Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T01:14:52.616Z Has data issue: false hasContentIssue false

The effect of long term under- and over-feeding on the expression of genes related to lipid metabolism in mammary tissue of sheep

Published online by Cambridge University Press:  01 December 2014

Eleni Tsiplakou*
Affiliation:
Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, GR-11855, Athens, Greece
Emmanouil Flemetakis
Affiliation:
Department of Agricultural Biotechnology, Agricultural University of Athens, Iera Odos 75, GR-11855, Athens, Greece
Evangelia-Diamanto Kouri
Affiliation:
Department of Agricultural Biotechnology, Agricultural University of Athens, Iera Odos 75, GR-11855, Athens, Greece
Kyriaki Sotirakoglou
Affiliation:
Department of Mathematics and Statistics, Agricultural University of Athens, Iera Odos 75, GR-11855, Athens, Greece
George Zervas
Affiliation:
Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, GR-11855, Athens, Greece
*
*For correspondence; e-mail: [email protected]

Abstract

Milk fatty acid (FA) synthesis by the mammary gland involves expression of a large number of genes whose nutritional regulation remains poorly defined. In this study, we examined the effect of long-term under- and over-feeding on the expression of genes (acetyl Co A carboxylase, ACC; fatty acid synthetase, FAS; lipoprotein lipase, LPL; stearoyl Co A desaturase, SCD; peroxisome proliferator activated receptor γ2, PPARγ2; sterol regulatory element binding protein-1, SREBP-1c; and hormone sensitive lipase, HSL) related to FA metabolism in sheep mammary tissue (MT). Twenty-four lactating sheep were divided into three homogenous sub-groups and fed the same ration in quantities covering 70% (underfeeding), 100% (control) and 130% (overfeeding) of their energy and crude protein requirements. The results showed a significant reduction of mRNA of ACC, FAS, LPL and SCD in the MT of underfed sheep, and a significant increase on the mRNA of LPL and SREBP-1c in the MT of overfed compared with the control respectively. In conclusion, the negative, compared to positive, energy balance in sheep down-regulates ACC, FAS, LPL, SCD, SREBP-1c and PPARγ2 expression in their MT which indicates that the decrease in nutrient availability may lead to lower rates of lipid synthesis.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2014 

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

Ahnadi, CE, Beswick, N, Delbecchi, L, Kennely, JJ & Lacasse, P 2002 Addition of fish oil to diets for dairy cows. II. Effects on milk fat and gene expression of mammary lipogenic enzymes. Journal of Dairy Research 69 521531Google Scholar
Bauman, DE & Griinari, JM 2003 Nutritional regulation of milk fat synthesis. Annual Review of Nutrition 23 203227Google Scholar
Bernard, L, Rouel, J, Leroux, C, Ferlay, A, Faulconnier, Y, Legrand, P & Chiliard, Y 2005 Mammary lipid metabolism and fatty acid secretion in Alpine goats fed vegetable lipids. Journal of Dairy Science 88 14781489Google 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 67108CrossRefGoogle ScholarPubMed
Bernard, L, Leroux, C & Chilliard, Y 2013 Nutritional regulation of mammary lipogenesis and milk fat in ruminant: contribution to sustainable milk production. Revista Colombiana de Ciencias Pecuarias 26 22302Google Scholar
Bionaz, M & Loor, JJ 2007 Identification of reference genes for quantitative real-time PCR in the bovine mammary gland during the lactation cycle. Physiological Genomics 29 312319Google Scholar
Bionaz, M & Loor, JJ 2008 Genes networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 9 366387Google Scholar
Bionaz, M, Chen, S, Khan, MJ & Loor, JJ 2013 Functional role of PPARs in ruminants: potential targets for fine-tuning metabolism during growth and lactation. PPAR Research 2013 128Google Scholar
Brennan, KM, Michal, JJ, Ramsey, JJ & Johnson, KA 2009 Body weight loss in beef cows: I. The effect of increased β-oxidation on messenger ribonucleic acid levels of uncoupling proteins two and three and peroxisome proliferator-activated receptor in skeletal muscle. Journal of Animal Science 87 28602866CrossRefGoogle ScholarPubMed
Carcangiu, V, Mura, MC, Daga, C, Luridiana, S, Bodano, S, Sanna, GA, Diaz, ML & Cosso, G 2013 Association between SREBP-1 gene expression in mammary gland and milk fat yield in Sarda breed sheep. Meta Gene 1 4349Google Scholar
Chilliard, Y, Bocquier, F & Doreau, M 1998 Digestive and metabolic adaptations of ruminants to undernutrition, and consequences on reproduction. Reproduction Nutrition Development 38 131152Google Scholar
Fielging, BA & Frayn, KN 1998 Lipoprotein lipase and the disposition of fatty acids. British Journal of Nutrition 80 495502Google Scholar
Jensen, DR, Gavigan, S, Sawicki, V, Witsell, DL, Eckel, RH & Neville, MC 1994 Regulation of lipoprotein lipase activity and mRNA in the mammary gland of the lactating mouse. Biochemical Journal 298 321327Google Scholar
Kuhla, B, Gors, S & Metges, CC 2011 Hypothalamic orexin A expression and the involvement of AMPK and PPAR-gamma signalling in energy restricted dairy cows. Archiv für Tierzucht-Archives of Animal Breeding 54 567579Google Scholar
Lin, X, Luo, J, Zhang, L, Wang, W & Gou, D 2013 MiR-103 controls milk fat accumulation in goat (Capra hircus) mammary gland during lactation. PLoS ONE 8 e79258Google Scholar
Loor, JJ, Everts, RE, Bionaz, M, Dann, HM, Morin, DE, Oliveira, R, Rodriguez-Zas, SL, Drackley, JK & Lewin, HA 2007 Nutrition-induced ketosis alters metabolic and signaling gene networks in liver of periparturient dairy cows. Physiological Genomics 32 105116CrossRefGoogle ScholarPubMed
Ma, L & Corl, BA 2012 Transcriptional regulation of lipid synthesis in bovine mammary epithelial cells by sterol regulatory element binding protein-1. Journal of Dairy Science 95 37433755Google Scholar
Martín-Hidalgo, A, Huerta, L, Alvarez, N, Alegría, G, Del Val Toledo, M & Herrera, E 2005 Expression, activity, and localization of hormone-sensitive lipase in rat mammary gland during pregnancy and lactation. Journal of Lipid Research 46 458668CrossRefGoogle ScholarPubMed
Miller, N, Delbecchi, L, Petitclerc, D, Wagner, GF, Talbot, BG & Lacasse, P 2006 Effect of stage of lactation and parity on Mammary gland cell renewal. Journal of Dairy Science 89 46694677CrossRefGoogle ScholarPubMed
Nørgaard, JV, Nielsen, MO, Theil, PK, Sørensen, MT, Safayi, S & Sejrsen, K 2008 Development of mammary glands of fat sheep submitted to restricted feeding during late pregnancy. Small Ruminant Research 76 155165Google Scholar
Ollier, S, Robert-Granié, C, Bernard, L, Chilliard, Y & 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 560567Google Scholar
Piperova, LS, Teter, BB, Bruckental, I, Sampugna, J, Millis, SE, Yurawecz, MP, Fritsche, J, Ku, K & 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 25682574Google Scholar
Ramakers, C, Ruijter, JM, Deprez, RH & Moorman, AF 2003 Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339 6266Google Scholar
Rudolph, MC, Monks, J, Burns, V, Phistry, M, Marians, R, Foote, M, Bauman, DE, Anderson, SM & Neville, MC 2010 Sterol regulatory element binding protein and dietary lipid regulation of fatty acid synthesis in the mammary epithelium. American Journal of Physiology Endocrinology and Metabolism 299 E918E927CrossRefGoogle ScholarPubMed
Shi, HB, Luo, J, Yao, DW, Zhu, JJ, Xu, HF, Shi, HP & Loor, JJ 2013 Peroxisome proliferator-activated receptor –γ stimulates the synthesis of monounsaturated fatty acids in dairy goat mammary epithelial cells via the control of stearoyl-coenzyme A desaturase. Journal of Dairy Science 96 78447853Google Scholar
Shi, HB, Zhao, WS, Luo, J, Yao, DW, Sun, YT, Li, J, Shi, HP & Loor, JJ 2014 Peroxisome proliferator-activated receptor γ1 and γ2 isoforms alter lipogenic gene networks in goat mammary epithelial cells to different extents. Journal of Dairy Science 97 54375447Google Scholar
Shingfield, KJ, Bonnet, M & Scollan, ND 2013. Recent developments in altering the fatty acid composition of ruminant-derived foods. Animal 7 132162Google Scholar
Tsiplakou, E, Chadio, S & Zervas, G 2012 The effect of long term under- and over- feeding of sheep on milk and plasma fatty acids profile and on insulin and leptin concentrations. Journal of Dairy Research 79 192200Google 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 0034.10034.11Google 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 3639Google Scholar