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Effect of plasma insulin and branched-chain amino acids on skeletal muscle protein synthesis in fasted lambs

Published online by Cambridge University Press:  09 March 2007

T. J. Wester ,
G. E. Lobley ,
L. M. Birnie ,
L. A. Crompton ,
S. Brown ,
V. Buchan ,
A. G. Calder ,
E. Milne  and
M. A. Lomax
T. J. Wester
Affiliation:
Department of Agriculture, MacRobert Building, University of Aberdeen, Aberdeen AB24 5UA, Scotland, UK
G. E. Lobley
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, Scotland, UK
L. M. Birnie
Affiliation:
Department of Agriculture, MacRobert Building, University of Aberdeen, Aberdeen AB24 5UA, Scotland, UK
L. A. Crompton
Affiliation:
School of Agriculture, Policy & Development, The University of Reading, Whiteknights, PO Box 237, Reading RG6 6AR, UK
S. Brown
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, Scotland, UK
V. Buchan
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, Scotland, UK
A. G. Calder
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, Scotland, UK
E. Milne
Affiliation:
School of Agriculture, Policy & Development, The University of Reading, Whiteknights, PO Box 237, Reading RG6 6AR, UK
M. A. Lomax*
Affiliation:
Department of Agricultural Sciences, Imperial College, Wye, Kent TN25 5AH, UK
*
*Corresponding author: fax + 44 020 759 42919, Email [email protected]
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Abstract

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The increase in fractional rate of protein synthesis (Ks) in the skeletal muscle of growing rats during the transition from fasted to fed state has been explained by the synergistic action of a rise in plasma insulin and branched-chain amino acids (BCAA). Since growing lambs also exhibit an increase in Ks with level of feed intake, the objective of the present study was to determine if this synergistic relationship between insulin and BCAA also occurs in ruminant animals. Six 30 kg fasted (72 h) lambs (8 months of age) received each of four treatments, which were based on continuous infusion into the jugular vein for 6 h of: (1) saline (155 mmol NaCl/l); (2) a mixture of BCAA (0·778 μmol leucine, 0·640 μmol isoleucine and 0·693 μmol valine/min·kg); (3) 18·7 μmol glucose/min·kg (to induce endogenous insulin secretion); (4) co-infusion of BCAA and glucose. Within each period all animals received the same isotope of phenylalanine (Phe) as follows: (1) l-[1-13C]Phe; (2) l-phenyl-[ring 2H5]-alanine; (3) l-[15N]Phe; (4) l-[ring 2,6-3H]Phe. Blood was sampled serially during infusions to measure plasma concentrations of insulin, glucose and amino acids, and plasma free Phe isotopic activity; biopsies were taken 6 h after the beginning of infusions to determine Ks in m. longissimus dorsi and vastus muscle. Compared with control (saline-infused) lambs, Ks was increased by an average of 40 % at the end of glucose infusion, but this effect was not statistically significant in either of the muscles sampled. BCAA infusion, alone or in combination with glucose, also had no significant effect on Ks compared with control sheep. Ks was approximately 60 % greater for vastus muscle than for m. longissimus dorsi (P>0·01), regardless of treatment. It is concluded that there are signals other than insulin and BCAA that are responsible for the feed-induced increase in Ks in muscle of growing ruminant animals.

Keywords

Muscle protein synthesisInsulinBranched-chain amino acids
Type
Research Article
Information
British Journal of Nutrition , Volume 92 , Issue 3 , September 2004 , pp. 401 - 409
Copyright
Copyright © The Nutrition Society 2004

References

Baillie, AG & Garlick, PJResponses of protein synthesis in different skeletal muscles to fasting and insulin in rats. Am J Physiol (1991) 260, E891–E896.Google ScholarPubMed
Baillie, AG & Garlick, PJAttenuated responses of muscle protein synthesis to fasting and insulin in adult female rats. Am J Physiol (1992) 262, E1–E5.Google ScholarPubMed
Barua, JM, Wilso, E, Downie, S, Weryk, B, Cuschieri, A & Rennie, MJThe effect of alanyl glutamine peptide supplementation on muscle protein synthesis in post-surgical patients receiving glutamine-free amino acids intravenously. Proc Nutr Soc (1992) 51, 115A.Google Scholar
Bennet, WM, Connacher, AA, Scrimgeour, CM, Jung, RT & Rennie, MJEuglycemic hyperinsulinemia augments amino acid uptake by human leg tissues during hyperaminoacidemia. Am J Physiol (1990) 259, E185–E194.Google ScholarPubMed
Bequette, BJ, Kyle, CE, Crompton, LA, Anderson, SE & Hanigan, MDProtein metabolism in lactating goats subjected to the insulin clamp. J Dairy Sci (2002) 85, 1546–1555.CrossRefGoogle Scholar
Biolo, G, Declan Fleming, RY & Wolfe, RRPhysiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest (1995) 95, 811–819.CrossRefGoogle ScholarPubMed
Calder, AG, Anderson, SE, Grant, I, McNurlan, MA & Garlick, PJThe determination of low phenylalanine enrichment (0·002–0·09 atom percent excess) after conversion to phenylethylamine, in relation to protein turnover studies by gas chromatography (electron ionisation) mass spectrometry. Rapid Commun Mass Spectrom (1992) 6, 421–424.CrossRefGoogle ScholarPubMed
Calder, AG & Smith, AStable isotope ratio analysis of leucine and ketoisocaproic acid in blood plasma by gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom (1988) 2, 14–16.CrossRefGoogle ScholarPubMed
Cole, NA, Purdy, CW & Hallford, DMInfluence of fasting and postfast diet energy level on feed intake, feeding pattern and blood variables of lambs. J Anim Sci (1988) 66, 798–805.CrossRefGoogle ScholarPubMed
Crompton, LA & Lomax, MAThe relationship between hindlimb muscle protein metabolism and growth hormone, insulin, cortisol and thyroxine in growing lambs. Proc Nutr Soc (1987) 46, 45A.Google Scholar
Crompton, LA & Lomax, MA (1993) Hindlimb protein turnover and muscle protein synthesis in lambs: a comparison of techniques. Br J Nutr 69, 345–348.CrossRefGoogle ScholarPubMed
Davis, TA, Fiorotto, ML, Beckett, PR, Burrin, DG, Reeds, PJ, Wray-Cahen, D & Nguyen, HVDifferential effects of insulin on peripheral and visceral tissue protein synthesis in neonatal pigs. Am J Physiol (2001) 280, E770–E779.Google ScholarPubMed
Dawson, JM, Buttery, PJ, Lammiman, MJ, Soar, JB & Essex, CPNutritional and endocrinological manipulation of lean deposition in forage-fed steers. Br J Nutr (1991) 66, 171–185.CrossRefGoogle ScholarPubMed
Douglas, RG, Gluckman, PD, Ball, K, Breier, B & Shaw, JHThe effects of infusion of insulin-like growth factor (IGF) I, IGF-II, and insulin on glucose and protein metabolism in fasted lambs. J Clin Invest (1991) 88, 614–622.CrossRefGoogle ScholarPubMed
Ferrando, AA, Williams, BD, Stuart, CA, Lane, HW & Wolfe, RROral branched-chain amino acids decrease whole-body proteolysis. J Parenter Enteral Nutr (1995) 19, 47–54.CrossRefGoogle ScholarPubMed
Fryburg, DA, Barret, EJ, Louard, RJ & Gelfand, RAEffect of starvation on human muscle protein metabolism and its response to insulin. Am J Physiol (1990) 259, E477–E482.Google ScholarPubMed
Fryburg, DA, Jahn, LA, Hill, SA, Oliveras, DM & Barrett, EJInsulin and insulin-like growth factor-I enhance human skeletal muscle protein anabolism during hyperaminoacidemia by differential mechanisms. J Clin Invest (1995) 96, 1722–1729.CrossRefGoogle Scholar
Garlick, PJ, Fern, M & Preedy, VRThe effect of insulin infusion and food intake on muscle protein synthesis in postabsorptive rats. Biochem J (1983) 210, 669–676.CrossRefGoogle ScholarPubMed
Garlick, PJ & Grant, IAmino acid infusion increases the sensitivity of muscle protein synthesis in vivo to insulin: effect of branched-chain amino acids. Biochem J (1988) 254, 579–584.CrossRefGoogle ScholarPubMed
Garlick, PJ, McNurlan, MA, Bark, T, Lang, CH & Gelato, MCHormonal regulation of protein metabolism in relation to nutrition and disease. J Nutr (1998) 128, 356S–359S.CrossRefGoogle ScholarPubMed
Garlick, PJ, Maltin, CA, Baillie, AGS, Delday, MI & Grubb, DAFiber-type composition of nine rat muscles. II Relationship to protein turnover. Am J Physiol (1989) 257, E828–E832.Google ScholarPubMed
Heinrikson, RL & Meredith, SCAmino acid analysis by reverse-phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate. Anal Biochem (1984) 136, 65–74.CrossRefGoogle ScholarPubMed
Heitmann, RN & Bergman, ENIntegration of amino acid metabolism in sheep: effects of fasting and acidosis. Am J Physiol (1980) 239, E248–E254.Google ScholarPubMed
Hillier, TA, Fryburg, DA, Jahn, LA & Barrett, EJExtreme hyperinsulinemia unmasks insulin's effect to stimulate protein synthesis in the human forearm. Am J Physiol (1998) 274, E1067–E1074.Google ScholarPubMed
Hoskin, SO, Savary, IC, Zuur, G & Lobley, GEEffect of feed intake on ovine hindlimb protein metabolism based on thirteen amino acids and arterio–venous techniques. Br J Nutr (2001) 86, 577–585.CrossRefGoogle ScholarPubMed
Hoskin, SO, Savary-Auzeloux, IC, Calder, AG, Zuur, G & Lobley, GEEffect of feed intake on amino acid transfers across ovine hindquarters. Br J Nutr (2003) 89, 167–179.CrossRefGoogle ScholarPubMed
Jepson, MM, Bates, PC & Millward, DJThe role of insulin and thyroid hormones in the regulation of muscle growth and protein turnover in response to dietary protein in the rat. Br J Nutr (1988) 59, 397–415.Google ScholarPubMed
Kriel, GV, Bryant, MJ & Lomax, MAEffect of dietary protein intake and intravenous glucose infusion on plasma concentrations of insulin-like growth factor-I in lambs. J Endocrinol (1992) 132, 195–199.CrossRefGoogle ScholarPubMed
Larbaud, D, Debras, E, Taillandier, D, Samuels, SE, Temparis, S, Champredon, C, Grizard, J & Attaix, DEuglycemic hyperinsulinemia and hyperaminoacidemia decrease skeletal muscle ubiquitin mRNA in goats. Am J Physiol (1996) 271, E505–E512.Google ScholarPubMed
Lobley, GE, Bremner, DM, Nieto, R, Obitsu, T, Hotson Moore, A & Brown, DSTransfers of N metabolites across the ovine liver in response to short-term infusions of an amino acid mixture into the mesenteric vein. Br J Nutr (1998) 80, 371–379.CrossRefGoogle Scholar
Lobley, GE, Connell, A, Milne, E, Buchan, V, Calder, AG, Anderson, SE & Vint, HMuscle protein synthesis in response to testosterone administration in wether lambs. Br J Nutr (1990) 64, 691–704.CrossRefGoogle ScholarPubMed
Lobley, GE, Harris, PM, Skene, PA, Brown, D, Milne, E, Calder, AG, Anderson, SE, Garlick, PJ, Nevison, I & Connell, AResponses in tissue protein synthesis to sub- and supra-maintenance intake in young growing sheep: comparison of large-dose and continuous-infusion techniques. Br J Nutr (1992) 68, 373–388.CrossRefGoogle ScholarPubMed
Lobley, GE, Sinclair, KD, Grant, CM, Miller, L, Mantle, D, Calder, AG, Warkup, CC & Maltin, CAThe effects of breed and level of nutrition on whole-body and muscle protein metabolism in pure-bred Aberdeen Angus and Charolais beef steers. Br J Nutr (2000) 84, 275–284.CrossRefGoogle ScholarPubMed
Lomax, MA & Baird, GDBlood flow and nutrient exchange across the liver and gut of the dairy cow. Effects of lactation and fasting. Br J Nutr (1983) 49, 481–496.CrossRefGoogle ScholarPubMed
McNurlan, MA & Garlick, PJProtein metabolism in the cancer patient. Biochimie (1994) 76, 713–717.Google Scholar
Maltin, CA, Lobley, CE, Grant, CM, Miller, LA, Kyle, DJ, Horgan, GW, Matthews, KR & Sinclair, KDFactors influencing beef eating quality – 2. Effects of nutritional regimen and genotype on muscle fibre characteristics. Anim Sci (2001) 72, 279–287.CrossRefGoogle Scholar
Midgley, AR, Rebau, RW & Niswender, GDRadioimmunoassays employing double antibody techniques. Acta Endocrinol (1969) 142, 247–254.Google ScholarPubMed
Millward, DJ, Fereday, A, Gibson, NR & Pacy, PJPost-prandial protein metabolism. Baillieres Best Pract Res Clin Endocrinol Metab (1996) 10, 533–549.CrossRefGoogle ScholarPubMed
Nicholas, GA, Lobley, GE & Harris, CIUse of the constant infusion technique for measuring rates of protein synthesis in the New Zealand White rabbit. Br J Nutr (1977) 38, 1–17.CrossRefGoogle ScholarPubMed
Oddy, VH, Lindsay, DB, Barker, PJ & Northrop, AJEffect of insulin on hindlimb and whole-body leucine and protein metabolism in fed and fasted sheep. Br J Nutr (1987) 58, 143–154.CrossRefGoogle Scholar
Papet, I, Glomot, F, Grizard, J & Arnal, MLeucine excess under conditions of low or compensated aminoacidemia does not change skeletal muscle and whole-body protein synthesis in suckling lambs during postprandial period. J Nutr (1992) 122, 2307–2315.CrossRefGoogle Scholar
Preedy, VR & Garlick, PJThe response of muscle protein synthesis to nutrient intake in postabsorptive rats: the role of insulin and amino acids. Biosci Rep (1986) 6, 177–183.CrossRefGoogle ScholarPubMed
Reecy, JM, Williams, JE, Kerley, MS, MacDonald, RS, Thornton, WH Jr & Davis, JLThe effect of postruminal amino acid flow on muscle cell proliferation and protein turnover. J Anim Sci (1996) 74, 2158–2169.CrossRefGoogle ScholarPubMed
Sandstrom, R, Svanberg, E, Hyltander, A, Haglind, E, Ohlsson, C, Zachrisson, H, Berglund, B, Lindholm, E, Brevinge, H & Lundholm, KThe effect of recombinant human IGF-I on protein metabolism in post-operative patients without nutrition compared to effects in experimental animals. Eur J Clin Invest (1995) 25, 784–792.CrossRefGoogle ScholarPubMed
Schaefer, AL, Davis, SR & Hughson, GAEstimation of tissue protein synthesis in sheep during sustained elevation of plasma leucine concentration by intravenous infusion. Br J Nutr (1986) 56, 281–288.CrossRefGoogle ScholarPubMed
Svanberg, E, Möller-Loswick, A-C, Matthews, DE, Körner, U, Andersson, M & Lunholm, KEffects of amino acids on synthesis and degradation of skeletal muscle proteins in humans. Am J Physiol (1996 a) 271, E718–E724.Google ScholarPubMed
Svanberg, E, Zachrisson, H, Ohlsson, C, Iresjö, B-M & Lundholm, KGRole of insulin and IGF-I in activation of muscle protein synthesis after oral feeding. Am J Physiol (1996 b) 270, E614–E620.Google ScholarPubMed
Tauveron, I, Larbaud, D, Champredon, C, Debras, E, Tesseraud, S, Bayle, G, Bonnet, Y, Thieblot, P & Grizard, JEffect of hyperinsulinemia and hyperaminoacidemia on muscle and liver protein synthesis in lactating goats. Am J Physiol (1994) 267, E877–E885.Google ScholarPubMed
Tesseraud, S, Grizard, J, Debras, E, Papet, I, Bonnet, Y, Bayle, G & Champredon, CLeucine metabolism in lactating and dry goats: effect of insulin and substrate availability. Am J Physiol (1993) 265, E402–E413.Google ScholarPubMed
Waalkes, TP & Udenfriend, SA fluorometric method for the estimation of tyrosine in plasma and tissues. J Lab Clin Med (1957) 50, 733–736.Google ScholarPubMed
Watt, PW, Corbett, ME & Rennie, MJStimulation of protein synthesis in pig skeletal muscle by infusion of amino acids during constant insulin availability. Am J Physiol (1992 a) 263, E453–E460.Google ScholarPubMed
Watt, PW, Hundal, HS, Downie, S & Rennie, MJGlutamine increase protein synthesis in heart, skeletal muscle, liver and gut of dexamethasone-treated rats. Proc Nutr Soc (1992 b) 51, 106AGoogle Scholar
Wester, TJ, Lobley, GE, Birnie, LM & Lomax, MAInsulin stimulates phenylalanine uptake across the hind limb in fed lambs. J Nutr (2000) 130, 608–611.CrossRefGoogle ScholarPubMed
Wray-Cahen, D, Metcalfe, JA, Backwell, FR, Bequette, BJ, Brown, DS, Sutton, JD & Lobley, GEHepatic response to increased exogenous supply of plasma amino acids by infusion into the mesentereic vein of Holstein–Friesian cows in late gestation. Br J Nutr (1997) 78, 913–930.CrossRefGoogle ScholarPubMed
Wray-Cahen, D, Nguyen, HV, Burrin, DG, Beckett, PR, Fiorotto, ML, Reeds, PR, Wester, TJ & Davis, TAResponse of skeletal muscle protein synthesis to insulin in suckling pigs decreases with development. Am J Physiol (1998) 275, E602–E609.Google ScholarPubMed