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Dietary sunflower oil modulates milk fatty acid composition without major changes in adipose and mammary tissue fatty acid profile or related gene mRNA abundance in sheep

Published online by Cambridge University Press:  02 December 2014

T. Castro-Carrera ,
P. Frutos ,
C. Leroux ,
Y. Chilliard ,
G. Hervás ,
A. Belenguer ,
L. Bernard  and
P. G. Toral
T. Castro-Carrera
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n. 24346 Grulleros, León, Spain INRA, UMR 1213 Herbivores, Equipe Alimentation Génomique Lactation, Site de Theix, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
P. Frutos
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n. 24346 Grulleros, León, Spain
C. Leroux*
Affiliation:
INRA, UMR 1213 Herbivores, Equipe Alimentation Génomique Lactation, Site de Theix, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
Y. Chilliard
Affiliation:
INRA, UMR 1213 Herbivores, Equipe Alimentation Génomique Lactation, Site de Theix, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
G. Hervás
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n. 24346 Grulleros, León, Spain
A. Belenguer
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n. 24346 Grulleros, León, Spain
L. Bernard
Affiliation:
INRA, UMR 1213 Herbivores, Equipe Alimentation Génomique Lactation, Site de Theix, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
P. G. Toral
Affiliation:
INRA, UMR 1213 Herbivores, Equipe Alimentation Génomique Lactation, Site de Theix, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
*
†E-mail: christine.leroux@clermont.inra.fr
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Abstract

There are very few studies in ruminants characterizing mammary and adipose tissue (AT) expression of genes and gene networks for diets causing variations in milk fatty acid (FA) composition without altering milk fat secretion, and even less complementing this information with data on tissue FA profiles. This work was conducted in sheep in order to investigate the response of the mammary gland and the subcutaneous and perirenal AT, in terms of FA profile and mRNA abundance of genes involved in lipid metabolism, to a diet known to modify milk FA composition. Ten lactating Assaf ewes were randomly assigned to two treatments consisting of a total mixed ration based on alfalfa hay and a concentrate (60 : 40) supplemented with 0 (control diet) or 25 (SO diet) g of sunflower oil/kg of diet dry matter for 7 weeks. Milk composition, including FA profile, was analysed after 48 days on treatments. On day 49, the animals were euthanized and tissue samples were collected to analyse FA and mRNA abundance of 16 candidate genes. Feeding SO did not affect animal performance but modified milk FA composition. Major changes included decreases in the concentration of FA derived from de novo synthesis (e.g. 12:0, 14:0 and 16:0) and increases in that of long-chain FA (e.g. 18:0, c9-18:1, trans-18:1 isomers and c9,t11-CLA); however, they were not accompanied by significant variations in the mRNA abundance of the studied lipogenic genes (i.e. ACACA, FASN, LPL, CD36, FABP3, SCD1 and SCD5) and transcription factors (SREBF1 and PPARG), or in the constituent FA of mammary tissue. Regarding the FA composition of AT, the little influence of SO did not appear to be linked to changes in gene mRNA abundance (decreases of GPAM and SREBF1 in both tissues, and of PPARG in the subcutaneous depot). Similarly, the great variation between AT (higher contents of saturated FA and trans-18:1 isomers in the perirenal, and of cis-18:1, c9,t11-CLA and n-3 PUFA in the subcutaneous AT) could not be related to differences in gene mRNA abundance due to tissue site (higher LPL and CD36, and lower SREBF1 in perirenal than in subcutaneous AT). Overall, these results suggest a marginal contribution of gene expression to the nutritional regulation of lipid metabolism in these tissues, at least with the examined diets and after 7 weeks on treatments. It cannot be ruled out, however, that the response to SO is mediated by other genes or post-transcriptional mechanisms.

Keywords

fatty acid compositionlactating ewelipogenic gene expressionplant oiltissue
Type
Research Article
Information
animal , Volume 9 , Issue 4 , April 2015 , pp. 582 - 591
Copyright
© The Animal Consortium 2014 

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References

Barber, MC, Ward, RJ, Richards, SE, Salter, AM, Buttery, PJ, Vernon, RG and Travers, MT 2000. Ovine adipose tissue monounsaturated fat content is correlated to depot-specific expression of the stearoyl-CoA desaturase gene. Journal of Animal Science 78, 62–68.Google Scholar
Bas, P, Chilliard, Y, Morand-Fehr, P, Rouzeau, A and Mandran, N 1987. Composition des principaux tissus adipeux de la chèvre Alpine en fin de lactation. Annales de Zootechnie 36, 361–374.Google Scholar
Bauman, DE 2000. Regulation of nutrient partitioning during lactation: homeostasis and homeorhesis revisited. In Ruminant physiology: digestion, metabolism, growth and reproduction (ed. PB Cronje), pp. 311–328. CABI Publishing, Wallingford, UK.Google Scholar
Bernard, L, Leroux, C and Chilliard, Y 2008. Expression and nutritional regulation of lipogenic genes in the ruminant lactating mammary gland. Advances in Experimental Medicine and Biology 606, 67–108.Google Scholar
Bernard, L, Leroux, C and Chilliard, Y 2013. Expression and nutritional regulation of stearoyl-CoA desaturase genes in the ruminant mammary gland: relationship with milk fatty acid composition. In Stearoyl-CoA desaturase genes in lipid metabolism (ed. JM Ntambi), pp. 161–194. iSpringer Science+Business Media, New York, USA.Google Scholar
Bernard, L, Bonnet, M, Leroux, C, Shingfield, KJ and 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, 6083–6094.Google Scholar
Bernard, L, Leroux, C, Bonnet, M, Rouel, J, Martin, P and Chilliard, Y 2005a. Expression and nutritional regulation of lipogenic genes in mammary gland and adipose tissues of lactating goats. Journal of Dairy Research 72, 250–255.CrossRefGoogle ScholarPubMed
Bernard, L, Leroux, C, Faulconnier, Y, Durand, D, Shingfield, KJ and 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, 241–248.CrossRefGoogle ScholarPubMed
Bernard, L, Rouel, J, Leroux, C, Ferlay, A, Faulconnier, Y, Legrand, P and Chilliard, Y 2005b. Mammary lipid metabolism and milk fatty acid secretion in Alpine goats fed vegetable lipids. Journal of Dairy Science 88, 1478–1489.CrossRefGoogle ScholarPubMed
Bichi, E, Frutos, P, Toral, PG, Keisler, D, Hervás, G and Loor, JJ 2013. Dietary marine algae and its influence on tissue gene network expression during milk fat depression in dairy ewes. Animal Feed Science and Technology 186, 36–44.Google Scholar
Bonnet, M, Bernard, L, Bes, S and Leroux, C 2013. Selection of reference genes for quantitative real-time PCR normalisation in adipose tissue, muscle, liver and mammary gland from ruminants. Animal 7, 1344–1353.Google Scholar
Chilliard, Y 1999. Metabolic adaptations and nutrient partitioning in the lactating animal. In Biology of lactation (ed. J Martinet, L-M Houdebine and H Head), pp. 503–552. INRA Publishing, Paris, France.Google Scholar
Chilliard, Y and Robelin, J 1985. Activité lipoprotéine-lipasique de différents dépôts adipeux, et ses relations avec la taille des adipocytes chez la vache tarie en cours d’engraissement, ou en début de lactation. Reproduction Nutrition Development 25, 287–293.Google Scholar
Chilliard, Y, Sauvant, D, Bas, P, Pascal, G and Morand-Fehr, P 1981. Importance relative et activités métaboliques des différents tissus adipeux de la chèvre laitière. In Nutrition et systèmes d’alimentation de la chèvre, Tome I (ed. P Morand-Fehr, A Borbouze and M de Simiane), pp. 80–89. INRA-ITOVIC, Tours, France.Google Scholar
Chilliard, Y, Gagliostro, G, Flechet, J, Lefaivre, J and 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.Google Scholar
Christie, WW 1981. Lipid metabolism in ruminant animals. Pergamon Press Ltd, Oxford, UK.Google Scholar
Dervishi, E, Joy, M, Sanz, A, Alvarez-Rodriguez, J, Molino, F and Calvo, JH 2012. Forage preservation (grazing vs. hay) fed to ewes affects the fatty acid profile of milk and CPT1B gene expression in the sheep mammary gland. BMC Veterinary Research 8, 106.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M and Sloane-Stanley, GH 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–509.Google Scholar
Glass, RL 1971. Alcoholysis, saponification and the preparation of fatty acid methyl esters. Lipids 6, 919–925.Google Scholar
Gómez-Cortés, P, de la Fuente, MA, Toral, PG, Frutos, P, Juárez, M and Hervás, G 2011. Effects of different forage : concentrate ratios in dairy ewe diets supplemented with sunflower oil on animal performance and milk fatty acid profile. Journal of Dairy Science 94, 4578–4588.Google Scholar
Harvatine, KJ, Perfield, JW and Bauman, DE 2009. Expression of enzymes and key regulators of lipid synthesis is upregulated in adipose tissue during CLA-induced milk fat depression in dairy cows. Journal of Nutrition 139, 849–854.Google Scholar
INRA 2007. Alimentation des bovins, ovins et caprins. Besoins des Animaux: Valeur des aliments. Tables INRA 2007. INRA, Versailles, France.Google Scholar
Jacobs, AAA, van Baal, J, Smits, MA, Taweel, HZH, Hendriks, WH, van Vuuren, AM and Dijkstra, J 2011. Effects of feeding rapeseed oil, soybean oil, or linseed oil on stearoyl-CoA desaturase expression in the mammary gland of dairy cows. Journal of Dairy Science 94, 874–887.CrossRefGoogle ScholarPubMed
Murrieta, CM, Hess, BW, Scholljegerdes, EJ, Engle, TE, Hossner, KL, Moss, GE and Rule, DC 2006. Evaluation of milk somatic cells as a source of mRNA for study of lipogenesis in the mammary gland of lactating beef cows supplemented with dietary high-linoleate safflower seeds. Journal of Animal Science 84, 2399–2405.Google Scholar
Ntambi, JM 1999. Regulation of stearoyl-CoA desaturase by polyunsaturated fatty acids and cholesterol. Journal of Lipid Research 40, 1549–1558.CrossRefGoogle ScholarPubMed
Ollier, S, Leroux, C, de la Foye, A, Bernard, L, Rouel, J and Chilliard, Y 2009. Whole intact rapeseeds or sunflower oil in high-forage or high-concentrate diets affects milk yield, milk composition, and mammary gene expression profile in goats. Journal of Dairy Science 92, 5544–5560.CrossRefGoogle ScholarPubMed
Peterson, DG, Matitashvili, EA and Bauman, DE 2003. Diet-induced milk fat depression in dairy cows results in increased trans-10, cis-12 CLA in milk fat and coordinate suppression of mRNA abundance for mammary enzymes involved in milk fat synthesis. Journal of Nutrition 133, 3098–3102.CrossRefGoogle ScholarPubMed
Piperova, LS, Teter, BB, Bruckental, I, Sampugna, J, Mills, SE, Yurawecz, MP, Fritsche, J, Ku, K and Erdman, RA 2000. Mammary lipogenic enzyme activity, trans fatty acids and conjugated linoleic acids are altered in lactating dairy cows fed a milk fat-depressing diet. Journal of Nutrition 130, 2568–2574.Google Scholar
Schmitt, E, Ballou, MA, Correa, MN, DePeters, EJ, Drackley, JK and Loor, JJ 2011. Dietary lipid during the transition period to manipulate subcutaneous adipose tissue peroxisome proliferator-activated receptor-γ co-regulator and target gene expression. Journal of Dairy Science 94, 5913–5925.Google Scholar
Shingfield, KJ, Bernard, L, Leroux, C and Chilliard, Y 2010. Role of trans fatty acids in the nutritional regulation of mammary lipogenesis in ruminants. Animal 4, 1140–1166.Google Scholar
Shingfield, KJ, Chilliard, Y, Toivonen, V, Kairenius, P and Givens, DI 2008. Trans fatty acids and bioactive lipids in ruminant milk. Advances in Experimental Medicine and Biology 606, 3–65.Google Scholar
Shingfield, KJ, Reynolds, CK, Hervás, G, Griinari, JM, Grandison, AS and Beever, DE 2006. Examination of the persistency of milk fatty acid composition responses to fish oil and sunflower oil in the diet of dairy cows. Journal of Dairy Science 89, 714–732.Google Scholar
Shingfield, KJ, Ahvenjärvi, S, Toivonen, V, Äröla, A, Nurmela, KVV, Huhtanen, P and Griinari, JM 2003. Effect of dietary fish oil on biohydrogenation of fatty acids and milk fatty acid content in cows. Animal Science 77, 165–179.Google Scholar
Thering, BJ, Graugnard, DE, Piantoni, P and Loor, JJ 2009. Adipose tissue lipogenic gene networks due to lipid feeding and milk fat depression in lactating cows. Journal of Dairy Science 92, 4290–4300.Google Scholar
Toral, PG, Hervás, G, Gómez-Cortés, P, Frutos, P, Juárez, M and de la Fuente, MA 2010. Milk fatty acid profile and dairy sheep performance in response to diet supplementation with sunflower oil plus incremental levels of marine algae. Journal of Dairy Science 93, 1655–1667.Google Scholar
Toral, PG, Belenguer, A, Shingfield, KJ, Hervás, G, Toivonen, V and Frutos, P 2012. Fatty acid composition and bacterial community changes in the rumen fluid of lactating sheep fed sunflower oil plus incremental levels of marine algae. Journal of Dairy Science 95, 794–806.Google Scholar
Toral, PG, Bernard, L, Delavaud, C, Gruffat, D, Leroux, C and Chilliard, Y 2013. Effects of fish oil and additional starch on tissue fatty acid profile and lipogenic gene mRNA abundance in lactating goats fed a diet containing sunflower-seed oil. Animal 7, 948–956.Google Scholar
Vernon, RG 1980. Lipid metabolism in the adipose tissue of ruminant animals. Progress in Lipid Research 19, 23–106.Google Scholar
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