Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T14:40:43.322Z Has data issue: false hasContentIssue false
  • English
  • Français

Long-chain fatty acids differentially alter lipogenesis in bovine and caprine mammary slices

Published online by Cambridge University Press:  17 December 2012

Laurence Bernard ,
Mohamad B. Montazer Torbati ,
Benoit Graulet ,
Christine Leroux  and
Yves Chilliard
Laurence Bernard*
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000 Clermont-Ferrand, France
Mohamad B. Montazer Torbati
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000 Clermont-Ferrand, France Department of Animal Science, Faculty of Agriculture, University of Birjand, Iran
Benoit Graulet
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000 Clermont-Ferrand, France
Christine Leroux
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000 Clermont-Ferrand, France
Yves Chilliard
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000 Clermont-Ferrand, France
*
*For Correspondence; e-mail: Laurence.Bernard@clermont.inra.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

Indirect comparisons from studies in vivo have suggested that caprine mammary tissue is less sensitive than bovine mammary tissue to the anti-lipogenic effect of long-chain fatty acids (LCFA), including specific rumen biohydrogenation (RBH) intermediates of polyunsaturated fatty acids (PUFA). Our objective was to investigate the effects on lipogenesis of 18-carbon LCFA differing in the degree of unsaturation and/or double bond conformation using cultured slices of bovine and caprine mammary tissues. Mammary tissues were collected from five multiparous Holstein × Normande cows and six multiparous Alpine goats in mid lactation. The expression of genes involved in milk component synthesis was measured in tissues collected at slaughter and after slice preparation: FASN, SCD1, CD36, SREBF1 and PPARG1 mRNA levels were higher in bovine than caprine samples, whereas the opposite was observed for CSN2 mRNA levels. Bovine and caprine mammary slices were incubated for 20 h in a medium with BSA (control), cis-9-18 : 1, 18 : 2n-6, 18 : 3n-3, cis-9, trans-11-CLA, or trans-10, cis-12-CLA (the latter at 3 increasing concentrations: C1 (0·11 mm), C2 (0·16 mm), C3 (0·37 mm)). Lipogenesis was estimated by measuring the incorporation of 14C-acetate into total lipid. Significant differences of individual LCFA (P < 0·05) were observed between species: bovine tissue showed a decrease in total lipogenesis with 18 : 2n-6, 18 : 3n-3, trans-10,cis-12-CLA (C2 and C3) while caprine tissue showed an increase after treatment with 18 : 3n-3, cis-9, trans-11-CLA or trans-10, cis-12-CLA (C3). These results were not related to the mRNA abundance of our set of genes in the mammary slices after incubation. In conclusion, this study demonstrates that caprine mammary slices reacted differently from bovine mammary slices to the anti-lipogenic activity of specific LCFA and suggests that regulation of lipogenesis via other genes and/or at protein level and enzyme activity may be involved.

Keywords

Long-chain fatty acidslipogenic activitymammary sliceslactating cowlactating goat
Type
Research Article
Information
Journal of Dairy Research , Volume 80 , Issue 1 , February 2013 , pp. 89 - 95
Copyright
Copyright © Proprietors of Journal of Dairy Research 2012

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

Barber, MC, Clegg, RA, Travers, MT & Vernon, RG 1997 Lipid metabolism in the lactating mammary gland. Biochimica et Biophysica Acta 1347 101–126CrossRefGoogle ScholarPubMed
Baumgard, LH, Corl, BA, Dwyer, DA, Sæbø, A & Bauman, DE 2000 Identification of the conjugated linoleic acid isomer that inhibits milk fat synthesis. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 278 R179–R184Google Scholar
Baumgard, LH, Corl, BA, Dwyer, DA & Bauman, DE 2002 Effects of conjugated linoleic acids (CLA) on tissue response to homeostatic signals and plasma variables associated with lipid metabolism in lactating dairy cows. Journal of Animal Science 80 1285–1293Google Scholar
Bernard, L, Rouel, J, Leroux, C, Ferlay, A, Faulconnier, Y, Legrand, P & Chilliard, Y 2005 Mammary lipid metabolism and milk fatty acid secretion in alpine goats fed vegetable lipids. Journal of Dairy Science 88 1478–1489Google Scholar
Bernard, L, Leroux, C & Chilliard, Y 2008 Expression and nutritional regulation of lipogenic genes in the ruminant lactating mammary gland. Advances in Experimental Medicine and Biology 606 67–108Google Scholar
Bernard, L, Bonnet, M, Leroux, C, Shingfield, KJ & Chilliard, Y 2009a Effect of sunflower-seed oil and linseed oil on tissue lipid metabolism, gene expression and milk fatty acid secretion in Alpine goats fed maize silage based diets. Journal of Dairy Science 92 6083–6094CrossRefGoogle ScholarPubMed
Bernard, L, Leroux, C, Faulconnier, Y, Durand, D, Shingfield, KJ & Chilliard, Y 2009b Effect of sunflower-seed oil or linseed oil on milk fatty acid secretion and lipogenic gene expression in goats fed hay-based diets. Journal of Dairy Research 76 241–248Google Scholar
Bonnet, M, Leroux, C, Chilliard, Y & Martin, P 2001 A fluorescent reverse transcription-polymerase chain reaction assay to quantify the lipoprotein lipase messenger RNA. Molecular and Cellular Probes 15 187–194CrossRefGoogle ScholarPubMed
Bonnet, M, Bernard, L, Bes, S & Leroux, C 2012 Selection of reference genes for quantitative real-time PCR normalisation in adipose tissue, muscle, liver and mammary gland from ruminants. Animal, in pressGoogle Scholar
Chilliard, Y, Gagliostro, G, Flechet, J, Lefaivre, J & 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 1844–1854CrossRefGoogle ScholarPubMed
Chilliard, Y, Glasser, F, Ferlay, A, Bernard, L, Rouel, J & Doreau, M 2007 Diet, rumen biohydrogenation, cow and goat milk fat nutritional quality. European Journal of Lipid Science and Technology 109 828–855Google Scholar
Christensen, RA, Drackley, JK, LaCount, DW & Clark, JH 1994 Infusion of four long-chain fatty acid mixtures into the abomasum of lactating dairy cows. Journal of Dairy Science 77 1052–1069Google 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 Biology and Chemistry 226 497–509Google Scholar
Gagliostro, G, Chilliard, Y & Davicco, MJ 1991 Duodenal rapeseed oil infusion in early and midlactation cows. 3. Plasma hormones and mammary apparent uptake of metabolites. Journal of Dairy Science 74 1893–1903Google Scholar
Gervais, R, McFadden, JW, Lengi, AJ, Corl, BA & Chouinard, PY 2009 Effects of intravenous infusion of trans-10, cis-12 18 : 2 on mammary lipid metabolism in lactating dairy cows. Journal of Dairy Science 92 5167–5177Google Scholar
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 84 309–318Google Scholar
Hansen, HO & Knudsen, J 1987 Effect of exogenous long-chain fatty acids on individual fatty acid synthesis by dispersed ruminant mammary gland cells. Journal of Dairy Science 70 1350–1354Google Scholar
Hansen, HO, Jensen, SS & Knudsen, J 1986 Absence of monoacylglycerol pathway for triacylglycerol synthesis in goat mammary gland. Biochemical Journal 238 173–176Google Scholar
Harvatine, KJ & Bauman, DE 2006 SREBP1 and thyroid hormone responsive spot 14 (S14) are involved in the regulation of bovine mammary lipid synthesis during diet-induced milk fat depression and treatment with CLA. Journal of Nutrition 136 2468–2474Google Scholar
Jayan, GC & Herbein, JH 2000 ‘Healthier’ dairy fat using trans-vaccenic acid. Nutrition and food Science 30 304–309Google Scholar
Kadegowda, AK, Bionaz, M, Piperova, LS, Erdman, RA & Loor, JJ 2009 Peroxisome proliferator-activated receptor-gamma activation and long-chain fatty acids alter lipogenic gene networks in bovine mammary epithelial cells to various extents. Journal of Dairy Science 92 4276–4289Google Scholar
Kadegowda, AK, Connor, EE, Teter, BB, Sampugna, J, Delmonte, P, Piperova, LS & Erdman, RA 2010 Dietary trans fatty acid isomers differ in their effects on mammary lipid metabolism as well as lipogenic gene expression in lactating mice. Journal of Nutrition 140 919–924Google Scholar
Lin, X, Loor, JJ & Herbein, JH 2004 Trans10, cis12–18 : 2 is a more potent inhibitor of de novo fatty acid synthesis and desaturation than cis9, trans11–18 : 2 in the mammary gland of lactating mice. Journal of Nutrition 134 1362–1368Google Scholar
Liu, W, Degner, SC & Romagnolo, DF 2006 Trans-10, cis-12 conjugated linoleic acid inhibits prolactin-induced cytosolic NADP+ -dependent isocitrate dehydrogenase expression in bovine mammary epithelial cells. Journal of Nutrition 136 2743–2747Google Scholar
Loor, JJ & Herbein, JH 2003 Reduced fatty acid synthesis and desaturation due to exogenous trans10, cis12-CLA in cows fed oleic or linoleic oil. Journal of Dairy Science 86 1354–1369Google Scholar
Matitashvili, E & Bauman, DE 2000 Effect of different isomers of C18 : 1 and C18 : 2 fatty acids on lipogenesis in bovine mammary epithelial cells. Journal of Animal Science 78 165Google Scholar
Matitashvili, E, Baumgard, LH & Bauman, DE 2001 The effect of trans-10, cis-12 conjugated linoleic acid (CLA) infusion on milk fat synthesis and expression of lipogenic enzymes in the mammary gland of lactating cows. Journal of Animal Science 79 Suppl. 1310Google Scholar
McFadden, JW, Mullarky, IK & Corl, BA 2008 Inhibitory effect of unsaturated fatty acids on de novo fatty acid synthesis in bovine mammary epithelial cells. Journal of Animal Science, 86 566Google Scholar
Peterson, DG, Matitashvili, EA & Bauman, DE 2004 The inhibitory effect of trans-10, cis-12 CLA on lipid synthesis in bovine mammary epithelial cells involves reduced proteolytic activation of the transcription factor SREBP-1. Journal of Nutrition 134 2523–2527Google Scholar
Roy, A, Ferlay, A, Shingfield, KJ & Chilliard, Y 2006 Examination of the persistency of milk fatty acid composition responses to plant oils in cows fed different basal diets, with particular emphasis on trans-C18:1 fatty acids and isomers of conjugated linoleic acid. Animal Science 82 479–492Google Scholar
Shingfield, KJ, Rouel, J & Chilliard, Y 2009 Effect of calcium salts of a mixture of conjugated linoleic acids containing trans-10, cis-12 in the diet on milk fat synthesis in goats. British Journal of Nutrition 101 1006–1019Google Scholar
Shingfield, KJ, Bernard, L, Leroux, C & Chilliard, Y 2010 Role of trans fatty acids in the nutritional regulation of mammary lipogenesis in ruminants. Animal 4 1140–1166Google Scholar
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Van Roy, N, De Paepe, A & Speleman, F 2002 Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3 1–12Google Scholar
Yonezawa, T, Haga, S, Kobayashi, Y, Katoh, K & Obara, Y 2008 Regulation of hormone-sensitive lipase expression by saturated fatty acids and hormones in bovine mammary epithelial cells. Biochemical and Biophysical Research Communications 376 36–39Google Scholar