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Muscle protein synthesis in response to testosterone administration in wether lambs

Published online by Cambridge University Press:  09 March 2007

G. E. Lobley ,
Alexmary Connell ,
E. Milne ,
Vivien Buchan ,
A. G. Calder ,
Susan E. Anderson  and
Hazel Vint
G. E. Lobley
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
Alexmary Connell
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
E. Milne
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
Vivien Buchan
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
A. G. Calder
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
Susan E. Anderson
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
Hazel Vint
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB2 9SB
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Abstract

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A method has been developed based on stable isotopes and biopsy procedures which allows the large-dose procedure for measurement of protein synthesis to be applied in serial studies to farm species. Measurements of total nitrogen retention and protein synthesis in m. longissimus dorsi and m. vastus lateralis were made in five wether lambs (40–44 kg) infused intravenously, successively, with vehicle (10 d); testosterone (15 d; 9 mg/d); vehicle (15 d). N retention was improved by testosterone infusion (+2.9 g N/d; a 96% improvement total over control periods). Muscle protein synthesis was not significantly altered by exogenous hormone administration, nor were RNA:protein, RNA:DNA or protein: DNA. The implication of the developed procedure for dynamic studies in accessible tissues of large animals is discussed.

Keywords

Protein synthesisTestosteroneLambsMuscle
Type
Synthesis of Muscle Protein
Information
British Journal of Nutrition , Volume 64 , Issue 3 , November 1990 , pp. 691 - 704
Copyright
Copyright © The Nutrition Society 1990

References

Association of Official Agricultural Chemists (1980). Official Methods of Analysis, 13th ed. Washington, DC: Association of Official Agricultural Chemists.Google Scholar
Attaix, D., Aurousseau, E., Manghebati, A. & Arnal, M. (1988). Contribution of liver, skin and skeletal muscle to whole body protein synthesis in the young lamb. British Journal of Nutrition 60, 77–84.CrossRefGoogle ScholarPubMed
Attaix, D., Manghebati, A., Grizard, J. & Arnal, M. (1986). Assessment of in vivo protein synthesis in lamb tissues with [3H]valine flooding doses. Biochimica et Biophysica Acta 882, 389–397.CrossRefGoogle ScholarPubMed
Baillie, A. G. S., Maltin, C. A. & Garlick, P. J. (1988). The effect of fasting and insulin infusion on muscle protein synthesis in immature and adult rats. Proceedings of the Nutrition Society 47, 114A.Google Scholar
Ballard, F. J. & Francis, G. L. (1983). Effects of anabolic agents on protein breakdown in L6 myoblasts. Biochemical Journal 210, 243–249.CrossRefGoogle ScholarPubMed
Bates, P. C., Chew, L. F. & Millward, D. J. (1987). Effects of the anabolic steroid stanozolol on growth and protein metabolism in the rat. Journal of Endocrinology 114, 373–381.CrossRefGoogle ScholarPubMed
Bennet, W. W., Connacher, A. A., Scrimgeour, C. M., Smith, K. & Rennie, M. J. (1989). Increase in anterior tibialis muscle protein synthesis in healthy man during mixed amino acid infusion: studies of incorporation of [I-13C]leueine. Clinical Science 76, 447–454.CrossRefGoogle Scholar
Brown, B. H., Neill, S. F. & Horgan, R. (1986). Partial isotope fractionation during high-performance liquid chromatography of deuterium-labelled internal standards in plant hormone analysis: a cautionary note. Planta 167, 421–423.CrossRefGoogle ScholarPubMed
Burgess, T. D. & Lamming, G. E. (1960). The effect of diethylstilboestrol, hexoestrol and testosterone on the growth rate and carcass quality of fattening beef steers. Animal Production 2, 93–102.CrossRefGoogle Scholar
Burton, K. (1956). A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochemical Journal 62, 315–323.CrossRefGoogle ScholarPubMed
Buse, M. G., Atwell, R. & Mancusi, V. (1979). In vitro effect of branched chain amino acids on the ribosomal cycle in muscles of fasted rats. Hormone and Metabolic Research 11, 289–292.Google ScholarPubMed
Buse, M. G. & Reid, S. S. (1975). Leucine: a possible regulator of protein turnover in muscle. Journal of Clinical Investigation 56, 1250–1261.CrossRefGoogle ScholarPubMed
Buse, M. G. & Weigand, D. A. (1977). Studies concerning the specificity of the effect of leucine on the turnover of proteins in muscles of control and diabetic rats. Biochimica et Biophysica Acta 475, 81–89.CrossRefGoogle ScholarPubMed
Calder, A. G. & Smith, A. (1988). Stable isotope ratio analyses of leucine and ketoisocaproic acid in blood plasma by gas chromatography/mass spectrometry. Use of the tertiary butyldimethylsilyl derivatives. Rapid Communications in Mass Spectrometry 2, 14–16.CrossRefGoogle Scholar
Coxam, V., Bauchart, D., Durand, D., Davicco, M.-J., Opmeer, F. & Bartlet, J.-P. (1989). Nutrient effects on the hepatic production of somatomedin C (IGFI) in the milk-fed calf. British Journal of Nutrition 62, 425–437.CrossRefGoogle ScholarPubMed
Davis, S. L., Ohlson, D. L., Klindt, J. & Anfinson, M. S. (1977). Episodic growth hormone secretory patterns in sheep: relationship to gonadal steroid hormones. American Journal of Physiology 233, E519–E523.Google ScholarPubMed
de Loecker, W. (1965). The effects of testosterone on the incorporation of glycine-U-14C into the proteins and the nucleic acids of skeletal muscle. Archives Internationales de Pharmacodynamie 153, 69–78.Google Scholar
D'Occhio, M. J., Schanbacher, B. D. & Kinder, J. E. (1982). Relationship between serum testosterone concentration and patterns of luteinizing hormone secretion in male sheep. Endocrinology 110, 1547–1554.CrossRefGoogle ScholarPubMed
Dohm, G. L., Tapscott, E. B. & Louis, T. M. (1979). Skeletal muscle protein turnover after testosterone administration in the castrated male rat. IRCS Medical Science 7, 40.Google Scholar
Early, R. J., McBride, B. W. & Ball, R. O. (1988 a). Phenylalanine metabolism in sheep infused with glucose plus insulin. I. Effects on plasma phenylalanine concentration, entry rate and utilisation by the hindlimb. Canadian Journal of Animal Science 68, 711–719.CrossRefGoogle Scholar
Early, R. J., McBride, B. W. & Ball, R. O. (1988 b). Phenylalanine metabolism in sheep infused with glucose plus insulin. II. Effects on in vivo and in vitro protein synthesis and related energy expenditures. Canadian Journal of Animal Science 68, 721–730.CrossRefGoogle Scholar
Eisemann, J. H., Hammond, A. C., Romsey, T. S. & Bauman, D. E. (1989). Nitrogen protein metabolism and metabolites in plasma and urine of beef steers treated with somatotropin. Journal of Animal Science 67, 105–115.CrossRefGoogle ScholarPubMed
Fajans, S. S., Floyd, J. C., Knopf, R. F. & Conn, J. W. (1967). Effect of amino acids and protein on insulin secretion in man. Recent Progress in Hormone Research 23, 617–662.Google ScholarPubMed
Fletcher, J. M., Lobley, G. E. & Connell, A. (1986). Effects on growth and body composition of androgen deprivation by castration or autoimmunization to LH-releasing hormone in the male rat under conditions of controlled food intake. Endocrinology 110, 97–102.CrossRefGoogle ScholarPubMed
Ford, G. D., Cheng, K. N. & Halliday, D. (1985). Analysis of [1-13C]leucine and [13C]KIC in plasma by capillary gas chromatography/mass spectrometry in protein turnover studies. Biomedical Mass Spectrometry 12, 432–436.CrossRefGoogle ScholarPubMed
Fulks, R. M., Li, J. B. & Goldberg, A. L. (1975). Effect of insulin, glucose and amino acids on protein turnover in rat diaphragm. Journal of Biological Chemistry 250, 290–298.CrossRefGoogle ScholarPubMed
Fuller, M. F., Weekes, T. E. C., Cadenhead, A. & Bruce, J. B. (1977). The protein-sparing effect of carbohydrate. 2. The role of insulin. British Journal of Nutrition 38, 489–496.CrossRefGoogle ScholarPubMed
Gaitonde, M. K. & Nixey, R. W. K. (1972). Sources of error in the determination of specific radioactivity of amino acids isolated by ion-exchange chromatography. Analytical Biochemistry 50, 416–429.CrossRefGoogle ScholarPubMed
Garlick, P. J., Fern, M. & Preedy, V. R. (1983). The effect of insulin infusion and food intake on muscle protein synthesis in post absorptive rats. Biochemical Journal 210, 669–676.CrossRefGoogle Scholar
Garlick, P. J. & Grant, I. (1988). Amino acid infusion increases the sensitivity of muscle protein synthesis in vivo to insulin: effect of branch chain amino acids. Biochemical Journal 254, 579–584.CrossRefGoogle Scholar
Garlick, P. J., Grant, I. & Glennie, R. T. (1987). Short-term effects of corticosterone treatment on protein synthesis in relation to the response to feeding. Biochemical Journal 248, 439–442.CrossRefGoogle Scholar
Garlick, P. J., McNurlan, M. A. & Preedy, V. R. (1980). A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H]phenylalanine. Biochemical Journal 192, 719–723.CrossRefGoogle ScholarPubMed
Garlick, P. J., Wernerman, J., McNurlan, M. A., Essen, P., Lobley, G. E., Milne, E., Calder, A. G. & Vinnars, E. (1989). Measurement of the rate of protein synthesis in muscle of postabsorptive, young men by injection of a ‘flooding dose’ of [1-13C]leucine. Clinical Science 77, 329–336.CrossRefGoogle Scholar
Gaunce, A. P. & D'Iorio, A. (1970). Microdetermination of protein by an automated Lowry method. Analytical Biochemistry 37, 204–207.CrossRefGoogle ScholarPubMed
Grigsby, J. S., Bergen, W. G. & Merkel, R. A. (1976). The effect of testosterone on skeletal muscle development and protein synthesis in rabbits. Growth 40, 303–316.Google ScholarPubMed
Heys, S. D., McNurlan, M. A., Park, K. G. M., Milne, E. & Garlick, P. J. (1990 a). Baseline measurements for stable isotope studies. Proceedings of the Nutrition Society 49, 122A.Google Scholar
Heys, S. D., Park, K. G. M., McNurlan, M. A., Kennan, R. A., Miller, J. D. B., Eremin, O. & Garlick, P. J. (1990 b). Measurement of tissue protein synthesis in pathological conditions of the gastrointestinal tract in man. Proceedings of the Nutrition Society, 49, 135A.Google Scholar
Isgaard, J., Milsson, A., Vikman, K. & Isaksson, O. G. P. (1989). Growth hormone regulates the level of insulin-like growth factor-1 mRNA in rat skeletal muscle. Journal of Endocrinology 120, 107–112.CrossRefGoogle ScholarPubMed
Jansson, J.-O., Eden, S. & Isaksson, O. (1983). Sites of action of testosterone and estradiol on longitudinal bone growth. American Journal of Physiology 244, E135–E140.Google ScholarPubMed
Jepson, M. M., Bates, P. C. & Milward, 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 59, 397–415.Google ScholarPubMed
Kerr, S. E. & Seraidarian, K. (1945). The separation of purine nucleosides from free purines and the determination of the purines and ribose in these fractions. Journal of Biological Chemistry 159, 211–225.CrossRefGoogle Scholar
Kochakian, C. D. (1975). Definition of androgens and protein anabolic steroids. Pharmacology and Therapeutics B 1, 149–177.Google ScholarPubMed
Li, J. B. & Jefferson, L. S. E. (1978). Influence of amino acid availability on protein turnover in perfused skeletal muscle. Biochimica et Biophysica Acta 544, 351–359.CrossRefGoogle ScholarPubMed
Lobley, G. E. (1988). Protein turnover and energy metabolism in animals: interactions in leanness and obesity. In Leanness in Domestic Birds, pp. 331–361 [Leclerq, B. & Whitehead, C., editors]. London: Butterworths.CrossRefGoogle Scholar
Lobley, G. E., Connell, A., Buchan, V., Milne, E., Calder, A. G. & Skene, P. A. (1990). Use of a large dose, stable isotope procedure to measure muscle protein synthesis in sheep. Proceedings of the Nutrition Society 49, 134A.Google Scholar
Lobley, G. E., Connell, A., Buchan, V., Skene, P. A. & Fletcher, J. M. (1987). Administration of testosterone to wether lambs: effects of protein and energy metabolism and growth hormone status. Journal of Endocrinology 115, 439–445.CrossRefGoogle ScholarPubMed
Lobley, G. E., Milne, V., Lovie, J. M., Reeds, P. J. & Pennie, K. (1980). Whole body and tissue protein synthesis in cattle. British Journal of Nutrition 32, 491–502.CrossRefGoogle Scholar
MacKenzie, S. L. & Tenaschuk, D. (1974). Gas-liquid chromatography of N-heptafluorobutyryl esters of amino acids. Journal of Chromatography 97, 19–24.CrossRefGoogle ScholarPubMed
McNurlan, M. A., Fern, E. B. & Garlick, P. J. (1982). Failure of leucine to stimulate protein synthesis in vivo. Biochemical Journal 204, 831–838.CrossRefGoogle ScholarPubMed
Martinez, J. A., Buttery, P. J. & Pearson, J. T. (1984). The mode of action of anabolic agents: the effect of testosterone on muscle protein metabolism in the female rat. British Journal of Nutrition 52, 515–521.CrossRefGoogle ScholarPubMed
Matras, J. & Preston, R. (1985). Role of branched chain amino acids in the nitrogen utilisation of ruminants. Federation Proceedings 44, 750 Abstr.Google Scholar
Mayer, M. & Rosen, F. (1977). Interaction of glucocorticoids and androgens with skeletal muscle. Metabolism 26, 937–962.CrossRefGoogle ScholarPubMed
Mazzaferri, E. L., Ciofalo, L., Waters, S. A., Starich, G. H., Groshong, J. C. & DePalma, L. (1983). Effects of gastro inhibitory polypeptide on leucine- and arginine-stimulated insulin release. American Journal of Physiology 245, E114–E120.Google Scholar
Midgley, A. R., Rebau, R. W. & Niswender, G. D. (1969). Radioimmunoassays employing double antibody techniques. Acta Endocrinologica 142, Suppl., 247–254.Google ScholarPubMed
Millard, B. J. (1979). Quantitative Mass Spectrometry, p. 136. London: Heyden & Son.Google Scholar
Millward, D. J., Odedra, B. & Bates, P. C. (1983). The role of insulin, corticosterone and other factors in the acute recovery of muscle protein synthesis on refeeding food-deprived rats. Biochemical Journal 216, 383–387.CrossRefGoogle ScholarPubMed
Milne, E. & McGaw, B. A. (1987). The applicability of evacuated serological tubes for collection of breath for isotopic analysis of CO2 by isotope ratio mass spectrometry. Biomedical and Environmental Mass Spectrometry 15, 467–472.CrossRefGoogle Scholar
Nicholas, G. A., Lobley, G. E. & Harris, C. I. (1977). Use of the constant infusion technique for measuring rates of protein synthesis in the New Zealand White rabbit. British Journal of Nutrition 38, 1–17.CrossRefGoogle ScholarPubMed
Oddy, V. H., Lindsay, D. B., Barker, P. J. & Northrop, A. J. (1987). Effect of insulin on hind-limb and whole-body leucine and protein metabolism in fed and fasted lambs. British Journal of Nutrition 58, 437–452.CrossRefGoogle ScholarPubMed
Ohlsson, L., Isaksson, O. & Jansson, J.-O. (1987). Endogenous testosterone enhances growth hormone (GH)- releasing factor-induced GH secretion in vitro. Journal of Endocrinology 113, 249–253.CrossRefGoogle ScholarPubMed
O'Mary, C. C., Pope, A. L., Wilson, G. D., Bray, R. W. & Casida, L. E. (1952). The effects of diethylstilbestrol, testosterone and progesterone on growth and fattening and certain carcass characteristics of western lambs. Journal of Animal Science 11, 656–673.CrossRefGoogle Scholar
Palmer, R. M., Bain, P. A. & Reeds, P. J. (1985). The effect of insulin and intermittent mechanical stretching on rates of protein synthesis and degradation in isolated rabbit muscle. Biochemical Journal 230, 117–123.CrossRefGoogle ScholarPubMed
Papet, I., Breville, D., Glomot, F. & Arnal, M. (1988). Nutritional and metabolic effects of dietary leucine excess in the preruminant lamb. Journal of Nutrition 118, 450–455.CrossRefGoogle Scholar
Pell, J. M. & Bates, P. C. (1987). Collagen and non-collagen protein turnover in skeletal muscle of growth hormone-treated lambs. Journal of Endocrinology 115, Rl–R4.CrossRefGoogle ScholarPubMed
Pell, J. M., Bates, P. C., Elcock, C., Lane, S. E. & Simmonds, A. D. (1987). Growth hormone and clenbuterol: action and interaction on muscle growth, protein turnover, and serum IGF-I concentrations in dwarf mice. Journal of Endocrinology 115, Suppl., 68.Google Scholar
Powers, M. L. & Florini, J. R. (1975). A direct effect of testosterone on muscle cells in tissue culture. Endocrinology 97, 1043–1047.CrossRefGoogle Scholar
Prescott, J. H. & Lamming, G. E. (1964). The effects of castration on meat production in cattle, sheep and pigs. Journal of Agricultural Science 63, 341–356.CrossRefGoogle Scholar
Read, W. W., Read, M., Rennie, M. J., Griggs, R. C. & Halliday, D. (1984). Preparation of CO2 from blood and protein-bound amino acid carboxyl groups for quantitation of 13C-isotope enrichments. Biomedical Mass Spectrometry 15, 467–472.Google Scholar
Rocha, D. M., Faloona, G. R. & Unger, R. H. (1972). Glucagon-stimulating activity of 20 amino acids in dogs. Journal of Clinical Investigation 51, 2346–2351.CrossRefGoogle Scholar
Schaefer, A. L., Davis, S. R. & Hughson, G. A. (1986). Estimation of tissue protein synthesis in sheep during sustained elevation of plasma leucine concentration by intravenous infusion. British Journal of Nutrition 56, 281–288.CrossRefGoogle ScholarPubMed
Schanbacher, B. D., Crouse, J. D. & Ferrell, C. L. (1980). Testosterone influences on growth, performance, carcass characteristics and composition of young market lambs. Journal of Animal Science 51, 585–691.CrossRefGoogle ScholarPubMed
Schimpff, R. M., Donnadieu, M., Glasinovic, J. C., Warnet, J. M. & Girard, F. (1976). The liver as a source of somatomedin. Acta Endocrinologica 83, 365–372.Google ScholarPubMed
Scow, R. O. & Hagan, S. N. (1965). Effect of testosterone propionate and growth hormone on growth and chemical composition of muscle and other tissues in hypophysectomized male rats. Endocrinology 77, 852–858.CrossRefGoogle ScholarPubMed
Seve, B., Reeds, P. J., Fuller, M. F., Cadenhead, A. & Hay, S. M. (1986). Protein synthesis and retention in some tissues of the young pig as influenced by dietary protein intake after early weaning. Possible connection to the energy metabolism. Reproduction, Nutrition et Développement 26, 849–861.CrossRefGoogle Scholar
Singh, S. B., Galbraith, H., Scaife, J. R. & Hunter, E. A. (1985). Effects of oestrogenic and androgenic compounds on growth and body composition of male castrate lambs. Proceedings of the Nutrition Society 44, 93A.Google Scholar
Smith, T. K. (1985). Effect of leucine-rich dietary protein on in vitro protein synthesis in porcine muscle. Proceedings of the Society for Experimental Biology and Medicine 180, 538–543.CrossRefGoogle ScholarPubMed
Spangler, R. S. & Phillips, R. W. (1982). Portal vein insulin response of glucose intolerant Yucatan miniature swine to common secretagogues. Hormone Metabolic Research 14, 448–452.CrossRefGoogle Scholar
Stratman, F. W. (1978). Influence of anabolic hormones on protein metabolism in the isolated perfused rat hind limb: a technique for cyclic cross-perfusion of isolated limb and liver. Journal of Steroid Biochemistry 9, 1169–1177.CrossRefGoogle ScholarPubMed
Sumner, R. & Weekes, T. E. C. (1983). Effect of insulin infusion on nitrogen excretion in sheep. Proceedings of the Nutrition Society 42, 39A.Google Scholar
Suzuki, A. (1971). Histochemical classification of individual skeletal muscle fibres in the sheep. 1. On M. semitendinosus, M. longissimus dorsi, M. psoas major, M. latissimus dorsi and M. gastrocnemius. Japanese Journal of Zootechnical Science 42, 39–53.Google Scholar
Thomas, K. M. & Rodway, R. G. (1982). Suppression of adrenocorticol function in rats and sheep treated with the anabolic steroid trenbolone acetate. Proceedings of the Nutrition Society 41, 138A.Google Scholar
van Eenaeme, C., Baldwin, P., Lambot, O. & Bienfait, J. M. (1983). Estimation of in vivo muscle protein turnover in young bulls treated with anabolic agents. In 4th International Symposium on Protein Metabolism and Nutrition, European Association for Animal Production Publication no. 31, pp. 81–84 [Pion, R., Arnal, M. and Bonin, D., editors]. Paris: INRA.Google Scholar
Vernon, B. G. & Buttery, P. J. (1978). Protein metabolism of rats treated with trenbolone acetate. Animal Production 26, 1–9.Google Scholar
Young, I. R., Mesiano, S., Hintz, R., Caddy, D. J., Ralph, M. M., Browne, C. A. & Thorburn, G. D. (1989). Growth hormone and testosterone can independently stimulate the growth of hypophysectomised prepubertal lambs without any alteration in circulating concentrations of insulin-like growth factors. Journal of Endocrinology 121, 563–570.CrossRefGoogle Scholar