Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-19T12:28:38.699Z Has data issue: false hasContentIssue false

Energy expenditure associated with sodium/potassium transport and protein synthesis in skeletal muscle and isolated hepatocytes from hyperthyroid sheep

Published online by Cambridge University Press:  09 March 2007

Brian W. McBride
Affiliation:
Department of Animal and Poultry Science, The University of Guelph, Guelph, Ontario, N1G 2W1, Canada
Richard J. Early
Affiliation:
Department of Animal and Poultry Science, The University of Guelph, Guelph, Ontario, N1G 2W1, Canada
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.

The object of the present study was to determine the effect of thyroxine (T4) treatment of sheep on protein synthesis and associated energy costs in skeletal muscle and hepatocytes. Protein synthesis, and ouabain-sensitive and cycloheximide-sensitive respiration in isolated intercostal muscle and hepatocytes were determined in sheep after 5 weeks of daily injections of either saline or T4. Plasma T4 and total triiodothyronine (T3) concentrations were doubled and free T3 concentrations were quadrupled by T4 injections. The fractional rates of protein synthesis increased in isolated external intercostal muscle and hepatocytes from hyperthyroid sheep. Fractional rates of protein synthesis in isolated external intercostal muscle and hepatocytes were linearly correlated with plasma free T3 concentrations. Total oxygen consumption of muscle and hepatocytes was unaffected by T4 injections. Ouabain-sensitive respiration increased in hepatocytes and muscle of T4-treated animals. Cycloheximide-sensitive respiration was elevated in hepatocytes from hyperthyroid sheep. Cycloheximide-sensitive respiration in muscle was unaffected by T4 treatment. The present experiment demonstrates that T4 increases protein synthesis in ruminants. The energy expenditure in support of Na+, K+-ATPase and protein synthesis in skeletal muscle and hepatocytes may account for 34–60% of total cellular energy expenditure.

Type
Protein and Peptide Metabolism
Copyright
Copyright © The Nutrition Society 1989

References

REFERENCES

Bidlingmeyer, B.A., Cohen, S.A. & Tarvin, T.L. (1984). Rapid analysis of amino acids using pre-column derivatization. Journal of Chromatography 336, 93104.CrossRefGoogle ScholarPubMed
Brown, J.G., Bates, P.C., Holliday, M.A. & Millward, D.J. (1981). Thyroid hormones and muscle protein turnover. Biochemical Journal 194, 771782.CrossRefGoogle ScholarPubMed
Brown, J.G. & Millward, D.J. (1983). Dose response of protein turnover in rat skeletal muscle to triiodothyronine treatment. Biochimica et Biophysica Acta 767, 282290.Google Scholar
Christensen, H.N. (1982). Interorgan amino acid nutrition. Physiological Reviews 62, 11931239.CrossRefGoogle ScholarPubMed
Clark, M.G., Filsell, O.H. & Jarrett, I.G. (1976). Gluconeogenesis in isolated intact lamb liver cells. Biochemical Journal 156, 671680.CrossRefGoogle ScholarPubMed
Dawson, R.M.C., Elliot, D.C., Elliot, W.H. & Jones, K.M. (1969). Data for Biochemical Research. Oxford: Clarendon Press.Google Scholar
De Martino, D.N. & Goldberg, A.L. (1978). Thyroid hormones control lysosomal activites in liver and skeletal muscle. Proceedings of the National Academy of Sciences, USA 75, 13691373.CrossRefGoogle Scholar
Early, R.J., McBride, B.W. & Ball, R.O. (1988 a). Phenylalanine metabolism in sheep infused with glucose plus insulin. 1. Effects on plasma phenylalanine concentration, entry rate and utilization by hindlimb. Canadian Journal of Animal Science 68, 711719.CrossRefGoogle Scholar
Early, R.J., McBride, B.W. & Ball, R.O. (1988 b). Phenylalanine metabolism in sheep infused with glucose plus insulin. 2. Effects on in vivo and in vitro protein synthesis and related energy expenditures. Canadian Journal of Animal Science 68, 721730.CrossRefGoogle Scholar
Flaim, K.E., Li, J.B. & Jefferson, L.S. (1978). Effects of thyroxine on protein turnover in rat skeletal muscle. American Journal of Physiology 235, E231E236.Google ScholarPubMed
Garlick, P.J., Preedy, V.R. & Reeds, P.J. (1985). Regulation of protein turnover in vivo by insulin and amino acids. In Intracellular Protein Catabolism, Proceedings of the 5th International Symposium on Intracellular Protein Catabolism, pp. 555564s. [Khairallah, E.A., Bond, J.S. and Bird, J.W.C., editors]. New York: A. R. Liss.Google Scholar
Gregg, V.A. & Milligan, L.P. (1987). Thyroid induction of thermogenesis in cultured rat hepatocytes and sheep liver. In Energy Metabolism of Farm Animals, European Association for Animal Production Publication no. 32, pp. 1013 [Moe, P.W., Tyrrell, H.F. and Reynolds, P.J., editors]. Totowa, New Jersey: Rowman & Littlefield.Google Scholar
Harper, J.M.M., Soar, J.B. & Buttery, P.J. (1987). Changes in protein metabolism of ovine primary muscle cultures on treatment with growth hormone, insulin-like growth factor 1 or epidermal growth factor. Journal of Endocrinology 112, 8796.CrossRefGoogle ScholarPubMed
Heitmann, R.N. & Bergman, E.N. (1980). Integration of amino acid metabolism in sheep: effects of fasting and acidosis. American Journal of Physiology 239, E248E254.Google ScholarPubMed
Ismail-Beigi, F., Bissell, D.M. & Edelman, I.S. (1979). Thyroid thermogenesis in adult rat hepatocytes in primary monolayer cultures: direct action of thyroid hormones in vitro. Journal of General Physiology 73, 369383.CrossRefGoogle ScholarPubMed
Ismail-Beigi, F. & Edelman, I.S. (1970). Mechanism of thyroid calorigenesis: role of active sodium transport. Proceedings of the National Academy of Sciences, USA 67, 10711078.CrossRefGoogle Scholar
Jepson, M.M., Bates, P.C. & Millward, D.J. (1988). The role of insulin and thyroid hormones in the regulation of muscle growth and protein turnover in response to dietary protein in the rat. British Journal of Nutrition 69, 397415.Google Scholar
Karin, N.J. & Cook, J.S. (1983). Regulation of Na, K-ATPase by its biosynthesis and turnover. Current Topics in Membranes and Transport 19, 4349.Google Scholar
McBride, B.W. & Early, R.J. (1987). Effect of feeding frequency on tissue protein synthesis and related energy expenditures in sheep. Canadian Journal of Animal Science 68, 1190Google Scholar
McBride, B.W. & Milligan, L.P. (1985 a). Magnitude of ouabain-sensitive respiration of lamb hepatocytes (Ovis aries). International Journal of Biochemistry 17, 4349.CrossRefGoogle ScholarPubMed
McBride, B.W. & Milligan, L.P. (1985 b). Magnitude of ouabain-sensitive respiration in the liver of growing, lactating and starved sheep. British Journal of Nutrition 65, 293303.CrossRefGoogle Scholar
Moldeus, P., Hogberg, J. & Orrenious, S. (1978). Isolation and use of liver cells. Methods in Enzymology 52, 6071.CrossRefGoogle ScholarPubMed
Moses, A.C. & Pilistine, S.J. (1985). Insulin-like growth factors. In Control of Animal Cell Proliferation, vol. 1, pp. 91120 [Boynton, A.L. and Leffert, L., editors]. New York: Academic Press.CrossRefGoogle Scholar
Reeds, P.J., Fuller, M.F. & Nicholson, B.A. (1985). Metabolic basis of energy expenditure with particular reference to protein. In Substrate and Energy Metabolism in Man, pp. 4657 [Garrow, J.S. and Halliday, W., editors]. London: CRC Press.Google Scholar
Schultz, S.G. & Curran, P.F. (1970). Coupled transport of sodium and organic solutes. Physiological Reviews 50, 637718.CrossRefGoogle ScholarPubMed
Seglen, P.O. (1976). Preparation of isolated rat liver cells. Methods in Cell Biology 13, 2983.CrossRefGoogle ScholarPubMed
Siems, W., Dubiel, W., Dumdey, R., Muller, M. & Rapoport, S.M. (1984). Accounting for the ATP-consuming processes in rabbit reticulocytes. European Journal of Biochemistry 134, 101107.CrossRefGoogle Scholar
Smith, R.H., Palmer, R.M. & Reeds, P.J. (1983). Protein synthesis in isolated rabbit forelimb muscles. The possible role of metabolites of arachidonic acid in the response to intermittent stretching. Biochemical Journal 214, 153161.CrossRefGoogle ScholarPubMed
Statistical Analysis System Inc. (1982). SAS User's Guide: Statistics. Cary, North Carolina: SAS Inc.Google Scholar
Steel, R.G.D. & Torrie, J.H. (1960). Principles and Procedures of Statistics. New York: McGraw-Hill.Google Scholar
Vandenburgh, H. (1984). Relationship of muscle growth in vitro to sodium pump activity and transmembrane potential. Journal of Cellular Physiology 119, 283291.CrossRefGoogle ScholarPubMed
Vandenburgh, H.H. & Kaufman, S. (1981). Stretch-induced growth of skeletal myotubes correlates with activation of the sodium pump. Journal of Cellular Physiology 109, 205214.CrossRefGoogle ScholarPubMed
Wijayasinghe, M.S., Milligan, L.P. & Thompson, J.R. (1984). The preparation and in vitro viability of isolated external intercostal muscle fiber bundles from sheep. Canadian Journal of Animal Science 14, 785789.CrossRefGoogle Scholar
Zeman, R.J., Bernstein, P.L., Ludemann, R. & Etlinger, J.D. (1986). Regulation of Ca++-dependent protein turnover in skeletal muscle by thyroxine. Biochemical Journal 240, 269272.CrossRefGoogle Scholar