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Oxidation of essential amino acids by the ovine gastrointestinal tract

Published online by Cambridge University Press:  09 March 2007

Gerald E. Lobley ,
Xiangzhen Shen ,
Guowei Le ,
David M. Bremner ,
Eric Milne ,
A. Graham Calder ,
Susan E. Anderson  and
Ngaire Dennison
Gerald E. Lobley*
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Xiangzhen Shen
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Guowei Le
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
David M. Bremner
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Eric Milne
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
A. Graham Calder
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Susan E. Anderson
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Ngaire Dennison
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding Author: Dr G. E. Lobley, fax +44 1224 716629, email g.lobley@rowett.ac.uk
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Abstract

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It is not known if the ruminant animal gastrointestinal tract (GIT) can oxidise essential amino acids (AA) other than leucine. Therefore, the oxidation of four essential AA (leucine, lysine, methionine and phenylalanine), supplied systemically as labelled 1-13C forms, was monitored across the mesenteric-drained viscera (MDV; small intestine) and portal-drained viscera (PDV; total GIT), as part of a 4×4 Latin square design, in four wether sheep (35–45 kg) fed at 1·4 × maintenance. Oxidation was assessed primarily by appearance of 13CO2, corrected for sequestration of [13C]bicarbonate. The GIT contributed 25 % (P<0·001) and 10 % (P<0·05) towards whole-body AA oxidation for leucine and methionine respectively. This reduced net appearance across the PDV by 23 and 11 % respectively. The contribution of MDV metabolism to total PDV oxidation was 40 % for leucine and 60 % for methionine. There was no catabolism of systemic lysine or phenylalanine across the GIT. Production and exchange of secondary metabolites (e.g. 4-methyl-2-oxo-pentanoate, homocysteine, 2-aminoadipate) across the GIT was also limited. Less AA appeared across the PDV than MDV (P<0·001), indicative of use by tissues such as the forestomach, large intestine, spleen and pancreas. The PDV: MDV net appearance ratios varied (P<0·001) between AA, e.g. phenylalanine (0·81), lysine (0·71), methionine (0·67), leucine (0·56), histidine (0·71), threonine (0·63) and tryptophan (0·48). These differences probably reflect incomplete re-absorption of endogenous secretions and, together with the varied oxidative losses measured, will alter the pattern of AA net supply to the rest of the animal.

Keywords

Gastrointestinal tractOxidationLeucineMethionineLysinePhenylalanineSheep
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue 5 , May 2003 , pp. 617 - 629
Copyright
Copyright © The Nutrition Society 2003

References

Attaix, D & Meslin, JC (1991) Changes in small intestinal mucosa morphology and cell renewal in suckling, prolonged-suckling, and weaned lambs. American Journal of Physiology 261 R811–R818.Google ScholarPubMed
Ball, RO (2002) Definition of the amino acid requirements in pigs: partitioning between gut and muscle. In Amino Acids: Meat, Milk and More!, pp. 17–25 [Lapierre, H and Ouellet, DR, editors]. Quebec, Canda: Publié par la Comité organisateur du Congrés CSAS 2002.Google Scholar
Barazzoni, R, Meek, SE, Ekberg, K, Wahren, J & Nair, KS (1999) Arterial KIC as marker of liver and muscle intracellular leucine pools in healthy and type 1 diabetic humans. American Journal of Physiology 277 E238–E244.Google ScholarPubMed
Bennet, WM, O'Keefe, SJ & Haymond, MW (1993) Comparison of precursor pools with leucine, alpha-ketoisocaproate, and phenylalanine tracers used to measure splanchnic protein synthesis in man. Metabolism 42 691–695.CrossRefGoogle ScholarPubMed
Bequette, BJ, Backwell, FR, Macrae, JC, Lobley, GE, Crompton, LA, Metcalf, JA & Sutton, JD (1996) Effect of intravenous amino acid infusion on leucine oxidation across the mammary gland of the lactating goat. Journal of Dairy Science 79 2217–2224.CrossRefGoogle ScholarPubMed
Berthiaume, R, Dubreuil, P, Stevenson, M, Mcbride, BW & Lapierre, H (2001) Intestinal disappearance and mesenteric and portal appearance of amino acids in dairy cows fed ruminally protected methionine. Journal of Dairy Science 84 194–203.CrossRefGoogle ScholarPubMed
Biolo, G & Tessari, P (1997) Splanchnic versus whole-body production of alpha-ketoisocaproate from leucine in the fed state. Metabolism 46 164–167.CrossRefGoogle ScholarPubMed
Burrin, DG, Ferrell, CL, Britton, RA & Bauer, M (1990) Level of nutrition and visceral organ size and metabolic activity in sheep. British Journal of Nutrition 64 439–448.CrossRefGoogle ScholarPubMed
Burrin, DG, Ferrell, CL, Eisemann, JH, Britton, RA & Nienaber, JA (1989) Effect of level of nutrition on splanchnic blood flow and oxygen consumption in sheep. British Journal of Nutrition 62 23–34.CrossRefGoogle ScholarPubMed
Burrin, DG, Stoll, B, van Goudoever, JB & Reeds, PJ (2001) Nutrient requirements for intestinal metabolism and growth in the neonatal pig. In Digestive Physiology of Pigs, pp. 75–88 [Lindberg, JE and Ogle, B, editors]. New York: CAB International.Google Scholar
Bush, JA, Burrin, DG, Suryawan, A, O'Connor, PM, Nguyen, HV, Reeds, PJ, Steele, NC, van Goudoever, JB & Davis, TA (2003) Somatotropin-induced protein anabolism in hindquarters and portal-drained viscera of growing pigs. American Journal of Physiology 284 E302–E312.Google ScholarPubMed
Calder, AG, Garden, KE, Anderson, SE & Lobley, GE (1999) Quantitation of blood and plasma amino acids using isotope dilution electron impact gas chromatography/mass spectrometry with U-(13)C amino acids as internal standards. Rapid Communications in Mass Spectrometry 13 2080–2083.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Calder, AG & Smith, A (1988) Stable isotope ratio analysis of leucine and ketoisocaproic acid in blood plasma by gas chromatography/mass spectrometry. Use of tertiary butyldimethylsilyl derivatives. Rapid Communications in Mass Spectrometry 2 14–16.CrossRefGoogle ScholarPubMed
Campbell, IM (1974) Incorporation and dilution values – their calculation in mass spectrally stable isotope labeling experiments. Bioorganic Chemistry 3 386–397.CrossRefGoogle Scholar
Cheng, KN, Dworzak, F, Ford, GC, Rennie, MJ & Halliday, D (1985) Direct determination of leucine metabolism and protein break-down in humans using l-[1-13C, 15N]-leucine and the forearm model. European Journal of Clinical Investigation 15 349–354.CrossRefGoogle Scholar
Chinkes, D, Klein, S, Zhang, XJ & Wolfe, RR (1996) Infusion of labeled KIC is more accurate than labeled leucine to determine human muscle protein synthesis. American Journal of Physiology 33 E67–E71.Google Scholar
de Lange, CF, Sauer, WC, Souffrant, WB & Lien, KA (1992) 15N-leucine and 15N-isoleucine isotope dilution techniques versus the 15N-isotope dilution technique for determining the recovery of endogenous protein and amino acids in digesta collected from the distal ileum in pigs. Journal of Animal Science 70 1848–1856.CrossRefGoogle ScholarPubMed
Gate, JJ, Parker, DS & Lobley, GE (1999) The metabolic fate of the amido-N group of glutamine in the tissues of the gastrointestinal tract in 24 h-fasted sheep. British Journal of Nutrition 81 297–306.CrossRefGoogle ScholarPubMed
Goodwin, GW, Gibboney, W, Paxton, R, Harris, RA & Lemons, JA (1987) Activities of branched-chain amino acid aminotransferase and branched-chain 2-oxo acid dehydrogenase complex in tissues of maternal and fetal sheep. Biochemical Journal 242 305–308.CrossRefGoogle ScholarPubMed
Gresham, JD, Okamura, K, Williams, PE, Jabbour, K & Flakoll, PJ (2000) Gastrointestinal tract, hepatic, hindlimb, and renal recovery of CO2 in vivo. Journal of Applied Physiology 89 2000–2006.CrossRefGoogle ScholarPubMed
Kimball, SR & Jefferson, LS (2002) Control of protein synthesis by amino acid availability. Current Opinion in Clinical Nutrition and Metabolic Care 5 63–67.CrossRefGoogle ScholarPubMed
Lapierre, H, Bernier, JF, Dubreuil, P, Reynolds, CK, Farmer, C, Ouellet, DR & Lobley, GE (1999) The effect of intake on protein metabolism across splanchnic tissues in growing beef steers. British Journal of Nutrition 81 457–466.CrossRefGoogle ScholarPubMed
Lapierre, H, Blouin, JP, Bernier, JF, Reynolds, CK, Dubreuil, P & Lobley, GE (2002) Effect of supply of metabolizable protein on whole body and splanchnic leucine metabolism in lactating dairy cows. Journal of Dairy Science 85 2631–2641.CrossRefGoogle ScholarPubMed
Lapierre, H & Lobley, GE (2001) Nitrogen recycling in the ruminant: a review. Journal of Dairy Science 84 (suppl.), E223–E236.CrossRefGoogle Scholar
Le Floc'h, N, Thibault, JN & Seve, B (1997) Tissue localization of threonine oxidation in pigs. British Journal of Nutrition 77 593–603.Google ScholarPubMed
Leijssen, DPC & Elia, M (1996) Recovery of (CO2)-C-13 and (CO2)-C-14 in human bicarbonate studies: A critical review with original data. Clinical Science 91 665–677.CrossRefGoogle Scholar
Lien, KA, Sauer, WC & Fenton, M (1997) Mucin output in ileal digesta of pigs fed a protein-free diet. Zeitschrift fur Ernahrungswissenschaft 36 182–190.CrossRefGoogle ScholarPubMed
Lobley, GE (1998) Nutritional and hormonal control of muscle and peripheral tissue metabolism in farm species. Livestock Production Science 56 91–114.Google Scholar
Lobley, GE, Bremner, DM & Brown, DS (2001) Response in hepatic removal of amino acids by the sheep to short-term infusions of varied amounts of an amino acid mixture into the mesenteric vein. British Journal of Nutrition 85 689–698.CrossRefGoogle ScholarPubMed
Lobley, GE, Connell, A, Lomax, MA, Brown, DS, Milne, E, Calder, AG & Farningham, DA (1995) Hepatic detoxification of ammonia in the ovine liver: possible consequences for amino acid catabolism. British Journal of Nutrition 73 667–685.CrossRefGoogle ScholarPubMed
Lobley, GE, Connell, A, Milne, E, Newman, AM & Ewing, TA (1994) Protein synthesis in splanchnic tissues of sheep offered two levels of intake. British Journal of Nutrition 71 3–12.CrossRefGoogle ScholarPubMed
Lobley, GE, Connell, A & Revell, D (1996 a) The importance of transmethylation reactions to methionine metabolism in sheep: effects of supplementation with creatine and choline. British Journal of Nutrition 75 47–56.CrossRefGoogle ScholarPubMed
Lobley, GE, Weijs, PJ, Connell, A, Calder, AG, Brown, DS & Milne, E (1996 b) The fate of absorbed and exogenous ammonia as influenced by forage or forage–concentrate diets in growing sheep. British Journal of Nutrition 76 231–248.CrossRefGoogle ScholarPubMed
Mabjeesh, SJ, Kyle, CE, Macrae, JC & Bequette, BJ (2000) Lysine metabolism by the mammary gland of lactating goats at two stages of lactation. Journal of Dairy Science 83 996–1003.CrossRefGoogle ScholarPubMed
MacRae, JC, Bruce, LA, Brown, DS & Calder, AG (1997 a) Amino acid use by the gastrointestinal tract of sheep given lucerne forage. American Journal of Physiology 273 G1200–G1207.Google ScholarPubMed
MacRae, JC, Bruce, LA, Brown, DS, Farningham, DA & Franklin, M (1997 b) Absorption of amino acids from the intestine and their net flux across the mesenteric- and portal-drained viscera of lambs. Journal of Animal Science 75 3307–3314.CrossRefGoogle ScholarPubMed
MacRae, JC, Bruce, LA & Yu, F (1999) The effect of flavomycin on gastrointestinal leucine metabolism and liveweight gain in lambs. South African Journal of Animal Science 29 (ISRP), 243–244.Google Scholar
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 57 237–245.Google Scholar
Matthews, DE, Schwarz, HP, Yang, RD, Motil, KJ, Young, VR & Bier, DM (1982) Relationship of plasma leucine and alpha-ketoisocaproate during a l-[1-13C]leucine infusion in man: a method for measuring human intracellular leucine tracer enrichment. Metabolism 31 1105–1112.CrossRefGoogle Scholar
Mukkur, TK, Watson, DL, Saini, KS & Lascelles, AK (1985) Purification and characterization of goblet-cell mucin of high Mr from the small intestine of sheep. Biochemical Journal 229 419–428.CrossRefGoogle ScholarPubMed
National Research Council (2001) Protein and amino acids. In Nutrient Requirements of Dairy Cattle, pp. 43–104Washington, DC: National Academy of Sciences.Google Scholar
Ouellet, DR, Demers, M, Zuur, G, Lobley, GE, Seoane, JR, Nolan, JV & Lapierre, H (2002) Effect of dietary fiber on endogenous nitrogen flows in lactating dairy cows. Journal of Dairy Science 85 3013–3025.Google Scholar
Pape, I, Lezebot, N, Barre, F, Arnal, M & Harper, AE (1988) Influence of dietary leucine content on the activities of branched-chain amino acid aminotransferase (EC 2.6.1.42) and branched-chain alpha-keto acid dehydrogenase (EC 1.2.4.4) complex in tissues of preruminant lambs. British Journal of Nutrition 59 475–483.CrossRefGoogle Scholar
Pell, JM, Caldarone, EM & Bergman, EN (1986) Leucine and alpha-ketoisocaproate metabolism and interconversions in fed and fasted sheep. Metabolism 35 1005–1016.Google Scholar
Ram, L, Nieto, R & Lobley, GE (1999) Tissue sequestration of C-labelled bicarbonate [HCO3-] in fed and fasted young sheep. Comparative Biochemistry and Physiology A 122 323–330.CrossRefGoogle ScholarPubMed
Reeds, PJ & Burrin, DG (2001) Glutamine and the bowel. Journal of Nutrition 131 2505S–2508S.CrossRefGoogle Scholar
Reeds, PJ, Burrin, DG, Stoll, B & Jahoor, F (2000) Intestinal glutamate metabolism. Journal of Nutrition 130 978S–982S.CrossRefGoogle ScholarPubMed
Rerat, A, Simoes-Nunes, C, Mendy, F, Vaissade, P & Vaugelade, P (1992) Splanchnic fluxes of amino acids after duodenal infusion of carbohydrate solutions containing free amino acids or oligopeptides in the non-anaesthetized pig. British Journal of Nutrition 68 111–138.Google Scholar
Sanchez, M, El Khoury, AE, Castillo, L, Chapman, TE, Filho, AB, Beaumier, L & Young, VR (1996) Twenty-four-hour intravenous and oral tracer studies with l-[1-13C]phenylalanine and l-[3,3-2H2]tyrosine at a tyrosine-free, generous phenylalanine intake in adults. American Journal of Clinical Nutrition 63 532–545.CrossRefGoogle Scholar
Sarraseca, A, Milne, E, Metcalf, MJ & Lobley, GE (1998) Urea recycling in sheep: effects of intake. British Journal of Nutrition 79 79–88.CrossRefGoogle ScholarPubMed
Seal, CJ & Parker, DS (1996) Effect of intraruminal propionic acid infusion on metabolism of mesenteric- and portal-drained viscera in growing steers fed a forage diet: II. Ammonia, urea, amino acids, and peptides. Journal of Animal Science 74 245–256.Google Scholar
Siddons, RC, Nolan, JV, Beever, DE & MacRae, JC (1985) Nitrogen digestion and metabolism in sheep consuming diets containing contrasting forms and levels of N. British Journal of Nutrition 54 175–187.Google Scholar
Stegink, LD & den Besten, L (1972) Synthesis of cysteine from methionine in normal adult subjects: effect of alimentation. Science 178 514–516.CrossRefGoogle ScholarPubMed
Stoll, B, Henry, J, Reeds, PJ, Yu, H, Jahoor, F & Burrin, DG (1998) Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein-fed piglets. Journal of Nutrition 128 606–614.CrossRefGoogle ScholarPubMed
Tagari, H & Bergman, EN (1978) Intestinal disappearance and portal blood appearance of amino acids in sheep. Journal of Nutrition 108 790–803.CrossRefGoogle ScholarPubMed
van der Schoor, SRD, van Goudoever, JB, Stoll, B, Henry, JF, Rosenberger, JR, Burrin, DG & Reeds, PJ (2001) The pattern of intestinal substrate oxidation is altered by protein restriction in pigs. Gastroenterology 121 1167–1175.CrossRefGoogle ScholarPubMed
van Goudoever, JB, Stoll, B, Henry, JF, Burrin, DG & Reeds, PJ (2000) Adaptive regulation of intestinal lysine metabolism. Proceedings of the National Academy of Sciences USA 97 11620–11625.CrossRefGoogle ScholarPubMed
Wajed, SA, Laird, PW & DeMeester, TR (2001) DNA methylation: an alternative pathway to cancer. Annals of Surgery 234 10–20.Google Scholar
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 E453–E460.Google ScholarPubMed
Windmueller, HG & Spaeth, AE (1980) Respiratory fuels and nitrogen metabolism in vivo in small intestine of fed rats. Quantitative importance of glutamine, glutamate, and aspartate. Journal of Biological Chemistry 255 107–112.Google Scholar
Wolff, JE & Bergman, EN (1972) Metabolism and interconversions of five plasma amino acids by tissues of the sheep. American Journal of Physiology 223 447–454.Google Scholar
Yu, F, Bruce, LA, Calder, AG, Milne, E, Coop, RL, Jackson, F, Horgan, GW & MacRae, JC (2000) Subclinical infection with the nematode Trichostrongylus colubriformis increases gastrointestinal tract leucine metabolism and reduces availability of leucine for other tissues. Journal of Animal Science 78 380–390.Google Scholar