Skip to main content Accessibility help
×
Home

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

  • D. Gruffat (a1), M. Gobert (a1) (a2), D. Durand (a1) and D. Bauchart (a1)

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.

Copyright

Corresponding author

References

Hide All
Abumrad, N, Harmon, C, Ibrahimin, A 1998. Membrane transport of long-chain fatty acids: evidence for facilitated process. Journal of Lipid Research 39, 23092318.
Bauchart, D, Gruffat, D, Durand, D 1996. Lipid absorption and hepatic metabolism in ruminants. Proceedings of the Nutrition Society 55, 3947.
Bojesen, IN, Bojesen, E 1999. Sheep erythrocyte membrane binding and transfer of long-chain fatty acids. Journal of Membrane Biology 171, 141149.
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, 28822894.
Bouyekhf, M, Rule, DC, Hu, CY 1992. Glycerolipid biosynthesis in adipose tissue of bovine during growth. Comparative Biochemistry and Physiology B 103, 101104.
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, 8591.
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, 965969.
Burdge, GC, Calder, PC 2005. Conversion of α-linoleic acid to longer-chain polyunsaturated fatty acids in human adults. Reproduction, Nutrition and Development 45, 581597.
Chilliard, Y 1993. Dietary fat and adipose tissue metabolism in ruminants, pigs and rodents: a review. Journal of Dairy Science 76, 38973931.
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, 469482.
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, 18441854.
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, 5762.
Christie, WW, Sébédio, JL, Juanéda, P 2001. A practical guide to the analysis of conjugated linoleic acid. INFORM 12, 147152.
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, 867876.
Demeyer, D, Doreau, M 1999. Targets and procedures for altering ruminant meat and milk lipids. Proceedings of the Nutrition Society 58, 593607.
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, 441451.
Doreau, M, Chilliard, Y 1997. Digestion and metabolism of dietary fat in farm animals. British Journal of Nutrition 78 (suppl. 1), S15S35.
Emery, RS, Liesman, JS, Herdt, TH 1992. Metabolism of long chain fatty acids by ruminant liver. Journal of Nutrition 122, 832837.
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, R80R86.
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, 497509.
Gavino, GR, Gavino, VC 1991. Modulation of polyunsaturated fatty acid content of triglycerides in rat pre-adipocytes in culture. Lipids 26, 705710.
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, 179198.
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, 749753.
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, 12121219.
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, 309318.
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, 645652.
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, 295301.
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, 529536.
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.
Hocquette, JF, Graulet, B, Olivecrona, T 1998. Lipoprotein lipase activity and mRNA levels in bovine tissues. Comparative Biochemistry and Physiology B 121, 201212.
Hulbert, AJ, Turner, N, Storlien, LH, Else, PL 2005. Dietary fats and membrane function: implications for metabolism and disease. Biological Reviews 80, 155169.
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, 1024710255.
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, 448463.
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, 18121822.
Jacobi, SK, Miner, JL 2002. Human acylation-stimulating protein and lipid biosynthesis in bovine adipose tissue explants. Journal of Animal Science 80, 751756.
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, 135140.
Novakofski, J 2004. Adipogenesis: usefulness of in vitro and in vivo experimental models. Journal of Animal Science 82, 905915.
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, 77100.
Reid, JCW, Husbands, DR 1985. Oxidative metabolism of long-chain fatty acids in mitochondria from sheep and rat liver. Biochemical Journal 225, 233237.
Simopoulos, AP 1999. Essential fatty acids in health and chronic disease. American Journal of Clinical Nutrition 70 (suppl. 3), 560S569S.
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, 149154.
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, 4455.
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, 981989.
Sprecher, H 1981. Biochemistry of essential fatty acids. Progress in Lipid Research 20, 1322.
Sprecher, H 2000. Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochimica et Biophysica Acta 1486, 219231.
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, 343358.
Zakim, D 1996. Fatty acids enter cells by simple diffusion. Proceedings of the Society for Experimental Biology and Medicine 212, 514.
Zhang, F, Kamp, F, Hamilton, JA 1996. Dissociation of long and very long chain fatty acids from phospholipid bilayers. Biochemistry 35, 1605516060.

Keywords

Related content

Powered by UNSILO

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

  • D. Gruffat (a1), M. Gobert (a1) (a2), D. Durand (a1) and D. Bauchart (a1)

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.