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The metabolic fate of the amido-N group of glutamine in the tissues of the gastrointestinal tract in 24 h-fasted sheep

Published online by Cambridge University Press:  09 March 2007

J. J. Gate ,
D. S. Parker  and
G. E. Lobley
J. J. Gate
Affiliation:
Department of Biological and Nutritional Sciences Faculty of Agriculture and Biological Sciences, University of Newcastle, Newcastle-upon-Tyne, NE1 7RU, UK
D. S. Parker
Affiliation:
Department of Biological and Nutritional Sciences Faculty of Agriculture and Biological Sciences, University of Newcastle, Newcastle-upon-Tyne, NE1 7RU, UK
G. E. Lobley*
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen, AB21 9SB, UK
*
‡Corresponding author: Dr G. E. Lobley, fax +44 (0) 1224 716629, email [email protected]
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Abstract

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Whole-body and gastrointestinal tract (GIT) metabolism of [5-15N]glutamine were monitored in lambs (33 kg live weight) fasted for 24 h. Animals were previously prepared with vascular catheters across the mesenteric-(MDV) and portal-drained viscera (PDV) to permit quantification of mass and isotopic transfers of metabolites by arterio-venous difference. Continuous infusions of [5-15N]glutamine into the jugular vein were conducted for 10 h and integrated blood samples withdrawn over 75 min intervals for the last 5 h of infusion. The lambs were then killed and portions from various tissues of the digestive tract and other body organs removed for determination of 15N enrichment in RNA, DNA and protein (the latter obtained by difference using total acid-precipitable N). Whole-body glutamine flux was 108 μmol/min of which 23 and 47 % could be attributed to MDV and PDV metabolism (P < 0·001) respectively. There was a small net production of glutamine across the MDV. GIT blood-flows and NH3 production were partitioned 3:2 between MDV and non-MDV components. Less than 5 % of the NH3 produced was derived from the amido-N of glutamine, while across the small intestine (MDV) 26 % of the glutamine flux was converted to NH3, compared with 18 % for non-MDV transfers. The 15N enrichments in protein were of the order jejunum > duodenum > ileum with mucosal cells more labelled than serosal (P < 0·001). Lesser enrichments were observed for other GIT tissues (abomasum > caecum > rumen) while liver and lymph were comparable with the abomasum; kidney, spleen and muscle were lower still (P < 0·05). Enrichments of RNA were similar to that of protein and followed the same pattern, except for higher relative values for liver, spleen and lymphoid tissue. The lowest enrichments were observed for DNA, but again the pattern order was similar except for increased label in lymph, caecum and the spleen. For the MDV there was reasonable agreement between 15N-disappearance as glutamine and appearance in NH3 (24 %), protein (81 %), RNA (3·6 %) and DNA (2·1 %). For the total PDV there was a shortfall (−12 %), however, which may be due to losses in lumen components. These results show the importance of the GIT as a contributor to total glutamine plasma flux, but indicate a lesser reliance on glutamine metabolism by the digestive tract of the ruminant compared with observations from non-ruminants.

Keywords

Glutamine15N-kineticsSheepGastrointestinal tract
Type
Research Article
Information
British Journal of Nutrition , Volume 81 , Issue 4 , April 1999 , pp. 297 - 306
Copyright
Copyright © The Nutrition Society 1999

References

Aurousseau, B, Thivend, P & Vermorel, M (1984 a) Influence du remplacement d'une partie du suif d'un aliment par de la tricaproïne ou de la tricapryline en association à de l'huile de coprah sur la croissance du jeune veau préruminant (Influence of substituting part of the milk replacer tallow by tricaproin or tricaprylin combined with coconut oil on the growth of young preruminant calves). Annales de Zootechniues 33, 219–234.CrossRefGoogle Scholar
Aurousseau, B, Vermorel, M & Bouvier, JC (1983) Influence du remplacement d'une partie du suif d'un aliment d'allaitement par de la tricaproïne ou de l'huile de coprah, sur l'utilisation de l'énergie et de l'azote par le veau préruminant; influence du niveau d'alimentation antérieur (Effect on energy and nitrogen balances of replacing part of the tallow in a milk replacer for preruminant calves by tricaproin or coconut oil: effect of previous feeding level). Reproduction Nutrition Développement 23, 587–597.CrossRefGoogle Scholar
Aurousseau, B, Vermorel, M & Bouvier, JC (1984 b) Influence du remplacement d'une partie du suif d'un aliment d'allaitement par de la tricapryline ou de l'huile de coprah sur l'utilisation de l'énergie et de l'azote par le veau préruminant (Effect on energy and nitrogen balances of substituting tricaprylin or coconut oil for a part of the tallow in a milk replacer for the preruminant calf). Reproduction Nutrition Développement 24, 265–279.CrossRefGoogle Scholar
Bach, AC, Ingenbleek, Y & Frey, A (1996) The usefulness of dietary medium-chain triglycerides in body weight control: fact or fancy?. Journal of Lipid Research 37, 708–726.CrossRefGoogle ScholarPubMed
Barnouin, J, El Idilbi, N, Chilliard, Y, Chacornac, JP & Lefaivre, R (1986) Automated micro-determination of bovine plasma 3-hydroxybutyrate without deproteinization. Annales de Recherches Vétérinaires 17, 129–139.Google ScholarPubMed
Bauchart, D, Durand, D, Picherit, C, Graulet, B & Gruffat, D (1998) Effects of dietary coconut oil on blood transport and in vivo hepatic metabolism of fatty acids in the preruminant calf. Reproduction Nutrition Development 38, 203.CrossRefGoogle Scholar
Bauchart, D, Ortigues, I, Hocquette, JF, Guffant, D & Durand, D (1996) Energy and fat metabolism of the liver, the digestive tract and muscles: transporting, processing, energy consumption and fixation by tissues. In Veal, Perspectives to the Year 2000, Proceedings of the International Symposium, Le Mans, France, pp. 255–290 [The French Federation of Veal Producers, editors]. Le Mans, France: Presse de Jouve.Google Scholar
Bouziane, M, Belleville, J & Prost, J (1997) Hepatic storage and transport of n-3 and n-6 polyunsaturated fatty acids by very-low density lipoproteins in growing rats fed low- or adequate-protein diets with sunflower, soybean, coconut, and salmon oils. American Journal of Clinical Nutrition 65, 750–760.CrossRefGoogle ScholarPubMed
Christensen, E, Hagve, TA, Gronn, M & Christopherson, BO (1989) β-Oxidation of medium chain (C8-C14) fatty acids studied in isolated liver cells. Biochimica et Biophysica Acta 1004, 187–195.CrossRefGoogle ScholarPubMed
Christiansen, EN, Gray, TJ & Lake, BG (1985) Effect of very-long chain fatty acids on peroxisomal beta-oxidation in primary rat hepatocyte cultures. Lipids 20, 929–932.CrossRefGoogle ScholarPubMed
Craig, SR & Gatlin, DM (1995) Coconut oil and beef tallow, but not tricaprylin, can replace menhaden oil in the diet of red drum (Sciaenops ocellatus) without adversely affecting growth or fatty acid composition. Journal of Nutrition 125, 3041–3048.Google ScholarPubMed
Crozier, GL (1988) Medium-chain triglycerides feeding over the long term: the metabolic fate of [14C]octanoate and [14C]oleate in isolated rat hepatocytes. Journal of Nutrition 118, 297–304.CrossRefGoogle Scholar
Demarne, Y, Epo, N, Flanzy, J & Lecourtier, MJ (1978) Comparison of long-term lipogenic effects of two different medium-chain triglycerides (tri C8:0 and tri C12:0) in the growing rat. Archives Internationales de Physiologie et de Biochimie 86, 25–35.CrossRefGoogle Scholar
Durand, D & Bauchart, D (1986) Variations nyctémérales de la lipémie et de la glycémie au niveau des voies afférentes et efférentes du foie chez le veau préruminant (Nyctemeral variations of lipaemia and glycaemia in afferent and efferent hepatic blood vessels in the preruminant calf). Reproduction Nutrition Développement 26, 371–372.CrossRefGoogle Scholar
Eckel, RH, Hanson, AS, Chen, AY, Berman, JN, Yost, TJ & Brass, EP (1992) Dietary substitution of medium-chain triglycerides improves insulin-mediated glucose metabolism in NIDDM subjects. Diabetes 41, 641–647.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GHS (1957) A simple method of the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497–509.CrossRefGoogle ScholarPubMed
Gruffat, D, Durand, D, Graulet, B & Bauchart, D (1996) Regulation of VLDL synthesis and secretion in the liver. Reproduction Nutrition Development 36, 375–389.CrossRefGoogle ScholarPubMed
Hill, JO, Peters, JC, Swift, L, Yang, D, Sharp, T, Abumrad, N & Greene, H (1990) Changes in blood lipids during six days of overfeeding with medium or long-chain triglycerides. Journal of Lipid Research 31, 407–416.CrossRefGoogle ScholarPubMed
Hocquette, JF & Bauchart, D (1999) Intestinal absorption, blood transport and hepatic and muscle metabolism of fatty acids in preruminant and ruminant animals. Reproduction Nutrition Development 39, 27–48.CrossRefGoogle ScholarPubMed
Hocquette, JF, Bornes, F, Balage, M, Ferre, P, Grizard, J & Vermorel, M (1995) Glucose-transporter (GLUT4) protein content in oxidative and glycolytic skeletal muscles from calf and goat. Biochemical Journal 305, 465–470.CrossRefGoogle ScholarPubMed
Hocquette, JF, Ortigues-Marty, I & Vermorel, M (1998) Nutritional regulation of energy metabolism in growing ruminants. In Proceedings of the Symposium on Growth in Ruminants: Basic Aspects, Theory and Practice for the Future, pp. 76–85 [Blum, JW, Elsasser, T and Guilloteau, P, editors]. Berne, Switzerland: University of Berne.Google Scholar
Jenkins, KJ, Kramer, JKG, Sauer, FD & Emmons, DB (1985) Influence of triglycerides and free fatty acids in milk replacers on calf performance, blood plasma, and adipose lipids. Journal of Dairy Science 68, 669–680.CrossRefGoogle ScholarPubMed
Leighton, F, Pérrico, R & Necochea, C (1984) Peroxisomal fatty acid oxidation is selectively inhibited by phenothiazines in isolated hepatocytes. Biochemical and Biophysical Research Communications 120, 505–511.CrossRefGoogle ScholarPubMed
Leplaix-Charlat, L, Durand, D & Bauchart, D (1996) Effects of diets containing tallow and soybean oil with and without cholesterol on hepatic metabolism of lipids and lipoproteins in the preruminant calf. Journal of Dairy Science 79, 1826–1835.CrossRefGoogle ScholarPubMed
Leyton, J, Drury, PJ & Crawford, MA (1987) Differential oxidation of saturated and unsaturated fatty acids in vivo in the rat. British Journal of Nutrition 57, 383–393.CrossRefGoogle ScholarPubMed
Miller, GM, Conrad, JH, Keenan, TW & Featherston, WR (1971) Fatty acid oxidation in young pigs. Journal of Nutrition 101, 1343–1350.CrossRefGoogle ScholarPubMed
Nicolisi, R, Herrera, MG, El Hozy, M & Hayes, KC (1976) Effect of dietary fat on hepatic metabolism of 14C-oleic acid and very-low density lipoprotein triglycerides in the gerbil. Journal of Nutrition 106, 1279–1285.CrossRefGoogle Scholar
Piot, C, Veerkamp, JH, Durand, D, Bauchart, D & Hocquette, JF (1998) Contribution of mitochondria and peroxisomes to palmitate oxidation in rat and bovine tissues. Comparative Biochemistry and Physiology 121B, 69–78.Google Scholar
Power, GW & Newsholme, EA (1997) Dietary fatty acids influence the activity and metabolic control of mitochondrial carnitine palmitoyltransferase I in rat heart and skeletal muscle. Journal of Nutrition 127, 2142–2150.CrossRefGoogle ScholarPubMed
Reubsaet, FAG, Veerkamp, JH, Trijbels, JMF & Monnens, LAH (1989) Total and peroxisomal oxidation of various saturated and unsaturated fatty acids in the rat liver, heart and M. quadriceps. Lipids 24, 945–950.CrossRefGoogle ScholarPubMed
Ricks, CA & Cook, RM (1981) Regulation of volatile fatty acid uptake by mitochondrial acyl-CoA synthetases of bovine liver. Journal of Dairy Science 64, 2324–2335.CrossRefGoogle ScholarPubMed
Stein, DT, Stevenson, BE, Chester, MW, Basit, M, Daniels, MB, Turley, SD & McGarry, JD (1997) The insulinotropic potency of fatty acids is influenced profoundly by their chain length and degree of saturation. Journal of Clinical Investigation 100, 398–403.CrossRefGoogle ScholarPubMed
St John, LC, Lunt, DK & Smith, SB (1991) Fatty acid elongation and desaturation enzyme activities of bovine liver and subcutaneous adipose tissue microsomes. Journal of Animal Science 69, 1064–1073.CrossRefGoogle ScholarPubMed
Takase, S & Hosoya, N (1986) Effect of dietary medium-chain triglycerides on lipogenic enzyme activity in rat liver. Journal of Nutrition Science and Vitaminology 32, 219–227.CrossRefGoogle ScholarPubMed
Toullec, R (1978) Le Veau (The Calf). In INRA Alimentation des Ruminants, pp. 270–271. Versailles, France: INRA Publications.Google Scholar
Veerkamp, JH & Van Moerkerk, HTB (1986) Peroxisomal fatty acid oxidation in rat and human tissues. Effect of nutritional state, clofibrate treatment and postnatal development in the rat. Biochimica et Biophysica Acta 875, 301–310.CrossRefGoogle ScholarPubMed
Wiley, JH & Leveille, GA (1973) Metabolic consequences of dietary medium-chain triglycerides in the rat. Journal of Nutrition 103, 829–835.CrossRefGoogle ScholarPubMed
Wilson, DE, Chan, IF, Stevenson, KB, Horton, SC & Schipke, C (1983) Eucaloric substitution of medium-chain triglycerides for dietary long chain fatty acids in acquired total lipodystrophy: effects on hyperlipoproteinemia and endogenous insulin resistance. Journal of Clinical Endocrinology and Metabolism 57, 517–523.CrossRefGoogle ScholarPubMed
Yaqoob, P, Sherrington, EJ, Jeffery, NM, Sanderson, P, Harvey, DJ, Newsholme, C & Calder, PC (1995) Comparison of the effects of a range of dietary lipids upon serum and tissue lipid composition in the rat. International Journal of Biochemistry and Cellular Biology 27, 297–310.CrossRefGoogle ScholarPubMed