrations of thyroid hormones after a meal in young growing pigs. Journal of Endocrinology 139, 131141.CrossRefGoogle ScholarPubMed
Dørup, I. (1996). Effects of K+, Mg2+ deficiency and adrenal steroids on Na+-K+ pump concentration in skeletal muscle. Acta Physiologica Scandinavica 156, 305311.CrossRefGoogle ScholarPubMed
Duchamp, C., Burton, K. A., Herpin, P. & Dauncey, M. J. (1994). Perinatal ontogeny of porcine nuclear 3,5,3'-triiodothyronine receptors and its modification by thyroid status. American Journal of Physiology 267, 687693.Google Scholar
Everts, M. E., Andersen, J. P., Clausen, T. & Hansen, O. (1989). Quantitative detemination of Ca2+-dependent Mg2+-ATPase from sarcoplasmic reticulum in muscle biopsies. Biochemical Journal 260, 443448.CrossRefGoogle Scholar
Gold, H. K., Spann, J. F. & Braunwald, E. (1970). Effect of alterations in the thyroid state on the intrinsic contractile properties of isolated rat skeletal muscle. Journal of Clinical Investigation 49, 849854.CrossRefGoogle ScholarPubMed
Harrison, A. P., Clausen, T. & Dauncey, M. J. (1994 a). Cation pumps in skeletal muscle undergo dramatic up-regulation in the perinatal period. Proceedings of the Nutrition Society 53, 246A.Google Scholar
Harrison, A. P., Clausen, T., Duchamp, C. & Dauncey, M. J. (1994 b). Roles of skeletal muscle morphology and activity in determining Na+, K+-ATPase concentration in young pigs. American Journal of Physiology 35, R102R111.Google Scholar
Harrison, A. P., Clausen, T., Tivey, D. R. & Dauncey, M. J. (1994 c). Regulation of Na+, K+-ATPase concentration in skeletal muscle of neonatal pigs: role of thyroid hormones. Journal of Endocrinology 140, P65.Google Scholar
Harrison, A. P., Rowlerson, A. M. & Dauncey, M. J. (1996). Selective regulation of myofiber differentiation by energy status during postnatal development. American Journal of Physiology 270, R667R674.Google ScholarPubMed
Harrison, A. P., Tivey, D. R., Duchamp, C. & Dauncey, M. J. (1993). Neonatal hypothyroidism and its influence on contractile and metabolic properties of skeletal muscle. Journal of Endocrinology 139, P49.Google Scholar
Hegyvary, C. (1977). Effect of aldosterone and methylprednisolone on cardiac NaK-ATPase. Experientia 33, 12801281.CrossRefGoogle ScholarPubMed
Hoffman, R. K., Lazar, M. A., Rubinstein, N. A. & Kelly, A. M. (1994). Differential expression of αl, α2 and β1 thyroid hormone receptor genes in developing rat skeletal muscle. Journal of Cell Biochemistry 18D, 517.Google Scholar
Izumo, S., Nadal-Ginard, B. & Mahdavi, V. (1986). All members of the MHC multigene family respond to thyroid hormone in a highly tissue-specific manner. Science 231, 597600.CrossRefGoogle Scholar
Kiss, E., Jakab, G., Kranias, E. G. & Edes, I. (1994). Thyroid hormone-induced alterations in phospholamban protein expression. Regulatory effects on sarcoplasmic reticulum Ca2+ transport and myocardial relaxation. Circulation Research 75, 245251.CrossRefGoogle ScholarPubMed
Kjeldsen, K., Everts, M. E. & Clausen, T. (1986 a). The effects of thyroid hormones on 2H-ouabain binding site concentration, Na, K-contents and 86Rb-efflux in rat skeletal muscle. Pflügers Archiv: European Journal of Physiology 46, 529535.CrossRefGoogle Scholar
Kjeldsen, K., Everts, M. E. & Clausen, T. (1986 b). Effects of semi-starvation and potassium deficiency on the concentration of [3H]ouabain-binding sites and sodium and potassium contents in rat skeletal muscle. British Journal of Nutrition 56, 519532.CrossRefGoogle ScholarPubMed
Kühn, E. R., Verheyen, G., Chiasson, R. B., Huts, C., Huybrechts, L., Van den Steen, P. & Decuypere, E. (1987). Growth hormone stimulates the peripheral conversion of thyroxine into triiodothyronine by increasing the liver 5'-monodeiodinase activity in the fasted and normal fed chicken. Hormone andMetabolic Research 19, 304308.CrossRefGoogle ScholarPubMed
Lawes Agricultural Trust (1987). Genstat 5. Rothamsted, Herts.: Lawes Agricultural Trust.Google Scholar
Lazar, M. A. (1993). Thyroid hormone receptors: Multiple forms, multiple possibilities. Endocrine Reviews 14, 184193.Google ScholarPubMed
McAllister, R. M., Ogilvie, R. W. & Terjung, R. L. (1991). Functional and metabolic consequences of skeletal muscle remodeling in hypothyroidism. American Journal of Physiology 260, E272E279.Google ScholarPubMed
Matsumura, M., Kuzuya, N., Kawakami, Y. & Yamashita, K. (1992). Effects of fasting, refeeding, and fasting with T2 administration on Na-K, ATPase in rat skeletal muscle. Metabolism 41, 991999.CrossRefGoogle Scholar
Mickleson, J. R., Beaudry, T. M. & Louis, C. F. (1985). Regulation of skeletal muscle sarcoplasmic ATP-dependent calcium transport by calmodulin and cAMP-dependent protein kinase. Archives of Biochemistry and Biophysics 242, 127136.CrossRefGoogle Scholar
Montgomery, A. (1992). The time course of thyroid-hormone-induced changes in the isotonic and isometric properties of rat soleus muscle. Pfiügers Archiv: European Journal of Physiology 421, 350356.CrossRefGoogle ScholarPubMed
Morovat, A. & Dauncey, M. J. (1995). Regulation of porcine skeletal muscle nuclear 3,5,3'-triiodothyronine receptor binding capacity by thyroid hormones: modification by energy balance. Journal of Endocrinology 144, 233242.CrossRefGoogle ScholarPubMed
Mount, L. E. (1979). Adaptation to Thermal Environment. London: Edward Arnold.Google Scholar
Muller, A., van der Linden, G. C., Zuidwijk, M. J., Simonides, W. S., van der Laarse, W. J. & van Hardeveld, C. (1994). Differential effects of thyroid hormone on the expression of sarcoplasmic reticulum Ca2+-ATPase isoforms in rat skeletal muscle fibers. Biochemical and Biophysical Research Communications 203, 10351042.CrossRefGoogle ScholarPubMed
Nørgaard, A., Kjeldsen, K., Hansen, O. & Clausen, T. (1983). A simple and rapid method for the determination of the number of 3H-ouabain binding sites in biopsies of skeletal muscle. Biochemical and Biophysical Research Communications 111, 319325.CrossRefGoogle ScholarPubMed
Nwoye, L., Mommaerts, W. F., Simpson, D. R., Seraydarian, K. & Marusich, M. (1982). Evidence for a direct action of thyroid hormone in specifying muscle properties. American Journal of Physiology 242, R401R408.Google ScholarPubMed
Rohrer, D. & Dillmann, W. H. (1988). Thyroid hormone markedly increases the mRNA coding for sarcoplasmic reticulum Ca2+-ATPase in the rat heart. Journal of Biological Chemistry 263, 69416944.CrossRefGoogle ScholarPubMed
Simonides, W. S. & van Hardeveld, C. (1989). The postnatal development of sarcoplasmic reticulum Ca2+ transport activity in skeletal muscle of the rat is critically dependent on thyroid hormone. Endocrinology 124, 11451153.CrossRefGoogle ScholarPubMed
ŚlebodziŃiski, A. B., Ingram, D. L. & Dauncey, M. J. (1985). Conversion of thyroxine into 3,5,3'-triiodothyronine and 3,3'5'-triiodothyronine in the young pig. Comparative Biochemistry and Physiology 80A, 559563.CrossRefGoogle Scholar