Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T08:58:18.278Z Has data issue: false hasContentIssue false

Lysine metabolism across the hindquarters of sheep; effect of intake on transfers from plasma and red blood cells

Published online by Cambridge University Press:  09 March 2007

Isabelle C. Savary*
Affiliation:
INRA-Theix, 63122 St Genès Champanelle, France
Simone O. Hoskin
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, Scotland, UK
Ngaire Dennison
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, Scotland, UK
Gerald E. Lobley
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, Scotland, UK
*
*Corresponding author: Dr Isabelle C. Savary, fax +33 4 73 62 46 39, email savary@clermont.inra.fr
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.

Both plasma and red blood cells contain amino acids (AA), but the relative amount of AA transferred from each vascular compartment to the tissues remains unclear. For splanchnic tissues, the relative transfers between the plasma, the red blood cells and the tissues may vary with nutritional state, but whether the same situation pertains for other tissues is not known. The current study focused on the transfer of lysine from plasma and red blood cells across the hindquarters of sheep offered four levels of intakes (0.5, 1.0, 1.5 and 2.5×maintenance energy). This design, coupled with use of [U-13C]lysine as tracer, also allowed the effect of intake on protein kinetics to be examined. At all intakes, the concentration of lysine in the sheep’ red blood cells exceeded that in plasma by 50 % (P<0.001), while the distribution of labelled lysine between the plasma and the red blood cells was 0.71:0.29. Net lysine uptake by the hindquarters increased in a linear manner (P<0.001) with intake, with more than 90 % extracted from the plasma. Free lysine enrichments in plasma from the posterior vena cava were less than that from the artery (P<0.001), but those in red blood cells were not different between the artery and vein. The red blood cells thus play a minor role in the transfers to and from the hindquarter tissues, regardless of intake. Based on plasma transfers and the enrichment of lysine in arterial plasma, hindquarter protein synthesis increased linearly with intake (P<0.001). In contrast, protein breakdown was unaffected by intake. The contribution of hindquarter protein synthesis to whole-body lysine flux remained unchanged with intake (18–20 %).

Type
Research Article
Copyright
Copyright © The Nutrition Society 2001

References

Ang, SD, Leskiw, MJ & Stein, TP (1983) The effect of increasing total parenteral nutrition on protein metabolism. Journal of Parenteral and Enteral Nutrition 7, 525529.CrossRefGoogle ScholarPubMed
Aoki, TT, Brennan, MF, Müller, WA, Soeldner, JS, Alpert, JS, Saltz, SB, Kaufmann, RL, Tan, MH & Cahill, GF (1976) Amino acid levels across normal forearm muscle and splanchnic bed after a protein meal. American Journal of Clinical Nutrition 29, 340350.CrossRefGoogle ScholarPubMed
Baillie, AG & Garlick, PJ (1991) Responses of protein synthesis in different skeletal muscles to fasting and insulin in rats. American Journal of Physiology 260, E891E896.Google ScholarPubMed
Biolo, G, Fleming, RYD, Maggi, SP & Wolfe, RR (1995 a) Transmembrane transport and intracellular kinetics of amino acids in human skeletal muscle. American Journal of Physiology 268, E75E84.Google ScholarPubMed
Biolo, G, Fleming, RYD & Wolfe, RR (1995 b) Physiological hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino-acids in human skeletal-muscle. Journal of Clinical Investigation 95, 811819.CrossRefGoogle ScholarPubMed
Boisclair, Y, Bauman, DE & Bell, AW (1993) Muscle protein synthesis and whole-body N balance in fed and unfed steers. Journal of Nutrition 123, 10761088.Google Scholar
Calder, AG, Garden, KE, Anderson, SE & Lobley, GE (1999) Quantitation of blood and plasma amino acids using isotope dilution mass spectrometry impact gas chromatography/mass spectrometry with U-13C amino acids as internal standards. Rapid Communications in Mass Spectrometry 13, 20802083.3.0.CO;2-O>CrossRefGoogle Scholar
Cherel, Y, Attaix, D, Rosolowska-Huszcz, D, Belkhov, R, Robin, J-P, Arnat, M & Le Maho, Y (1991) Whole body and tissue protein synthesis during brief and prolonged fasting in the rat. Clinical Science 81, 611620.CrossRefGoogle ScholarPubMed
Christensen, HN (1990) Role of amino acid transport and counter-transport in nutrition and metabolism. Physiological Reviews 70, 4377.CrossRefGoogle Scholar
Crompton, LA & Lomax, MA (1993) Hindlimb protein turnover and muscle protein synthesis in lambs: a comparison of techniques. British Journal of Nutrition 69, 345348.CrossRefGoogle ScholarPubMed
Elwyn, DH, Launder, WJ, Parikh, HC & Wise, EM (1972) Roles of plasma and erythrocytes in interorgan transport of amino acids in dogs. American Journal of Physiology 222, 13331342.CrossRefGoogle ScholarPubMed
Felipe, A, Vinas, O & Remesar, X (1990) Cationic and anionic amino acid transport studies in rat red blood cells. Bioscience of Reproduction 10, 527535.CrossRefGoogle ScholarPubMed
Garlick, PJ & Grant, I (1988) Amino acid infusion increases the sensitivity of muscle protein synthesis in vivo to insulin. Effect of branched-chain amino acids. Biochemical Journal 254, 579584.CrossRefGoogle ScholarPubMed
Garlick, PJ, Maltin, CA, Baillie, AG, Delday, MI & Grubb, DA (1989) Fiber-type composition of nine rat muscles. II Relationship to protein turnover. American Journal of Physiology 257, E828E832.Google ScholarPubMed
Golden, MH, Waterlow, JC & Picou, D (1977) Protein turnover, synthesis and breakdown before and after recovery from protein-energy malnutrition. Clinical Science and Molecular Medicine 53, 473477.Google ScholarPubMed
Hanigan, MD, Calvert, CC, DePeters, EJ, Reis, BL & Baldwin, RL (1991) Whole blood and plasma amino acid uptakes by lactating bovine mammary glands. Journal of Dairy Science 74, 24842490.CrossRefGoogle ScholarPubMed
Harris, PM, Skene, PA, Buchan, V, Milne, E, Calder, AG, Anderson, SE, Connell, A & Lobley, GE (1992) Effect of food intake on hind-limb and whole-body protein metabolism in young growing sheep: chronic studies based on arterio-venous techniques. British Journal of Nutrition 68, 389407.CrossRefGoogle ScholarPubMed
Heitmann, RN & Bergman, EN (1980) Transport of amino acids in whole blood and plasma of sheep. American Journal of Physiology Endocrinology and Metabolism 239, E242E247.Google ScholarPubMed
Houlier, ML, Patureau Mirand, P, Durand, D, Bauchart, D, Lefaivre, J & Bayle, G (1991) Transport des acides aminés dans l'aire splanchnique par le plasma sanguin et le sang chez le veau préruminant (Transport of amino acids by plasma and blood across the splanchnic region of pre-ruminant calves). Reproduction Nutrition Development 31, 399410.CrossRefGoogle Scholar
Hunter, RA & Magner, T (1990) Whole-body and tissue protein synthesis in steers losing weight on a low-protein roughage diet: the effect of trenbolone acetate. Journal of Agricultural Science 115, 121127.CrossRefGoogle Scholar
Keith, MO, Botting, HG & Peace, RW (1977) Dietary effects on the concentrations of free amino acids in plasma and whole blood of pigs. Canadian Journal of Animal Science 57, 295303.CrossRefGoogle Scholar
Le Floc'h, N, Mézière, N & Sève, B (1999) Whole blood and plasma amino acid transfers across the portal drained viscera and liver of the pig. Reproduction, Nutrition Development 39, 433442.CrossRefGoogle ScholarPubMed
Liu, SM, Mata, G, O'Donoghue, H & Masters, DG (1998) The influence of live weight, live-weight change and diet on protein synthesis in the skin and skeletal muscle in young merino sheep. British Journal of Nutrition 79, 267274.CrossRefGoogle ScholarPubMed
Lobley, GE (1998) Nutritional and hormonal control of muscle and peripheral tissue metabolism in farm species. Livestock Production Science 56, 91114.CrossRefGoogle Scholar
Lobley, GE, Connell, A, Lomax, MA, Brown, DS, Milne, E, Calder, AG & Farningham, DAH (1995) Hepatic detoxification of ammonia in the ovine liver, possible consequences for amino acid catabolism. British Journal of Nutrition 73, 667685.CrossRefGoogle ScholarPubMed
Lobley, GE, Connell, A, Revell, DK, Bequette, BJ, Brown, DS & Calder, AG (1996) Splanchnic-bed transfers of amino acids in sheep blood and plasma, as monitored through use of a multiple U-13C-labelled amino acid mixture. British Journal of Nutrition 75, 217235.CrossRefGoogle ScholarPubMed
Lobley, GE, Harris, PM, Skene, PA, Brown, D, Milne, E, Calder, AG, Anderson, SE, Garlick, PJ, 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, 373388.CrossRefGoogle ScholarPubMed
Lobley, GE, Milne, V, Lovie, JM, Reeds, PJ & Pennie, K (1980) Whole body and tissue protein synthesis in cattle. British Journal of Nutrition 43, 491502.CrossRefGoogle ScholarPubMed
Lochs, H, Morse, EL & Adibe, SA (1990) Uptake and metabolism of dipeptides by human red blood cells. Biochemical Journal 271, 133137.CrossRefGoogle ScholarPubMed
MacRae, JC, Walker, A, Brown, D & Lobley, GE (1993) Accretion of total protein and individual amino acids by organs and tissues of growing lambs and the ability of nitrogen balance techniques to quantitate protein retention. Animal Production 57, 237245.Google Scholar
Marston, NR (1948) Nutritional factors involved in wool production by Merino sheep. Australian Journal of Scientific Research 81, 362375.Google Scholar
Millward, DJ, Garlick, PJ, Nnanyelugo, DO & Waterlow, JC (1976) The relative importance of muscle protein synthesis and breakdown in the regulation of muscle mass. Biochemical Journal 156, 185188.CrossRefGoogle ScholarPubMed
Müller, M, Dubiel, W, Rathmann, J & Rapoport, S (1980) Determination and characteristics of energy-dependent proteolysis in rabbit reticulocytes. European Journal of Biochemistry 109, 405410.CrossRefGoogle ScholarPubMed
Oddy, VH (1993) Regulation of muscle protein metabolism in sheep and lambs: nutritional, endocrine and genetic aspects. Australian Journal of Agricultural Research 44, 901913.CrossRefGoogle Scholar
Oddy, VH, Lindsay, DB, Barker, PJ & Northrop, AJ (1987) Effect of insulin on hind-limb and whole-body leucine and protein metabolism in fed and fasted lambs. British Journal of Nutrition 58, 437452.CrossRefGoogle ScholarPubMed
Odoom, JE, Campbell, ID, Ellory, JC & King, GF (1990) Characterization of peptide fluxes into human erythrocytes. Biochemical Journal 267, 141147.CrossRefGoogle ScholarPubMed
Pell, JM, Caldarone, EM & Bergman, EN (1986) Leucine and alpha-ketoisocaproate metabolism and interconversions in fed and fasted sheep. Metabolism: Clinical and Experimental 35, 10051016.CrossRefGoogle ScholarPubMed
Pitts, RF, DeHaas, J & Kelin, J (1963) Relation of renal amino and amide nitrogen extraction to ammonia production. American Journal of Physiology 204, 187191.CrossRefGoogle ScholarPubMed
Reeds, PJ, Cadenhead, A, Fuller, MF, Lobley, GE & McDonald, JD (1980) Protein turnover in growing pigs. Effect of age and food intake. British Journal of Nutrition 43, 445455.CrossRefGoogle ScholarPubMed
Rocha, HJG, Nash, JE, Connell, A & Lobley, GE (1993) Protein synthesis in ovine muscle and skin: sequential measurements with three different amino acids based on the large-dose procedure. Comparative Biochemistry and Physiology 105B, 301307.Google ScholarPubMed
Savary, IC, Hoskin, SO & Lobley, GE (1999) Effect of intake on the transfer of lysine to the hindlimb in sheep blood and plasma.In Abstracts of the 8th International Symposium on Protein Metabolism and Nutrition (Aberdeen, UK), p.18. [GE, Lobley, A, White & JC, MacRae, editors]. Wageningen: Wageningen Pers.Google Scholar
Seve, B, Ballevre, O, Ganier, P, Noblet, J, Prugnaud, J & Obled, C (1993) Recombinant porcine somatotropin and dietary protein enhance protein synthesis in growing pigs. Journal of Nutrition 123, 529540.CrossRefGoogle ScholarPubMed
Seve, B, Reeds, PJ, Fuller, MF, Cadenhead, A & Hay, SH (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 Development 26, 849861.CrossRefGoogle Scholar
Teleni, E, Annison, EF & Lindsay, DB (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, 379393.CrossRefGoogle ScholarPubMed
Thompson, BC, Hosking, BJ, Sainz, RD & Oddy, VH (1997) The effect of nutritional status on protein degradation and components of the calpain system in skeletal muscle of weaned wether lambs. Journal of Agricultural Science 129, 471477.CrossRefGoogle Scholar
Wagenmakers, AJM (1999) Tracers to investigate protein and amino acid metabolism in human subjects. Proceedings of the Nutrition Society 58, 9871000.CrossRefGoogle ScholarPubMed
Watt, PW, Corbett, ME & Rennie, MJ (1992) Stimulation of protein synthesis in pig skeletal muscle by infusion of amino acids during constant insulin availability. American Journal of Physiology 263, E453E460.Google ScholarPubMed
Wester, TJ, Lobley, GE, Birnie, LM & Lomax, MA (2000) Insulin stimulates phenylalanine uptake across the hindlimb in fed lambs. Journal of Nutrition 130, 608611.CrossRefGoogle Scholar
Yahya, ZAH & Millward, DJ (1994 a) Dietary protein and the regulation of long-bone and muscle growth in the rat. Clinical Science 87, 213224.CrossRefGoogle ScholarPubMed
Yahya, ZAH, Tirapegui, JO, Bates, PC & Millward, DJ (1994 b) Influence of dietary protein, energy and corticoseroids on protein turnover, proteoglycan sulphuration and growth of long bone and skeletal muscle in the rat. Clinical Science 87, 607618.CrossRefGoogle Scholar
Young, JD, Ellory, JC & Tucker, EM (1976) Amino acid transport in normal and glutathione-deficient sheep erythrocytes Biochemical Journal 154, 4348.CrossRefGoogle ScholarPubMed