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Distinct metabolism of linoleic and linolenic acids in liver and adipose tissues of finishing Normande cull cows

Published online by Cambridge University Press:  07 February 2011

D. Gruffat ,
M. Gobert ,
D. Durand  and
D. Bauchart
D. Gruffat*
Affiliation:
INRA, UR1213 Herbivores, Site de Theix, F-63122 Saint Genès Champanelle, France
M. Gobert
Affiliation:
INRA, UR1213 Herbivores, Site de Theix, F-63122 Saint Genès Champanelle, France INRA, UR0370 Qualité des produits animaux, Site de Theix, F-63122 Saint Genès Champanelle, France
D. Durand
Affiliation:
INRA, UR1213 Herbivores, Site de Theix, F-63122 Saint Genès Champanelle, France
D. Bauchart
Affiliation:
INRA, UR1213 Herbivores, Site de Theix, F-63122 Saint Genès Champanelle, France
*
†E-mail: [email protected]
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Abstract

Feeding strategies based on the addition of plant lipids rich in polyunsaturated fatty acids (PUFAs) in diets of bovines during the finishing period are common to enhance the nutritional value of meat. However, following rumen biohydrogenations, these FAs could still be metabolised in various tissues/organs involved in the FA metabolism such as the liver and adipose tissues (ATs), thus affecting their subsequent deposition in muscles. In this context, the objective of this study was to characterise the various metabolic pathways of linoleic acid (LA) and α-linolenic acid (ALA) in the liver and ATs (subcutaneous (SC) and inter-muscular (IM)) of Normande cull cows fed a diet supplemented (LR) or not (C) with extruded linseeds and rapeseeds, using the ex vivo incubated tissue slice method. Hepatic uptake of both FAs was higher with the LR than with the C diet (P = 0.02). For the two diets, ALA uptake was higher than that of LA (+46%, P = 0.04). ALA was much more degraded by β-oxidation (>50% of ALA present in cells) than LA (∼27%) with both diets (P = 0.015). Whatever the diet, ALA was not converted into longer and/or more unsaturated FA, whereas about 14% of LA was converted into 20:4n-6. The intensity of the esterification pathway was higher (+70%, P = 0.004) with the LR than with the C diet, for both FAs. Hepatic secretion of ALA as part of the very-low-density lipoprotein particles was lower than that of LA (−58% and −23% for C and LR diets respectively, P = 0.02). In SC and IM ATs, dietary lipid supplementation did not alter metabolic pathways of LA and ALA. They were efficiently taken up by ATs (>68% of FA present in the medium), with uptake being higher for IM than for SC AT (+12%, P = 0.01). Moreover, LA uptake by ATs was higher than ALA uptake (+10.7%, P = 0.027). Both FAs were mainly esterified (>97% of FA present in adipocytes) into neutral lipids (>85% of esterified FA). Around 9.5% of LA was converted into 20:4n-6, whereas only around 1.3% of ALA was converted into 20:5n-3. We concluded that, in our experimental conditions, liver was highly active in ALA catabolism limiting its subsequent deposition in muscles. However, bovine liver and ATs were inefficient at converting ALA into long-chain n-3 PUFA, but actively converted LA into 20:4n-6.

Keywords

unsaturated fatty acidsmetabolismliveradipose tissuefinishing bovine
Type
Full Paper
Information
animal , Volume 5 , Issue 7 , 31 May 2011 , pp. 1090 - 1098
Copyright
Copyright © The Animal Consortium 2011

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References

Abumrad, N, Harmon, C, Ibrahimin, A 1998. Membrane transport of long-chain fatty acids: evidence for facilitated process. Journal of Lipid Research 39, 2309–2318.CrossRefGoogle ScholarPubMed
Bauchart, D, Gruffat, D, Durand, D 1996. Lipid absorption and hepatic metabolism in ruminants. Proceedings of the Nutrition Society 55, 39–47.CrossRefGoogle ScholarPubMed
Bojesen, IN, Bojesen, E 1999. Sheep erythrocyte membrane binding and transfer of long-chain fatty acids. Journal of Membrane Biology 171, 141–149.CrossRefGoogle ScholarPubMed
Bonnet, M, Faulconnier, Y, Leroux, C, Jurie, C, Cassar-Malek, I, Bauchart, D, Boulesteix, P, Pethick, D, Hocquette, JF, Chilliard, Y 2007. Glucose-6-phosphate dehydrogenase and leptin are related to marbling differences among Limousin and Angus or Japanese Black × Angus steers. Journal of Animal Science 85, 2882–2894.CrossRefGoogle ScholarPubMed
Bouyekhf, M, Rule, DC, Hu, CY 1992. Glycerolipid biosynthesis in adipose tissue of bovine during growth. Comparative Biochemistry and Physiology B 103, 101–104.CrossRefGoogle ScholarPubMed
Brenna, JT, Salem, N, Sinclair, AJ, Cunnane, SC 2009. α-linoleic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins, Leukotrienes and Essential Fatty Acids 80, 85–91.CrossRefGoogle Scholar
Bretillon, J, Chardigny, JM, Grégoire, S, Berdeaux, O, Sébédio, JL 1999. Effects of conjugated linoleic acid isomers on the hepatic microsomal desaturation activities in vitro. Lipids 34, 965–969.CrossRefGoogle ScholarPubMed
Burdge, GC, Calder, PC 2005. Conversion of α-linoleic acid to longer-chain polyunsaturated fatty acids in human adults. Reproduction, Nutrition and Development 45, 581–597.CrossRefGoogle Scholar
Chilliard, Y 1993. Dietary fat and adipose tissue metabolism in ruminants, pigs and rodents: a review. Journal of Dairy Science 76, 3897–3931.CrossRefGoogle ScholarPubMed
Chilliard, Y, Bauchart, D, Barnouin, J 1984. Determination of plasma non esterified fatty acids in herbivores and man: a comparison of value obtained by manual or automatic chromatographic, titrimetric, colorimetric and enzymatic methods. Reproduction, Nutrition and Development 24, 469–482.CrossRefGoogle ScholarPubMed
Chilliard, Y, Gagliostro, G, Flechet, J, Lefaivre, , Sebastian, I 1991. Duodenal rapeseed oil infusion in early and midlactation cows. 5. Milk fatty acids and adipose tissue lipogenic activities. Journal of Dairy Science 74, 1844–1854.CrossRefGoogle ScholarPubMed
Christiansen, EN, Lund, JS, Rortveit, T, Rustan, AC 1991. Effect of dietary n-3 and n-6 fatty acids on fatty acid desaturation in rat liver. Biochemical Biophysical Acta 1082, 57–62.CrossRefGoogle ScholarPubMed
Christie, WW, Sébédio, JL, Juanéda, P 2001. A practical guide to the analysis of conjugated linoleic acid. INFORM 12, 147–152.Google Scholar
Clouet, P, Niot, I, Bezard, J 1989. Pathway of α-linolenic acid through the mitochondrial outer membrane in the rat liver and influence on the rate of oxidation. Biochemical Journal 263, 867–876.Google Scholar
Demeyer, D, Doreau, M 1999. Targets and procedures for altering ruminant meat and milk lipids. Proceedings of the Nutrition Society 58, 593–607.CrossRefGoogle ScholarPubMed
De La Torre, A, Gruffat, D, Chardigny, JM, Sébédio, JL, Durand, D, Loreau, O, Bauchart, D 2005. In vitro metabolism of rumenic acid in bovine liver slices. Reproduction, Nutrition and Development 45, 441–451.CrossRefGoogle ScholarPubMed
Doreau, M, Chilliard, Y 1997. Digestion and metabolism of dietary fat in farm animals. British Journal of Nutrition 78 (suppl. 1), S15–S35.Google Scholar
Emery, RS, Liesman, JS, Herdt, TH 1992. Metabolism of long chain fatty acids by ruminant liver. Journal of Nutrition 122, 832–837.Google Scholar
Emmison, N, Gallagher, PA, Coleman, RA 1995. Linoleic and linolenic acids are selectively secreted in triacylglycerol by hepatocytes from neonatal rats. American Journal of Physiology 269, R80–R86.Google Scholar
Folch, J, Lees, M, Sloane-Stanley, GHS 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–509.Google Scholar
Gavino, GR, Gavino, VC 1991. Modulation of polyunsaturated fatty acid content of triglycerides in rat pre-adipocytes in culture. Lipids 26, 705–710.Google Scholar
Gibbons, GF, Wiggins, D 1995. Intracellular triacylglycerol lipase: its role in the assembly of hepatic very-low-density lipoprotein (VLDL). Advances in Enzyme Regulation 35, 179–198.CrossRefGoogle ScholarPubMed
Gibbons, GF, Bartlett, SM, Sparks, CE, Sparks, JD 1992. Extracellular fatty acids are not utilized directly for the synthesis of very-low density lipoprotein in primary cultures of rat hepatocytes. Biochemical Journal 287, 749–753.CrossRefGoogle Scholar
Graulet, B, Gruffat, D, Durand, D, Bauchart, D 1998. Fatty acid metabolism and very low density lipoprotein secretion in liver slices from rats and preruminant calves. Journal of Biochemistry 124, 1212–1219.CrossRefGoogle ScholarPubMed
Graulet, B, Gruffat-Mouty, D, Durand, D, Bauchart, D 2000. Effects of milk diets containing beef tallow or coconut oil on the fatty acid metabolism of liver slices from preruminant calves. British Journal of Nutrition 84, 309–318.CrossRefGoogle ScholarPubMed
Gruffat, D, Rémond, C, Durand, D, Loreau, O, Bauchart, D 2008. 9cis,11trans CLA is synthesized and desaturated into conjugated 18:3 in bovine adipose tissues. Animal 2, 645–652.CrossRefGoogle Scholar
Gruffat, D, De La Torre, A, Chardigny, JM, Durand, D, Loreau, O, Bauchart, D 2005. Vaccenic acid metabolism in the liver of rat and bovine. Lipids 40, 295–301.CrossRefGoogle ScholarPubMed
Hanson, RW, Ballard, FJ 1967. The relative significance of acetate and glucose as precursors for lipid synthesis in liver and adipose tissue from ruminants. Biochemical Journal 105, 529–536.CrossRefGoogle ScholarPubMed
Harnack, K, Andersen, G, Somoza, V 2009. Quantification of alphalinolenic acid elongation to eicospentaenoic and docosahexaenoic acid as affected by the ratio of n-6/n-3 fatty acids. Nutrition & Metabolism 6, 8.CrossRefGoogle Scholar
Hocquette, JF, Graulet, B, Olivecrona, T 1998. Lipoprotein lipase activity and mRNA levels in bovine tissues. Comparative Biochemistry and Physiology B 121, 201–212.Google Scholar
Hulbert, AJ, Turner, N, Storlien, LH, Else, PL 2005. Dietary fats and membrane function: implications for metabolism and disease. Biological Reviews 80, 155–169.Google Scholar
Ide, T, Ontko, JA 1981. Increased secretion of very low density lipoprotein triglyceride following inhibition of long chain fatty acid oxidation in isolated rat liver. Journal of Biological Chemistry 256, 10247–10255.CrossRefGoogle ScholarPubMed
Ide, T, Murata, M, Sugano, M 1996. Stimulation of the activities of hepatic fatty acid oxidation enzymes by dietary fat rich in α-linolelic acid in rats. Journal of Lipid Research 37, 448–463.CrossRefGoogle Scholar
Igarashi, M, Ma, K, Chang, L, Bell, JM, Rapopport, SI, DeMar, JC Jr 2006. Low liver conversion rate of α-linolenic to docosahexaenoic acid in awake rats on a high-docosahexaenoate-containing diet. Journal of Lipid Research 47, 1812–1822.Google Scholar
Jacobi, SK, Miner, JL 2002. Human acylation-stimulating protein and lipid biosynthesis in bovine adipose tissue explants. Journal of Animal Science 80, 751–756.Google Scholar
Kaluzny, MA, Rode, LM, Meritt, MV, Epps, DE 1985. Rapid separation of lipid classes in high yield and purity using bonded phase columns. Journal of Lipid Research 26, 135–140.CrossRefGoogle ScholarPubMed
Novakofski, J 2004. Adipogenesis: usefulness of in vitro and in vivo experimental models. Journal of Animal Science 82, 905–915.CrossRefGoogle ScholarPubMed
Olinga, P, Meijer, DKF, Slooff, MJH, Groothuis, GMM 1997. Liver slices in in vitro pharmacotoxicology with special reference to the use of human liver tissue. Toxicology in Vitro 12, 77–100.CrossRefGoogle Scholar
Reid, JCW, Husbands, DR 1985. Oxidative metabolism of long-chain fatty acids in mitochondria from sheep and rat liver. Biochemical Journal 225, 233–237.Google Scholar
Simopoulos, AP 1999. Essential fatty acids in health and chronic disease. American Journal of Clinical Nutrition 70 (suppl. 3), 560S–569S.CrossRefGoogle ScholarPubMed
Schwenk, RW, Holloway, GP, Luiken, JJFP, Bonen, A, Glatz, JFC 2010. Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins, Leukotrienes and Essential Fatty acids 82, 149–154.CrossRefGoogle ScholarPubMed
Smit, LA, Mozaffarian, D, Willett, W 2009. Review of fat and fatty acid requirements and criteria for developing dietary guidelines. Annals of Nutrition & Metabolism 55, 44–55.Google Scholar
Stremmel, W, Pohl, J, Ring, A, Herrmann, T 2001. A new concept of cellular uptake and intracellular trafficking of long-chain fatty acids. Lipids 36, 981–989.CrossRefGoogle ScholarPubMed
Sprecher, H 1981. Biochemistry of essential fatty acids. Progress in Lipid Research 20, 13–22.CrossRefGoogle ScholarPubMed
Sprecher, H 2000. Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochimica et Biophysica Acta 1486, 219–231.CrossRefGoogle ScholarPubMed
Wood, JD, Enser, M, Fisher, AV, Nute, GR, Sheard, PR, Richardson, RI, Hughes, SI, Whittington, FM 2008. Fat deposition, fatty acid composition and meat quality: a review. Meat Science 78, 343–358.Google Scholar
Zakim, D 1996. Fatty acids enter cells by simple diffusion. Proceedings of the Society for Experimental Biology and Medicine 212, 5–14.Google Scholar
Zhang, F, Kamp, F, Hamilton, JA 1996. Dissociation of long and very long chain fatty acids from phospholipid bilayers. Biochemistry 35, 16055–16060.Google Scholar