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Effect of tryptophan on the utilization of intra-duodenally infused labelled glucose in piglets given food at 1·35 times maintenance energy

Published online by Cambridge University Press:  18 August 2016

A. A. Ponter ,
J. J. Matte  and
B. Sève
A. A. Ponter
Affiliation:
Institut National de la Recherche Agronomique, Unité Mixte de Recherches sur le Veau et le Porc, 35590 Saint-Gilles, France Ecole Nationale Vétérinaire d’Alfort, Unité Biologie de la Reproduction, 7, Avenue du Général-de-Gaulle, 94704 Maisons-Alfort, France
J. J. Matte
Affiliation:
Research Centre, Agriculture and Agri-Food Canada, PO Box 90, Lennoxville, Québec J1 M 1Z3, Canada
B. Sève
Affiliation:
Institut National de la Recherche Agronomique, Unité Mixte de Recherches sur le Veau et le Porc, 35590 Saint-Gilles, France
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Abstract

Two experiments were conducted. The first, studied the chronic effect of tryptophan (trp) on glucose disposal and the second, the acute effect of trp on glucose disposal. In experiment 1, 12 piglets were allocated either to a trp deficient diet (T0) or a trp adequate diet (T1). After 14 days a 240-min intraduodenal infusion of glucose (130 µmol/kg per min) associated with D-(U-14C) glucose (1·18 kBq/kg per min) and an intrajugular infusion of D-(6-3H) glucose (1·85 kBq/kg per min) were started. In experiment 2, 18 piglets were given a trp adequate diet (T1) for 14 days. The piglets were then divided into two groups and received an intraduodenal infusion of either glucose (130 µmol/kg per min) or glucose plus trp (0·53 µmol/kg per min) for 240 min. At the same time an intrajugular infusion of D-(U-14C)glucose (1·48 kBq/kg per min) and D-(6-3H)glucose (2·59 kBq/kg per min) was given to all piglets. Blood samples were taken at regular intervals during the infusions for the measurement of plasma concentrations of insulin, glucose, lactate and blood specific activities of 14C-glucose, 14C-lactate, 3H-glucose and 3H-lactate. At the end of the infusion, samples were taken for the measurement of the accumulation of 14C and 3H in glycogen. In experiment 1, plasma insulin concentrations were higher in the T0 compared with the T1 group (at 30 min respectively, 837·7 (s.e.56·6) v. 404·9 (s.e.56·6) pmol/l, P < 0·001). Glucose concentrations were also higher in T0 compared with T1 (at 30 min respectively, 10·9 (s.e. 0·54) v. 9·3 (s.e. 0·54) mmol/l, P < 0·05). Glucose flux was unaffected by trp in both experiments. The accumulation of labelled glucose into liver and carcass glycogen was not affected by trp. The route of administration of glucose label had a significant effect on the percentage of label accumulated in liver glycogen. When both 14C and 3H were infused into the jugular vein there was no difference in the accumulation of the two tracers in liver glycogen (22·7 v. 21·8% of that infused, P > 0·05, respectively). However, when 14C was infused into the duodenum and 3H into the jugular vein, accumulation into liver glycogen was higher for 14C compared with 3H (19·9 v. 15·6%, P < 0·001, respectively). In conclusion, trp does not appear to influence glucose disposal measured at the end of a 240 min intraduodenal glucose infusion. Contrary to results published from experiments with rats the indirect pathway for glycogen synthesis (glucose→lactate→glycogen) does not appear to occur in underfed piglets.

Keywords

glucoseinsulinpigletstryptophan.
Type
Growth, development and meat science
Information
Animal Science , Volume 72 , Issue 2 , April 2001 , pp. 315 - 324
Copyright
Copyright © British Society of Animal Science 2001

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References

Chap, Z., Ishida, T., Chou, J., Lewis, R., Hartley, C., Entman, M. and Field, J. B. 1985. Effects of atropine and gastric inhibitory polypeptide on hepatic glucose uptake and insulin extraction in conscious dogs. Journal of Clinical Investigation 76: 1174–1181.CrossRefGoogle ScholarPubMed
Cherbuy, C., Darcy-Virllon, B., Posho, L., Vaugelade, P., Morel, M. T., Bernard, F., Leturque, A., Penicaud, L. and P. H., Duée 1997. GLUT2 and hexokinase control proximodistal gradient of intestinal glucose metabolism in the newborn pig. American Journal of Physiology 272: G1530–G1539.Google Scholar
Cortamira, N. O., B., Sève, Lebreton, Y. and Ganier, P. 1991. Effect of tryptophan on muscle, liver and whole-body protein synthesis in weaned piglets: relationship to plasma insulin. British Journal of Nutrition 66: 423–435.CrossRefGoogle ScholarPubMed
Cote, P. J., Wangsness, P. J., Varela-Alvarez, H., Griel, L. and Kavanaugh, J. F. 1982. Glucose turnover in fast-growing, lean and in slow-growing, obese swine. Journal of Animal Science 5: 89–94.Google Scholar
Dunn, A., Katz, J., Golden, S. and Chenoweth, M. 1976. Estimation of glucose turnover and recycling in rabbits using various [3H, 14C]glucose labels. American Journal of Physiology 230: 1159–1162.Google Scholar
Ferrannini, E., Bjorkman, O., Reichard, G. A., Pilo, A., Olsson, M., Wahren, J. and DeFronzo, R. A. 1985. The disposal of an oral glucose load in healthy subjects: a quantative study. Diabetes 34: 580–588.Google Scholar
Ferré, P., Pegorier, J. P., Marliss, E. B. and Girard, J. R. 1978. Influence of exogenous fat and gluconeogenic substrates on glucose homeostasis in the newborn rat. American Journal of Physiology 234: E129–E136.Google ScholarPubMed
Hess, V., Ponter, A. A., Matte, J. J. and Ferré Sève, B. 1997. Chronic and acute effects of tryptophan on metabolic responses to parenteral glucose infusion in piglets. Proceedings of the seventh symposium on digestive physiology in pigs, 26-28 May 1997, St. -Malo, France, pp. 325–329.Google Scholar
Huang, M. and Veech, R. L. 1988. Role of direct and indirect pathways for glycogen synthesis in rat liver in the postprandial state. Journal of Clinical Investigation 81: 872–878.Google Scholar
Katz, J., Lee, W. -N. P. Wals, P. A. and Bergner, E. A. 1989. Studies of glycogen synthesis and the Krebs cycle by mass isotopomer analysis with [U-13C]glucose in rats. Journal of Biological Chemistry 264: 12994–13001.Google Scholar
Katz, J. and Tayek, J. A. 1998. Gluconeogenesis and the Cori cycle in 12-, 20-, and 40-hour-fasted humans. American Journal of Physiology 275: E537–E542.Google Scholar
Katz, J., Wals, P. A. and Lee, W.-N. P. 1991. Determination of pathways of glycogen synthesis and the dilution of the three-carbon pool with [U-13C]glucose. Proceedings of the National Academy of Sciences of the United States of America 88: 2103–2107.Google Scholar
Katz, J., Wals, P. A. and Lee, W.-N. P. 1993. Isotopomer studies of gluconeogenesis and the Krebs cycle with [U-13C] lactate. Journal of Biological Chemistry 268: 25509–25521.Google Scholar
Koopmans, S. J., Mandarino, L. and DeFronzo, R. A. 1998. Time course of insulin action on tissue-specific intracellular glucose metabolism in normal rats. American Journal of Physiology 274: E642–E650.Google Scholar
Landau, B. R., Fernandez, C. A., Previs, S. F., Ekberg, K., Chandramouli, V., Wahren, J., Kalhan, S. C. and Brunengraber, H. A. 1995a. Limitation in the use of mass isotopomer distributions to measure gluconeogenesis in fasting humans. American Journal of Physiology 269: E18–E26. Google Scholar
Landau, B. R., Wahren, J., Chandramouli, V., Schulman, W. C. and Ekberg, K. 1995b. Use of 2H2O for estimating rates of gluconeogenesis. Journal of Clinical Investigation 95: 172–178.Google Scholar
Littell, R. C., Henry, P. R. and Ammerman, C. B. 1998. Statistical analysis of repeated measures data using SAS procedures. Journal of Animal Science 76: 1216–1231.Google Scholar
Livesey, G., Wilson, P. D., Dainty, J. R., Brown, J. C., Faulks, R. M., Roe, M. A., Newman, T. A., Eagles, J., Mellon, F. A. and Greenwood, R. H. 1998. Simultaneous time-varying systemic appearance of oral and hepatic glucose in adults monitored with stable isotopes. American Journal of Physiology 275: E717–E728.Google Scholar
McPhate, G.F. 1986. The effect of ingestion of single amino acids on gluco-regulatory hormones in man. M.Sc. thesis, University of Surrey, Surrey, UK.Google Scholar
Magnusson, I., Rothman, D. L., Jucker, B., Cline, G. W., Shulman, R. G. and Shulman, G. I. 1994. Liver glycogen turnover in fed and fasted humans. American Journal of Physiology 266: E796–E803.Google Scholar
Matte, J. J., Ponter, A. A. and B., Sève 1997. Effects of chronic parenteral pyridoxine and acute enteric tryptophan on pyridoxine status, glycemia and insulinemia stimulated by enteric glucose in weanling piglets. Canadian Journal of Animal Science 77: 663–668.CrossRefGoogle Scholar
Mitrakou, A., Jones, R., Okuda, Y., Pena, J., Nurjhan, N., Field, J. B. and Gerich, J. E. 1991. Pathway of carbon sources for hepatic glycogen repletion in dogs. American Journal of Physiology 260: E194–E202.Google ScholarPubMed
Moore, M. C., Pagliassoti, M. J., Swift, L. L., Asher, J., Murrel, J., Neal, D. and Cherrington, A. D. 1994. Disposal of a mixed meal by the conscious dog. American Journal of Physiology 266: E666–E675. Google Scholar
Morgan, L. M. 1992. Insulin secretion and the entero-insular axis. In Nutrient regulation of insulin secretion (ed. Flatt, P. R.), pp. 1–22. Portland Press Research Monograph, London and Chapel Hill, Great Britain.Google Scholar
Neese, R. A., Schwarz, J. M., Faix, D., Turner, S., Letscher, A., Vu, D. and Hellerstein, M. K. 1995. Gluconeogenesis and intrahepatic triose phosphate flux in response to fasting or substrate loads. Journal of Biological Chemistry 270: 4452–4463.Google Scholar
Newgard, C. B., Hirsch, L. J., Foster, D. H. and McGarry, J. D. 1983. Studies on the mechanism by which exogenous glucose is converted into liver glycogen in the rat. Journal of Biological Chemistry 258: 8046–8052.Google Scholar
Newgard, C. B., Moore, S. V., Foster, D. W. and McGarry, J. D. 1984. Efficient hepatic glycogen synthesis in refeeding rats requires continued carbon flow through the gluconeogenic pathway. Journal of Biological Chemistry 259: 6958–6963.Google Scholar
Pervis, S. F., Fernandez, C. A., Yang, D., Soloiev, M. V., David, F. and Brunengraber, H. 1995. Limitations of the mass isotopomer distribution analysis of glucose to study gluconeogenesis. Journal of Biological Chemistry 270: 19806–19815.Google Scholar
Ponter, A. A., Cortamira, N. O., B., Sève, Salter, D. N. and Morgan, L. M. 1994a. The effects of energy source and tryptophan on the rate of protein synthesis and on hormones of the entero-insular axis in the piglet. British Journal of Nutrition 71: 661–674.Google Scholar
Ponter, A. A., B., Sève and Morgan, L. M. 1994b. Intragastric tryptophan reduces glycemia after glucose, possibly via glucose-mediated insulinotropic polypeptide, in early-weaned piglets. Journal of Nutrition 124: 259–267.Google Scholar
Radziuk, J., McDonald, T. J., Rubenstein, D. and Dupré, J. 1978. Initial splanchinc extraction of ingested glucose in normal man. Metabolism, Clinical, Experimental 27: 657–669.Google Scholar
Rayner, D. V. 1991. The relationship between glucose absorption and insulin secretion and the migrating myoelectric complex in the pig. Experimental Physiology 76: 67–76.Google Scholar
Sawadogo, M. L., Piva, A., Panciroli, A., Meola, E., Mordenti, A. and B., Sève 1996. Efficacité d’utilisation du tryptophane cristallisé, sous forme libre ou protégée, pour le dépôt protéique chez le porcelet. Journées de la Recherche Porcine en France 28: 399–406.Google Scholar
Schulman, G. I., Rossetti, L., Rothman, D. L., Blair, J. B. and Smith, D. 1987. Quantitative analysis of glycogen repletion by nuclear magnetic resonance spectroscopy in conscious rat. Journal of Clinical Investigation 80: 387–393.CrossRefGoogle Scholar
Sève, B. and Ballèvre, O. 1991. Approches métaboliques du besoin en acides aminés chez le porc en croissance. Journées de la Recherche Porcine en France 23: 119–126.Google Scholar
Sève, B., Ronat, P., Hess, V., Matte, J. J. and Ponter, A. A. 1997. Evidence for the entero-insular axis in weanling piglets. Proceedings of the seventh symposium on digestive physiology in pigs, 26-28 May 1997, St.-Malo, France EAAP publication no. 88, pp. 270–273.Google Scholar
Statistical Analysis Systems Institute. 1996. SAS/STAT user’s guide, release 6·12 edition. SAS Institute Inc., Cary, NC. Google Scholar
Tayek, J. A. and Katz, J. 1996. Glucose production, recycling, and gluconeogenesis in normals and diabetics: a mass isotopomer [U-13C]glucose study. American Journal of Physiology 270: E709–E717.Google Scholar
Taylor, R., Magnusson, I., Rothman, D. L., Cline, G. W., Caumo, A., Cobelli, C. and Shulman, G. I. 1996. Direct assessment of liver glycogen storage by 13C nuclear magnetic resonance spectroscopy and regulation of glucose homeostasis after a mixed meal in normal subjects. Journal of Clinical Investigation 97: 126–132.Google Scholar
Tserng, K. and Kalhan, S. C. 1983. Estimation of glucose carbon recycling and glucose turnover with [U-13C]glucose. American Journal of Physiology 245: E476–E482.Google Scholar
Tsiolakis, D. and Marks, V. 1984. The differential effect of intragastric and intravenous tryptophan on plasma glucose, insulin, glucagon, GLI and GIP in the fasted rat. Hormone and Metabolic Research 16: 226–229.Google Scholar
Yip, R. G. and Wolfe, M. M. 2000. GIP biology and fat metabolism. Life Science 66: 91–103.Google Scholar