Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T11:45:38.717Z Has data issue: false hasContentIssue false
  • English
  • Français

Adaptations of hepatic amino acid uptake and net utilisation contributes to nitrogen economy or waste in lambs fed nitrogen- or energy-deficient diets

Published online by Cambridge University Press:  22 November 2010

G. Kraft ,
I. Ortigues-Marty ,
D. Durand ,
D. Rémond ,
T. Jardé ,
B. Bequette  and
I. Savary-Auzeloux
G. Kraft
Affiliation:
INRA, UR 1213, Unité de Recherches sur les Herbivores, Equipe Nutriments et Métabolismes, Site de Theix, F 63122 Saint-Genès-Champanelle, France
I. Ortigues-Marty
Affiliation:
INRA, UR 1213, Unité de Recherches sur les Herbivores, Equipe Nutriments et Métabolismes, Site de Theix, F 63122 Saint-Genès-Champanelle, France
D. Durand
Affiliation:
INRA, UR 1213, Unité de Recherches sur les Herbivores, Equipe Nutriments et Métabolismes, Site de Theix, F 63122 Saint-Genès-Champanelle, France
D. Rémond
Affiliation:
INRA, UMR 1019, Unité de Nutrition Humaine, F 63122 Saint-Genès-Champanelle, France
T. Jardé
Affiliation:
INRA, UR 1213, Unité de Recherches sur les Herbivores, Equipe Nutriments et Métabolismes, Site de Theix, F 63122 Saint-Genès-Champanelle, France
B. Bequette
Affiliation:
Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742-2311, USA
I. Savary-Auzeloux*
Affiliation:
INRA, UR 1213, Unité de Recherches sur les Herbivores, Equipe Nutriments et Métabolismes, Site de Theix, F 63122 Saint-Genès-Champanelle, France
*
†E-mail: [email protected]
Get access

Abstract

We investigated the effect of relative changes in dietary nitrogen (N) and energy supply and the subsequent variations in net portal appearance (NPA) of nitrogenous and energy nutrients on the net amino acid (AA) uptake by the liver and net N supply to the peripheral tissues. Six lambs were catheterised across the splanchnic tissues and received, in a replicated Latin square, one of three dietary treatments. The diets were formulated to either match the requirements of N and energy (C), or supply only 0.8 of the N requirement (LN) or 0.8 of the energy requirement (LE). Net fluxes of AA and urea-N were measured across the portal-drained viscera, and estimation of arterial hepatic flow allowed the estimation of hepatic fluxes. Catheters were implanted into the portal and hepatic veins as well as in the abdominal aorta for the measurement of AA fluxes. Animals fed the LN diet showed more efficient N retention (0.59 of digested N) than did the C and LE diet (0.50 and 0.33, respectively; P < 0.001). The NPA of total AA-N for the LN diet was only 0.60 of the value measured for the control (C) diet (P < 0.01). Despite this, the total estimated AA-N net splanchnic fluxes were not significantly different across the three diets (3.3, 1.9 and 2.6 g total AA-N/day for C, LN and LE, respectively, P = 0.52). Thus, different metabolic regulations must have taken place across the liver between the three experimental diets. A combination of decreased net uptake of total AA-N by the liver of animals in the LN diet (0.61 of the C diet; P = 0.002) and reduced urinary urea-N production (0.52 of the C diet; P = 0.001) spared AA from catabolism in the LN diet relative to the other two diets. For the LE diet, the urinary urea-N output was 1.3 times the value of the C diet (P = 0.01). This may relate to an increased catabolism of AA by the muscle and/or, to a lesser extent, to an increased utilisation of AA for gluconeogenesis in the liver. These effects may explain the reduced whole body protein retention observed with the LE diet.

Keywords

amino acidlamblivernet flux
Type
Full Paper
Information
animal , Volume 5 , Issue 5 , 04 April 2011 , pp. 678 - 690
Copyright
Copyright © The Animal Consortium 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Argiles, JM, Busquets, S, Lopez-Soriano, FJ 2001. Metabolic interrelationships between liver and skeletal muscle in pathological states. Life Science 69, 1345–1361.CrossRefGoogle ScholarPubMed
Attaix, D, Rémond, D, Savary-Auzeloux, IC 2005. Protein metabolism and turnover. In Quantitative aspects of ruminant digestion and metabolism (ed. J Dijksta, JM Forbes and J France), pp. 373–397. CABI Publishing, Wallingford, UK.CrossRefGoogle Scholar
Bach, A, Huntington, GB, Calsamiglia, S, Stern, MD 2000. Nitrogen metabolism of early lactation cows fed diets with two different levels of protein and different amino acid profiles. Journal of Dairy Science 83, 2585–2595.CrossRefGoogle ScholarPubMed
Barnes, RJ, Comline, RS, Dobson, A 1986. The control of splanchnic blood flow. In Control of digestion and metabolism in ruminants (ed. LP Milligan, WL Grovum and A Dobson), pp. 41–59. Prentice Hall, Engelwood Cliffs, NJ, USA.Google Scholar
Black, JL, Griffiths, DA 1975. Effects of live weight and energy intake on nitrogen balance and total N requirements of lambs. British Journal of Nutrition 33, 399–413.CrossRefGoogle ScholarPubMed
Blouin, JP, Bernier, JF, Reynolds, CK, Lobley, GE, Dubreuil, P, Lapierre, H 2002. Effect of supply of metabolizable protein on splanchnic fluxes of nutrients and hormones in lactating dairy cows. Journal of Dairy Science 85, 2618–2630.CrossRefGoogle ScholarPubMed
Bruckental, I, Huntington, GB, Baer, CK, Erdman, RA 1997. The effect of abomasal infusion of casein and recombinant somatotropin hormone injection on nitrogen balance and amino acid fluxes in portal-drained viscera and net hepatic and total splanchnic blood in Holstein steers. Journal of Animal Science 75, 1119–1129.CrossRefGoogle ScholarPubMed
Burrin, DG, Ferrell, CL, Eisemann, JH, Britton, RA 1991. Level of nutrition and splanchnic metabolite flux in young lambs. Journal of Animal Science 69, 1082–1091.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 Communication in Mass Spectrometry 2, 14–16.CrossRefGoogle 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 Communication in Mass Spectrometry 13, 2080–2083.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Castillo, AR, Kebreab, E, Beever, DE, Barbi, JH, Sutton, JD, Kirby, HC, France, J 2001. The effect of protein supplementation on nitrogen utilization in lactating dairy cows fed grass silage diets. Journal of Animal Science 79, 247–253.CrossRefGoogle ScholarPubMed
Chowdhury, SA, Orskov, ER 1997. Protein energy relationships with particular references to energy undernutrition: a review. Small Ruminant Research 26, 1–7.CrossRefGoogle Scholar
Connell, A, Calder, AG, Anderson, SE, Lobley, GE 1997. Hepatic protein synthesis in the sheep: effect of intake as monitored by use of stable-isotope-labelled glycine, leucine and phenylalanine. British Journal of Nutrition 77, 255–271.CrossRefGoogle ScholarPubMed
El-Kadi, SW, Baldwin, RL, Sunny, NE, Owens, SL, Bequette, BJ 2006. Intestinal protein supply alters amino acid, but not glucose, metabolism by the sheep gastrointestinal tract. Journal of Nutrition 136, 1261–1269.CrossRefGoogle Scholar
Ferrell, CL, Kreikemeier, KK, Freetly, HC 1999. The effect of supplemental energy, nitrogen, and protein on feed intake, digestibility, and nitrogen flux across the gut and liver in sheep fed low-quality forage. Journal of Animal Science 77, 3353–3364.CrossRefGoogle ScholarPubMed
Ferrell, CL, Freetly, HC, Goetsch, AL, Kreikemeier, KK 2001. The effect of dietary nitrogen and protein on feed intake, nutrient digestibility, and nitrogen flux across the portal-drained viscera and liver of sheep consuming high-concentrate diets ad libitum. Journal of Animal Science 79, 1322–1328.CrossRefGoogle ScholarPubMed
Hanigan, MD 2005. Quantitative aspects of ruminant splanchnic metabolism as related to predicting animal performance. Animal Science 80, 23–32.CrossRefGoogle Scholar
Harris, PM, Skene, PA, Buchan, V, Milne, E, Calder, AG, Anderson, SE, Connell, A, Lobley, GE 1992. Effet 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, 389–407.CrossRefGoogle Scholar
Heger, J, Patras, P, Nitrayova, S, Dolesova, P, Sommer, A 2007. Histidine maintenance requirement and efficiency of its utilization in young pigs. Archives of Animal Nutrition 61, 179–188.CrossRefGoogle ScholarPubMed
Huntington, GB 1982. Portal blood flow and net absorption of ammonia-nitrogen, urea-nitrogen, and glucose in nonlactating Holstein cows. Journal of Dairy Science 65, 1155–1162.CrossRefGoogle ScholarPubMed
Jarrige, R 1989. Ruminant nutrition: recommended allowances and feed tables. Institut National de la Recherche Agronomique, Paris, France.Google Scholar
Krehbiel, CR, Ferrell, CL 1999. Effects of increasing ruminally degraded nitrogen and abomasal casein infusion on net portal flux of nutrients in yearling heifers consuming a high-grain diet. Journal of Animal Science 77, 1295–1305.CrossRefGoogle ScholarPubMed
Lapierre, H, Vernet, J, Martineau, R, Sauvant, D, Nozière, P, Ortigues-Marty, I 2007. Portal absorption of N: partition between amino acids and ammonia in relation with nitrogen intake in ruminants. In Energy and protein metabolism and nutrition (ed. I Ortigues-Marty), EAAP Publication no. 124, pp. 579–580. Wageningen Academic Publishers, Wageningen, The Netherlands.CrossRefGoogle Scholar
Lapierre, H, Bernier, JF, Dubreuil, P, Reynolds, CK, Farmer, C, Ouellet, DR, Lobley, GE 2000. The effect of feed intake level on splanchnic metabolism in growing beef steers. Journal of Animal Science 78, 1084–1099.CrossRefGoogle ScholarPubMed
Lobley, GE 1994. Amino acid and protein metabolism in the whole body and individual tissues of ruminants. In Principles of protein nutrition of ruminants (ed. JM Asplund), pp. 147–178. CRC Press, London, UK.Google Scholar
Lobley, GE 2003. Protein turnover – what does it mean for animal production? Canadian Journal of Animal Science 83, 327–340.CrossRefGoogle Scholar
Lobley, GE 2007. Protein-energy interaction: horizontal aspects. In Energy and protein metabolism and nutrition (ed. I Ortigues-Marty), EAAP Publication no. 124, pp. 445–461. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Lobley, GE, Milano, GD 1997. Regulation of hepatic nitrogen metabolism in ruminants. Proceedings of the Nutrition Society 56, 547–563.CrossRefGoogle ScholarPubMed
Lobley, GE, Lapierre, H 2003. Post-absorptive metabolism of amino acids. In Progress in research on energy and protein metabolism (ed. WB Souffrant and CC Metges), EAAP Publication no. 109, pp. 737–756. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
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, 217–235.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, Shen, X, Le, G, Bremner, DM, Milne, E, Calder, AG, Anderson, SE, Dennison, N 2003. Oxidation of essential amino acids by the ovine gastrointestinal tract. British Journal of Nutrition 89, 617–630.CrossRefGoogle ScholarPubMed
MacRae, JC, Bruce, LA, Brown, DS, Farningham, DA, Franklin, M 1997. 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
Maxwell, JL, Terracio, L, Borg, TK, Baynes, JW, Thorpe, SR 1990. A fluorescent residualizing label for studies on protein uptake and catabolism in vivo and in vitro. Biochemical Journal 267, 155–162.CrossRefGoogle ScholarPubMed
Metcalf, JA, Beever, DE, Sutton, JD, Wray-Cahen, D, Evans, RT, Humphries, DJ, Backwell, FR, Bequette, BJ, MacRae, JC 1994. The effect of supplementary protein on in vivo metabolism of the mammary gland in lactating dairy cows. Journal of Dairy Science 77, 1816–1827.CrossRefGoogle ScholarPubMed
Milano, GD 1997. Liver N transactions in sheep (Ovis aries). PhD thesis, University of Aberdeen.Google Scholar
Milano, GD, Hotston-Moore, A, Lobley, GE 2000. Influence of hepatic ammonia removal on ureagenesis, amino acid utilization and energy metabolism in the ovine liver. British Journal of Nutrition 83, 307–315.CrossRefGoogle ScholarPubMed
Oldham, JD 1984. Protein–energy interrelationships in dairy cows. Journal of Dairy Science 67, 1090–1114.CrossRefGoogle ScholarPubMed
Ormsby, AA 1942. A direct colorimetric method for the determination of urea in blood and urine. Journal of Biological Chemistry 146, 595–604.CrossRefGoogle Scholar
Ortigues-Marty, I, Doreau, M 1995. Responses of the splanchnic tissues of ruminants to changes in intake: absorption of digestion end products, tissue mass, metabolic activity and implications to whole animal energy metabolism. Annales de Zootechnie 44, 321–346.CrossRefGoogle Scholar
Ortigues-Marty, I, Durand, D, Lefaivre, J 1994. Use of para-amino hippuric acid to measure blood flows through portal-drained-viscera, liver and hindquarters in sheep. Journal of Agricultural Science 122, 299–308.CrossRefGoogle Scholar
Raggio, G, Lemosquet, S, Lobley, GE, Rulquin, H, Lapierre, H 2006. Effect of casein and propionate supply on mammary protein metabolism in lactating dairy cows. Journal of Dairy Science 89, 4340–4351.CrossRefGoogle ScholarPubMed
Raggio, G, Pacheco, D, Berthiaume, R, Lobley, GE, Pellerin, D, Allard, G, Dubreuil, P, Lapierre, H 2004. Effect of level of metabolizable protein on splanchnic flux of amino acids in lactating dairy cows. Journal of Dairy Science 87, 3461–3472.CrossRefGoogle ScholarPubMed
Reynolds, CK 1992. Metabolism of nitrogenous compounds by ruminant liver. Journal of Nutrition 122, 850–854.CrossRefGoogle ScholarPubMed
Reynolds, CK 2006. Splanchnic amino acid metabolisms in ruminants. In Ruminant physiology: digestion, metabolism and impact of nutrition on gene expression, immunology and stress (ed. K Sejrsen, T Hvelplund and MO Nielsen), pp. 225–248. Wageningen Academic Publisher, Wageningen, The Netherlands.CrossRefGoogle Scholar
Rigout, S, Hurtaud, C, Lemosquet, S, Bach, A, Rulquin, H 2003. Lactational effect of propionic acid and duodenal glucose in cows. Journal of Dairy Science 86, 243–253.CrossRefGoogle ScholarPubMed
Ruot, B 2001. Synthèse des protéines de la réaction inflammatoire en réponse à l’infection. Déterminisme de l’hypoalbuminémie. PhD thesis, Université d’Auvergne, Clermont-Ferrand, France.Google Scholar
Savary-Auzeloux, I, Kraft, G, Ortigues-Marty, I 2007. Can liver protein synthesis be affected by an imbalanced dietary supply of energy or nitrogen in growing lambs? In Energy and protein metabolism and nutrition (ed. I Ortigues-Marty), EAAP Publication no. 124, pp. 351–352. Wageningen Academic Publishers, Wageningen, The Netherlands.CrossRefGoogle Scholar
Savary-Auzeloux, I, Majdoub, L, LeFloc’h, N, Ortigues-Marty, I 2003. Effects of intraruminal propionate supplementation on nitrogen utilization by the portal-drained viscera, the liver and the hindlimb in lambs fed frozen rye grass. British Journal of Nutrition 90, 939–952.CrossRefGoogle ScholarPubMed
Savary-Auzeloux, I, Durand, D, Gruffat, D, Bauchard, D, Ortigues-Marty, I 2008a. Food restriction and refeeding in lambs influence muscle antioxidant status. Animal 2, 738–745.CrossRefGoogle ScholarPubMed
Savary-Auzeloux, I, Kraft, G, Dardevet, D, Rémond, D, Loncke, C, Ortigues-Marty, I 2008b. Liver protein synthesis regulation by energetic and nitrogenous nutrient supply. Conference of the 7th International Symposium on Amino acid/Protein Metabolism in Health and Disease. Mechanisms and Pathways controlling Protein Expression and Turnover, 4–5 July 2008, Padova, Italy.Google Scholar
Savary-Auzeloux, I, Kraft, G, Bequette, BJ, Papet, I, Rémond, D, Ortigues-Marty, I 2010. Dietary nitrogen-to-energy ratio alters amino acid partition in the whole body and among the splanchnic tissues of growing rams. Journal of Animal Science 88, 2122–2131.CrossRefGoogle ScholarPubMed
Storm, E, Orskov, ER 1983. The nutritive value of rumen micro-organisms in ruminants. 1. Large-scale isolation and chemical composition of rumen micro-organisms. British Journal of Nutrition 50, 463–470.CrossRefGoogle ScholarPubMed
Vernet, J, Nozière, P, Sauvant, D, Leger, S, Ortigues-Marty, I 2005. Regulation of hepatic blood flow by feeding conditions in sheep: a meta-analysis. In Advanced nutrition and feeding strategies to improve sheep and goat production (ed. A Mougou and B Hervieu), Options Méditerranéennes no. 74, pp. 435–440. IAM, Paris, France.Google Scholar
Volpi, E, Lucidi, P, Cruciani, G, Monacchia, F, Reboldi, G, Brunetti, P, Bolli, GB, De Feo, P 1996. Contribution of amino acids and insulin to protein anabolism during meal absorption. Diabetes 45, 1245–1252.CrossRefGoogle ScholarPubMed
Wolff, JE, Bergman, EN 1972. Gluconeogenesis from plasma amino acids in fed sheep. American Journal of Physiology 223, 455–460.CrossRefGoogle ScholarPubMed