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Extruded linseed alone or in combination with fish oil modifies mammary gene expression profiles in lactating goats

Published online by Cambridge University Press:  10 November 2017

Y. Faulconnier ,
L. Bernard ,
C. Boby ,
J. Domagalski ,
Y. Chilliard  and
C. Leroux
Y. Faulconnier
Affiliation:
INRA, UMR 1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
L. Bernard
Affiliation:
INRA, UMR 1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
C. Boby
Affiliation:
INRA, UMR 1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
J. Domagalski
Affiliation:
INRA, UMR 1213 Herbivores, 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, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
C. Leroux*
Affiliation:
INRA, UMR 1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR Herbivores, BP 10448, F-63000, Clermont-Ferrand, France
*
† E-mail: [email protected]
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Abstract

Nutrition is a major factor that regulates ruminant milk components, particularly its fatty acid (FA) composition, which is an important determinant of milk nutritional quality. In the mammary gland, milk component biosynthesis involves a large number of genes under nutritional regulation that are not well understood. Thus, the objective of the present study was to evaluate the effects of extruded linseeds (EL) alone or in combination with fish oil (ELFO) on goat mammary gene expression. In total, 14 goats were fed one of the following three diets: a natural grassland hay basal diet (CTRL) alone, CTRL supplemented with 530 g/day of EL, or 340 g/day of EL plus 39 g/day of fish oil (ELFO). Mammary secretory tissues were collected after slaughter on day 28, to determine the expression of 14 lipogenic genes and five lipogenic enzyme activities and transcriptomic profiles. The mRNA abundance decreased for SCD1 (P<0.1) with ELFO v. CTRL, and for AZGP1 (P<0.1) and ACSBG1 (P<0.05) decreased with EL v. ELFO and the CTRL diets (only for ACSBG1), respectively. Transcriptomic analyses performed using a bovine microarray revealed 344 and 314 differentially expressed genes (DEG) in the EL and ELFO diets, respectively, compared with the CTRL diet, with 76 common DEGs. In total, 21 and 27 DEGs were involved in lipid metabolism and transport class in the EL and ELFO v. the CTRL diets, respectively, with eight common genes (ALDH3B1, ALDH18A1, DGKD1, ENPP1, IL7, NSMAF, PI4KA and SERINC5) down-regulated by these two treatments. In EL v. CTRL diets, a gene network related to lipid metabolism and transport was detected. Although this network was not detected in the ELFO v. CTRL analysis, five genes known to be involved in lipid metabolism and transport were up-regulated (SREBF1, PPARG and GPX4) or down-regulated (FABP1 and ENPP6) by ELFO. The protein metabolism and transport biological processes were largely altered by both EL and ELFO v. CTRL diets without changes in major milk protein secretion. Amino acid metabolism was highlighted as an enriched network by Ingenuity Pathway Analysis and was similar to cellular growth and proliferation function. Two regulation networks centered on the estrogen receptor (ESR1) and a transcriptional factor (SP1) were identified in EL and ELFO v. CTRL diets. In conclusion, these results show that these two supplemented diets, which largely changed milk FA composition, had more effects on mRNA linked to protein metabolism and transport pathways than to lipid metabolism, and could affect mammary remodeling.

Keywords

nutrigenomicstranscriptomecaprinemammary glandlipid supplementation
Type
Research Article
Information
animal , Volume 12 , Issue 8 , August 2018 , pp. 1564 - 1575
Copyright
© The Animal Consortium 2017 

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References

Benjamini, Y and Hochberg, Y 1995. Controlling the false discovery rate –- a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57, 289–300.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, Rouel, J, Delavaud, C, Shingfield, KJ and Chilliard, Y 2015. Effect of extruded linseeds alone or in combination with fish oil on intake, milk production, plasma metabolite concentrations and milk fatty acid composition in lactating goats. Animal 9, 810–821.Google Scholar
Bionaz, M, Chen, S, Khan, MJ and Loor, JJ 2013. Functional role of PPARs in ruminants: potential targets for fine-tuning metabolism during growth and lactation. PPAR Research 684159, 28.Google Scholar
Bionaz, M and Loor, JJ 2008. Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 9, 366.Google Scholar
Chilliard, Y and Ferlay, A 2004. Dietary lipids and forages interactions on cow and goat milk fatty acid composition and sensory properties. Reproduction Nutrition Development 44, 467–492.Google Scholar
Chilliard, Y, Glasser, F, Ferlay, A, Bernard, L, Rouel, J and Doreau, M 2007. Diet, rumen biohydrogenation and nutritional quality of cow and goat milk fat. European Journal of Lipid Science and Technology 109, 828–855.Google Scholar
Chilliard, Y, Toral, PG, Shingfield, KJ, Rouel, J, Leroux, C and Bernard, L 2014. Effects of diet and physiological factors on milk fat synthesis, milk fat composition and lipolysis in the goat: a short review. Small Ruminant Research 122, 31–37.Google Scholar
Faulconnier, Y, Chilliard, Y, Torbati, MB and Leroux, C 2011. The transcriptomic profiles of adipose tissues are modified by feed deprivation in lactating goats. Comparative Biochemistry Physiology: Part D Genomics Proteomics 6, 139–149.Google ScholarPubMed
Frasor, J and Gibori, G 2003. Prolactin regulation of estrogen receptor expression. Trends in Endocrinology and Metabolism 14, 118–123.Google Scholar
Harvatine, KJ and 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, 2468–2474.CrossRefGoogle ScholarPubMed
Invernizzi, G, Thering, BJ, McGuire, MA, Savoini, G and Loor, JJ 2010. Sustained upregulation of stearoyl-CoA desaturase in bovine mammary tissue with contrasting changes in milk fat synthesis and lipogenic gene networks caused by lipid supplements. Functional & Integrative Genomics 10, 561–575.Google Scholar
Kairenius, P, Ärölä, A, Leskinen, H, Toivonen, V, Ahvenjärvi, S, Vanhatalo, A, Huhtanen, P, Hurme, T, Griinari, JM and Shingfield, KJ 2015. Dietary fish oil supplements depress milk fat yield and alter milk fatty acid composition in lactating cows fed grass silage-based diets. Journal of Dairy Science 98, 5653–5671.Google Scholar
Koulajian, K, Ivovic, A, Ye, KT, Desai, T, Shah, A, Fantus, IG, Ran, QT and Giacca, A 2013. Overexpression of glutathione peroxidase 4 prevents beta-cell dysfunction induced by prolonged elevation of lipids in vivo. American Journal of Physiology-Endocrinology and Metabolism 305, E254–E262.Google Scholar
Lerch, S, Shingfield, KJ, Ferlay, A, Vanhatalo, A and Chilliard, Y 2012. Rapeseed or linseed in grass-based diets: effects on conjugated linoleic and conjugated linolenic acid isomers in milk fat from Holstein cows over 2 consecutive lactations. Journal of Dairy Science 95, 7269–7287.Google Scholar
Leroux, C, Bernard, L, Faulconnier, Y, Rouel, J, de la Foye, A, Domagalski, J and Chilliard, Y 2016. Bovine mammary nutrigenomics and changes in the milk composition due to rapeseed or sunflower oil supplementation of high-forage or high-concentrate diets. Journal of Nutrigenetics and Nutrigenomics 9, 65–82.Google Scholar
Li, S, Hosseini, A, Danes, M, Jacometo, C, Liu, J and Loor, JJ 2016. Essential amino acid ratios and mTOR affect lipogenic gene networks and miRNA expression in bovine mammary epithelial cells. Journal of Animal Science and Biotechnology 7, 44.CrossRefGoogle ScholarPubMed
Mach, N, Jacobs, AA, Kruijt, L, van Baal, J and Smits, MA 2011. Alteration of gene expression in mammary gland tissue of dairy cows in response to dietary unsaturated fatty acids. Animal 5, 1217–1230.CrossRefGoogle ScholarPubMed
Mach, N, Zom, RL, Widjaja, HC, van Wikselaar, PG, Weurding, RE, Goselink, RM, van Baal, J, Smits, MA and van Vuuren, AM 2013. Dietary effects of linseed on fatty acid composition of milk and on liver, adipose and mammary gland metabolism of periparturient dairy cows. Journal of Animal Physiology and Animal Nutrition (Berl) 97 (suppl. 1), 89–104.CrossRefGoogle ScholarPubMed
Marchitelli, C, Crisa, A, Mostarda, E, Napolitano, F and Moioli, B 2013. Splicing variants of SERPINA1 gene in ovine milk: characterization of cDNA and identification of polymorphisms. PLoS ONE 8, e73020.CrossRefGoogle ScholarPubMed
Mazzucchelli, R and Durum, SK 2007. Interleukin-7 receptor expression: intelligent design. Nature Reviews Immunology 7, 144–154.Google Scholar
Merida, I, Avila-Flores, A and Merino, E 2008. Diacylglycerol kinases: at the hub of cell signalling. Biochemical Journal 409, 1–18.Google Scholar
Moustafa, T, Fickert, P, Magnes, C, Guelly, C, Thueringer, A, Frank, S, Kratky, D, Sattler, W, Reicher, H, Sinner, F, Gumhold, J, Silbert, D, Fauler, G, Höfler, G, Lass, A, Zechner, R and Trauner, M 2012. Alterations in lipid metabolism mediate inflammation, fibrosis, and proliferation in a mouse model of chronic cholestatic liver injury. Gastroenterology 142, 140–151.Google Scholar
Neve, R, Chang, CH, Scott, GK, Wong, A, Friis, RR, Hynes, NE and Benz, CC 1998. The epithelium-specific ets transcription factor ESX is associated with mammary gland development and involution. FASEB Journal 12, 1541–1550.Google Scholar
Oliver, JR, Kushwah, R and Hu, J 2012. Multiple roles of the epithelium-specific ETS transcription factor, ESE-1, in development and disease. Laboratory Investigation 92, 320–330.Google Scholar
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
Ollier, S, Robert-Granie, C, Bernard, L, Chilliard, Y and Leroux, C 2007. Mammary transcriptome analysis of food-deprived lactating goats highlights genes involved in milk secretion and programmed cell death. Journal of Nutrition 137, 560–567.Google Scholar
Pauciullo, A, Cosenza, G, D’Avino, A, Colimoro, L, Nicodemo, D, Coletta, A, Feligini, M, Marchitelli, C, Di Berardino, D and Ramunno, L 2010. Sequence analysis and genetic variability of stearoyl CoA desaturase (SCD) gene in the Italian Mediterranean river buffalo. Molecular and Cellular Probes 24, 407–410.Google Scholar
Russell, ST and Tisdale, MJ 2011. Studies on the anti-obesity activity of zinc-alpha(2)-glycoprotein in the rat. International Journal of Obesity 35, 658–665.Google Scholar
Schams, D, Kohlenberg, S, Amselgruber, W, Berisha, B, Pfaffl, MW and Sinowatz, F 2003. Expression and localisation of oestrogen and progesterone receptors in the bovine mammary gland during development, function and involution. Journal of Endocrinology 177, 305–317.Google Scholar
Sharp, JA, Lefevre, C and Nicholas, KR 2008. Lack of functional alpha-lactalbumin prevents involution in Cape fur seals and identifies the protein as an apoptotic milk factor in mammary gland involution. BMC Biology 6, 48.Google Scholar
Shi, H, Zhao, W, Zhang, C, Shahzad, K, Luo, J and Loor, JJ 2016. Transcriptome-wide analysis reveals the role of PPARγ controlling the lipid metabolism in goat mammary epithelial cells. PPAR Research 2016, 9195680.CrossRefGoogle ScholarPubMed
Steinberg, SJ, Morgenthaler, J, Heinzer, AK, Smith, KD and Watkins, PA 2000. Very long-chain acyl-CoA synthetases. Human “bubblegum” represents a new family of proteins capable of activating very long-chain fatty acids. Journal of Biological Chemistry 275, 35162–35169.Google Scholar
Tao, H, Chang, GJ, Xu, TL, Zhao, HJ, Zhang, K and Shen, XZ 2015. Feeding a high concentrate diet down-regulates expression of ACACA, LPL and SCD and modifies milk composition in lactating goats. PLoS ONE 10, e0130525.CrossRefGoogle ScholarPubMed
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
Toral, PG, Chilliard, Y, Rouel, J, Leskinen, H, Shingfield, KJ and Bernard, L 2015. Comparison of the nutritional regulation of milk fat secretion and composition in cows and goats. Journal of Dairy Science 98, 7277–7297.Google Scholar
Wei, J, Yee, C, Ramanathan, P, Bendall, LJ and Williamson, P 2011. Variation in immunophenotype of lactating mice. Journal of Reproductive Immunology 89, 178–184.Google Scholar
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