Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T06:50:36.973Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of food intake on hind-limb and whole-body protein metabolism in young growing sheep: chronic studies based on arterio-venous techniques

Published online by Cambridge University Press:  09 March 2007

Patricia M. Harris ,
Pat A. Skene ,
Vivien Buchan ,
E. Milne ,
A. G. Calder ,
Susan E. Anderson ,
Alexmary Connell  and
G. E. Lobley
Patricia M. Harris
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
Pat A. Skene
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
Vivien Buchan
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
E. Milne
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
A. G. Calder
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
Susan E. Anderson
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
Alexmary Connell
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
G. E. Lobley
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB2 9SB
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.

Whole-body protein synthesis, estimated by the irreversible loss rate procedure, and hind-leg protein metabolism determined by arterio-venous techniques were monitored in response to three nutritional conditions (approximately 0.6, 12 and 1.8 x energy maintenance (M)) in ten wether lambs (33 kg average live weight). In all lambs and treatments measurements were based on radiolabelled phenylalanine, but the terminal procedures (five at 0.6 x M and five at 1.8 x M) also included infusion of [1-13C]leucine; this permitted comparison of amino acids catabolized (leucine) and non-metabolized (phenylalanine) by the hind-limb tissues. Whole-body protein synthesis increased with intake and the relationship with energy expenditure was slightly lower than that reported previously for pigs and cattle. The efficiency of protein retention: protein synthesis did not exceed 0.25 between the two intake extremes. Effects of intake on amino acid oxidation were similar to those observed for cattle. Hind-limb protein synthesis also increased significantly (P < 0.001) in response to intake. Estimates of protein gain, from net uptake values, indicated that the tissues made a greater proportional contribution to total protein retention above M and to protein loss below M, emphasizing the role played by muscle tissue in providing mobile protein stores. The rates of protein synthesis calculated depended on the selection of precursor (blood) metabolite, but rates based on leucine always exceeded those based on phenylalanine when precursor from the same pool was selected. The incremental efficiency of protein retained: protein synthesis was apparently unity between 0.6 and 1.2 x M but 0.3 from 1.2 to 1.8 x M. Blood flow through the iliac artery was also proportional to intake. Leucine and oxo-acid catabolism to carbon dioxide increased with intake such that the metabolic fate of the amino acid was distributed in the proportion 2:1 between protein gain and oxidation. The rates of oxidation were only 1–3% the reported capacity of the rate-limiting dehydrogenase enzyme in muscle, but sufficient enzyme activity resides in the hind-limb adipose tissue to account for such catabolism

Keywords

Food intakeProtein synthesisHind-limb protein metabolismLamb
Type
Protein Digestion and Metabolism
Information
British Journal of Nutrition , Volume 68 , Issue 2 , September 1992 , pp. 389 - 407
Copyright
Copyright © The Nutrition Society 1992

References

REFERENCES

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
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
Bergen, W. G., Busboom, J. R. & Merket, R. A. (1988). Leucine degradation in sheep. British Journal of Nutrition 59, 323–333.CrossRefGoogle ScholarPubMed
Block, K. P., Aftring, P., Mehard, W. B. & Buse, M. A. (1987 a). Modulation of rat skeletal muscle branched-chain α-keto acid dehydrogenase in vivo. Journal of Clinical Investigation 79, 1349–1358.CrossRefGoogle ScholarPubMed
Block, K. P., Richmond, W. B., Mehard, W. B. & Buse, M. A. (1987 b). Glucocorticoid-mediated activation of muscle branched-chain α-keto acid dehydrogenase in vivo. American Journal of Physiology 252, E396–E407.Google ScholarPubMed
Boisclair, Y., Bauman, D. E., Bell, A. W. & Dunshea, F. R. (1988). Muscle protein synthesis and whole-body N balance in fed and underfed steers. FASEB Journal 2, A848.Google Scholar
Brockway, J. M. & Lobley, G. E. (1983). The effect of exercise on amino acid oxidation and protein synthesis in sheep. In Energy Metabolism of Farm Animals. European Association of Animal Production Publication no. 29, pp. 124–127. [Ekern, A. and Sundstot, F., editors]. Aas-NLH: Agriculture University of Norway.Google Scholar
Brown, J., Crompton, L. A. & Lomax, M. A. (1990). The effect of femoral arterial infusion of cimaterol on hind-limb metabolism in growing lamb. Proceedings of the Nutrition Society 49, 139A.Google Scholar
Calder, A. G. & Smith, A. (1988). Stable isotope ratio analysis 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 ScholarPubMed
Chalmers, M. I., Grant, I. & White, F. (1982). Free amino-nitrogen exchange across the hindquarters of fed and fasted sheep and pigs. Journal of Agricultural Science, Cambridge 99, 91–104.CrossRefGoogle Scholar
Cheng, K. N., Dworzak, F., Ford, G. C., Rennie, M. J. & Halliday, D. (1985). Direct determination of leucine metabolism and protein breakdown in humans using l-[l-13C,15N]leucine and the forearm model. European Journal of Clinical Investigation 15, 349–354.CrossRefGoogle ScholarPubMed
Cheng, K. N., Pacy, P. J., Dworzak, F., Ford, G. C. & Halliday, D. (1987). Influence of fasting on leucine and muscle protein metabolism across the human forearm determined using l-[l-13C,15N]leucine as the tracer. Clinical Science 73, 241–246.CrossRefGoogle ScholarPubMed
Davis, S. R., Barry, T. N. & Hughson, G. A. (1981). Protein synthesis in tissues of growing lambs. British Journal of Nutrition 46, 409–419.CrossRefGoogle ScholarPubMed
Elwyn, D. M., Parikk, H. C. & Shoemaker, W. C. (1968). Amino acid movements between gut, liver and periphery in unanesthetized dog. American Journal of Physiology 215, 1260–1275.CrossRefGoogle Scholar
Garlick, P. J., Fern, M. & Preedy, V. R. (1983). The effect of insulin infusion and food intake on muscle protein synthesis in postabsorptive rats. Biochemical Journal 210, 669–676.CrossRefGoogle ScholarPubMed
Goodwin, G. W., Gibboney, W., Paxton, R., Harris, R. A. & Lemons, J. A. (1987). Activities of branch-chain amino acid aminotransferase and branch-chain 2-oxo acid dehydrogenase complex in tissues of maternal and fed sheep. Biochemical Journal 242, 305–308.CrossRefGoogle Scholar
Hales, J. R. S. (1973). Radioactive microsphere measurement of cardiac output and regional tissue blood flow in the sheep. Pflügers Archiv 344, 119–132.CrossRefGoogle ScholarPubMed
Harper, A. E., Miller, R. H. & Block, K. P. (1984). Branched-chain amino acid metabolism. Annual Reviews in Nutrition 4, 409–454.CrossRefGoogle ScholarPubMed
Harris, P. M., Garlick, P. J. & Lobley, G. E. (1989). Interactions between energy and protein metabolism in the whole body and hindlimb of the sheep in response to intake. In Energy Metabolism of Farm Animals. European Association of Animal Production Publication no. 43, pp. 167–170 [van der Honing, Y. and Close, W. H., editors]. Wageningen: Pudoc.Google Scholar
Harris, P. M. & Lobley, G. E. (1990). Amino acid and energy metabolism in the peripheral tissues of ruminants. In Physiological Aspects of Digestion and Metabolism in Ruminants, pp. 201–230 [Tsuda, T., Sasaki, Y. and Kawashima, R., editors]. London: Academic Press.Google 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 59, 397–415.Google ScholarPubMed
Jois, M., Smithard, R., McDowell, G. H., Annison, E. F. & Gooden, J. M. (1985). Effects of growth hormone on amino acid exchanges in muscle tissue in growing calves. Proceedings of the Nutrition Society of Australia 10, 92–95.Google Scholar
Krishnamurti, C. R. & Janssens, S. M. (1988). Determination of leucine metabolism and protein turnover in sheep, using gas-liquid chromatography-mass spectrometry. British Journal of Nutrition 59, 155–164.CrossRefGoogle ScholarPubMed
Linzell, J. L. (1974). Mammary blood flow and methods of identifying and measuring precursors of milk. In Lactation: a Comprehensive Treatise, vol. 1, pp. 143–225 [Larson, B. L. and Smith, V. R., editors]. New York: Academic Press.Google Scholar
Lobley, G. E. (1986). The physiological bases of nutrient responses: growth and fattening. Proceedings of the Nutrition Society 45, 203–214.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. and Whitehead, C. C., editors]. London: Butterworths.CrossRefGoogle Scholar
Lobley, G. E. (1990). Energy metabolism reactions in ruminant muscle: responses to age, nutrition and hormonal status. Reproduction, Nutrition, Développement 30, 13–34.CrossRefGoogle ScholarPubMed
Lobley, G. E., Connell, A. & Buchan, V. (1987). Effect of food intake on protein and energy metabolism in finishing beef steers. British Journal of Nutrition 57, 457–465.CrossRefGoogle ScholarPubMed
Lobley, G. E., Connell, A., Milne, E., Buchan, V., Calder, A. G., Anderson, S. E. & Vint, H. (1990). Muscle protein synthesis in response to testosterone administration in wether lambs. British Journal of Nutrition 64, 691–704.CrossRefGoogle ScholarPubMed
Lobley, G. E., Connell, A., Mollison, G. S., Brewer, A. C., Harris, C. I., Buchan, V. & Galbraith, H. (1985). The effects of a combined implant of trenbolone acetate and oestradiol-17 β on protein and energy metabolism in growing beef steers. British Journal of Nutrition 54, 681–694.CrossRefGoogle ScholarPubMed
Lobley, G. E., Harris, P. M., Skene, P. A., Brown, D., Milne, E., Calder, A. G., Anderson, S. E., Garlick, P. J., Nevison, I. & Connell, A. (1992). Responses in tissue protein synthesis to sub- and supra-maintenance intake in young growing sheep; comparison of large-dose, and continuous-infusion techniques. British Journal of Nutrition 68, 373–388.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
McCormick, M. E. & Webb, K. E. Jr (1987). Serum proteins as carriers of amino acids to and from the hind limbs of fed and fasted calves. Journal of Animal Science 64, 586–593.CrossRefGoogle Scholar
McGaw, B. A., Milne, E. & Duncan, G. J. (1988). A rapid method for the preparation of combustion samples for stable carbon isotope analysis by isotope ratio mass spectrometry. Biomedical and Environmental Mass Spectrometry 16, 269–273.CrossRefGoogle Scholar
MacRae, J. C. & Reeds, P. J. (1980). Prediction of protein deposition in ruminants. In Protein Deposition in Animals, pp. 225–249 [Buttery, P. J. and Lindsay, D. B., editors]. London: Butterworths.CrossRefGoogle Scholar
MacRae, J. C., Skene, P. A., Connell, A., Buchan, V. & Lobley, G. E. (1988). The actions of the β-agonist, clenbuterol, on protein and energy metabolism in fattening wether lambs. British Journal of Nutrition 59, 457–465.CrossRefGoogle ScholarPubMed
Millward, D. J., Garlick, P. J., Nnanyelugo, D. O. & Waterlow, J. C. (1976). The relative importance of muscle protein synthesis and breakdown in the regulation of muscle mass. Biochemical Journal 156, 185–188.CrossRefGoogle ScholarPubMed
Muramatsu, T., Ueda, Y., Hirata, T., Okumura, J. & Tasaki, I. (1988). A note on the effect of ageing on whole-body protein turn-over in goats. Animal Production 46, 479–481.CrossRefGoogle Scholar
Oddy, V. H., Brown, B. W. & Jones, A. E. (1981). Measurement of organ blood flow using tritiated water. 1. Hindlimb muscle blood flow in conscious ewes. Australian Journal of Biological Research 34, 419–425.Google ScholarPubMed
Oddy, V. H., Gooden, J. M. & Annison, E. F. (1984). Partition of nutrients in merino ewes. 1. Contribution of skeletal muscle, the pregnant uterus and the lactating mammary gland to energy expenditure. Australian Journal of Biological Science 37, 375–388.CrossRefGoogle ScholarPubMed
Oddy, V. H. & Lindsay, D. B. (1986). Determination of protein synthesis, gain and degradation in intact hind-limb muscle of lambs. Biochemical Journal 233, 417–425.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
Papet, I., Lezebot, N., Barre, F. & Arnal, M. (1988). Influence of dietary leucine content on the activities of branched-chain amino acid transferase (EC 2.6.2.42) and branched-chain α-keto acid dehydrogenase (EC 1.2.4.4) complex in tissues of pre-ruminant lambs. British Journal of Nutrition 59, 475–483.CrossRefGoogle Scholar
Pell, J. M., Calderone, E. M. & Bergman, E. N. (1986). Leucine and α-ketoisocaproate metabolism and interconversions in fed and fasted sheep. Metabolism 35, 1005–1016.CrossRefGoogle ScholarPubMed
Preedy, V. R., McNurlan, M. A. & Garlick, P. J. (1983). Protein synthesis in skin and bone of the young rat. British Journal of Nutrition 45, 517–523.CrossRefGoogle Scholar
Randle, P. J., Fatania, H. R. & Lau, K. S. (1984). Regulation of the mitochondrial branched-chain 2-oxo acid dehydrogenase complex of animal tissues by reversible phosphorylation. Molecular Aspects of Cellular Regulation 3, 1–26.Google 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
Reeds, P. J., Cadenhead, A., Fuller, M. F., Lobley, G. E. & McDonald, J. D. (1980). Protein turnover in growing pigs. Effects of age and food intake. British Journal of Nutrition 43, 445–455.CrossRefGoogle ScholarPubMed
Rulquin, H. (1986). Utilisation des produits terminaux de la digestion par la mamelle chez la vache laitiere (Utilization of digestion end-products by the mammary gland of the dairy cow). Reproduction, Nutrition, Développement 26, 583–588.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
Schwenk, W. F., Beaufrere, B. & Haymond, M. W. (1985). Use of reciprocal pool specific activities to model leucine metabolism in humans. American Journal of Physiology 249, E646–E650.Google 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 energy metabolism. Reproduction, Nutrition, Développement 26, 849–861.CrossRefGoogle Scholar
Smith, H. W., Finkelstein, N., Aliminosa, L., Crawford, B. & Graber, M. (1945). The renal clearances of substituted hippuric acid derivatives and other aromatic acids in dog and man. Journal of Clinical Investigation 24, 388–404.CrossRefGoogle ScholarPubMed
Storm, E. & Ørskov, E. R. (1984). The nutritive value of rumen micro-organisms in ruminants. 4. The limiting amino acids of microbial protein determined by a new approach. British Journal of Nutrition 52, 613–620.CrossRefGoogle ScholarPubMed
Teleni, E., Annison, E. F. & Lindsay, D. B. (1986). Metabolism of valine and the exchange of amino acids across the hind-limb muscles of fed and starved sheep. Australian Journal of Biological Sciences 39, 379–393.CrossRefGoogle ScholarPubMed
Weaver, B. M. O., Staddon, G. E. & Pearson, M. R. B. (1989). Tissue blood content in anaesthestized sheep and horses. Comparative Biochemistry and Physiology 94A, 401–404.CrossRefGoogle Scholar