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Peroxisome proliferator-activated receptor gamma (PPARγ) agonist fails to overcome trans-10, cis-12 conjugated linoleic acid (CLA) inhibition of milk fat in dairy sheep

Published online by Cambridge University Press:  10 November 2017

E. C. Sandri ,
M. Camêra ,
E. M. Sandri ,
K. J. Harvatine  and
D. E. De Oliveira
E. C. Sandri
Affiliation:
Department of Animal Production, Santa Catarina State University, Lages, Santa Catarina 88520-000, Brazil
M. Camêra
Affiliation:
Department of Animal Production, Santa Catarina State University, Lages, Santa Catarina 88520-000, Brazil
E. M. Sandri
Affiliation:
Department of Animal Science, Santa Catarina State University, Chapecó, Santa Catarina 89815-630, Brazil
K. J. Harvatine
Affiliation:
Department of Animal Science, Penn State University, University Park, PA 16802, USA
D. E. De Oliveira*
Affiliation:
Department of Animal Production, Santa Catarina State University, Lages, Santa Catarina 88520-000, Brazil
*
†E-mail: [email protected]; [email protected]
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Abstract

The trans-10, cis-12 conjugated linoleic acid (CLA) causes milk fat depression by downregulating expression of genes and transcription factors involved in lipogenesis and it has been proposed that peroxisome proliferator-activated receptor gamma (PPARγ) can be inhibited by trans-10, cis-12 CLA. The PPARγ is a nuclear receptor activated by natural or synthetic ligands and promotes expression of lipogenic genes and its effect on mammary lipogenesis and the interaction with trans-10, cis-12 CLA in lactating ewes was evaluated using thiazolidinedione (TZD), a chemical PPARγ agonist. A total of 24 lactating ewes were randomly assigned to one of the following treatments for 7 days: (1) Control (5 ml/day of saline solution); (2) TZD (4 mg/kg of BW/day in 5 ml of saline solution); (3) CLA (27 g/day with 29.9% of trans-10, cis-12); (4) TZD+CLA. Compared with Control, milk fat content was not changed by TZD, but was decreased 22.3% and 20.5% by CLA and TZD+CLA treatments. In the mammary gland, TZD increased PPARγ gene expression by 174.8% and 207.8% compared with Control and TZD+CLA treatments, respectively. Conjugated linoleic acid reduced sterol regulatory element-binding transcription protein 1 (SREBP1) gene expression 89.2% and 75.3% compared with Control and TZD+CLA, respectively, demonstrating that TZD fails to overcome CLA inhibition of SREBP1 signaling. In adipose tissue, the expression of SREBP1 and stearoyl CoA desaturase 1 (SCD1) genes were increased by the TZD+CLA treatment, compared with the other treatments. Conjugated linoleic acid decreased milk fat concentration and expression of lipogenic genes, while TZD had no effect on milk fat concentration, expression of lipogenic enzymes or regulators in the mammary gland and failed to overcome the inhibition of these by CLA. Therefore, CLA inhibition of milk fat synthesis was independent of the PPARγ pathway in lactating dairy ewes.

Keywords

gene expressionmilk fat depressionmilk fat synthesisovinethiazolidinedione
Type
Research Article
Information
animal , Volume 12 , Issue 7 , July 2018 , pp. 1405 - 1412
Copyright
© The Animal Consortium 2017 

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References

Association of Official Analytical Chemists (AOAC) 2000. Official methods of analysis, Volume 1. AOAC, Arlington, VA, USA.Google Scholar
Baumgard, LH, Corl, BA, Dwyer, DA, Saebo, A and Bauman, DE 2000. Identification of the conjugated linoleic acid isomer that inhibits fat synthesis. American Journal of Physiology Regulatory Integrative and Comparative Physiology 278, 179–184.CrossRefGoogle ScholarPubMed
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 1–28.Google ScholarPubMed
Bionaz, M, Hurley, W and Loor, JJ 2012. Milk protein synthesis in the lactating mammary gland: insights from transcriptomics analyses. In Milk protein (ed. WL Hurley), pp. 285–324. Intech Open Science, London, UK.Google Scholar
Bionaz, M and Loor, JJ 2008. Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 9, 1–21.CrossRefGoogle ScholarPubMed
Bontempo, V, Sciannimanico, D, Pastorelli, G, Rossi, R, Rosi, F and Corino, C 2004. Dietary conjugated linoleic acid positively affects immunologic variables in lactating sows and piglets. Journal of Nutrition 134, 817–824.CrossRefGoogle ScholarPubMed
Brown, JM, Boysen, MS, Jensen, SS, Morrison, RF, Storkson, J, Lea-Currie, R, Pariza, M, Mandrup, S and McIntosh, MK 2003. Isomer-specific regulation of metabolism and PPARγ signaling by CLA in human preadipocytes. Journal of Lipid Research 44, 1287–1300.CrossRefGoogle ScholarPubMed
Fernandes, D, Gama, MA, Ribeiro, CV, Lopes, FC and Oliveira, DE 2014. Milk fat depression and energy balance in stall-fed dairy goats supplemented with increasing doses of conjugated linoleic acid methyl esters. Animal 8, 587–595.CrossRefGoogle ScholarPubMed
Harvatine, KJ and Bauman, DE 2006. SREBP1 and Thyroid Hormone Responsive Spot14 (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.Google Scholar
Harvatine, KJ, Perfield, JW II and Bauman, DB 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.CrossRefGoogle ScholarPubMed
He, G, Sung, YM, DiGiovanni, J and Fischer, SM 2006. Thiazolidinediones inhibit insulin-like growth factor-induced activation of p70s6 kinase and suppress insulin-like growth factor-i tumor-promoting activity. Cancer Research 66, 1873–1879.CrossRefGoogle Scholar
Hussein, M, Harvatine, KH, Weerasinghe, WMPB, Sinclair, LA and Bauman, DE 2013. Conjugated linoleic acid-induced milk fat depression in lactating ewes is accompanied by reduced expression of mammary genes involved in lipid synthesis. Journal of Dairy Science 96, 3825–3834.CrossRefGoogle ScholarPubMed
Institut National De La Recherche Agronomique 2007. Alimentation des bovins, ovins et caprins: Besoins des animaux – Valeurs des aliments – Tables Inra Versailles. Ed. Quae, Versalhes, França.Google Scholar
Kadegowda, AKG, Bionaz, M, Piperova, LS, Erdman, RA and Loor, JJ 2009. Peroxisome proliferator-activated receptor-γ activation and long-chain fatty acids alter lipogenic gene networks in bovine mammary epithelial cells to various extents. Journal of Dairy Science 92, 4276–4289.CrossRefGoogle ScholarPubMed
Kennedy, A, Chung, S, LaPoint, K, Fabiyi, O and McIntosh, MK 2008. Trans-10, cis-12 conjugated linoleic acid antagonizes ligand-dependent PPARγ activity in primary cultures of human adipocytes. Journal of Nutrition 138, 455–461.CrossRefGoogle ScholarPubMed
Kinsella, JE 1972. Stearoyl CoA as a precursor of oleic acid and glycerolipids in mammary microsomes from lactating bovine: possible regulatory step in milk triglyceride synthesis. Lipids 7, 349–355.CrossRefGoogle Scholar
Lee, KN, Storkson, JM and Pariza, MW 1995. Dietary conjugated linoleic acid changes fatty acid composition in different tissues by decreasing monounsaturated fatty acids. IFT Annual Meet: Book of Abstracts 183.Google Scholar
Li, Y and Lazar, MA 2002. Differential gene regulation by PPARgamma agonist and constitutively active PPARgamma2. Molecular Endocrinology 16, 1040–1048.Google ScholarPubMed
Lock, AL, Teles, BM, Perfield, JW II, Bauman, DE and Sinclair, LA 2006. A conjugated linoleic acid supplement containing trans-10, cis-12 reduces milk fat synthesis in lactating sheep. Journal of Dairy Science 89, 1525–1532.CrossRefGoogle ScholarPubMed
Mackle, TR, Dwyer, DA, Ingvartsen, KL, Chouinard, PY, Lynch, JM, Barbano, DM and Bauman, DE 1999. Effects of insulin and amino acids on milk protein concentration and yield from dairy cows. Journal of Dairy Science 82, 1512–1524.CrossRefGoogle ScholarPubMed
Masters, N, McGuire, MA, Beerman, KA, Dasqupta, N and McGuire, MK 2002. Maternal supplementation with CLA decreases milk fat in humans. Lipids 37, 133–138.CrossRefGoogle ScholarPubMed
Medeiros, SR, Oliveira, DE, Aroeira, LJM, McGuire, MA, Bauman, DE and Lanna, DPD 2010. Effects of dietary supplementation of rumen-protected conjugated linoleic acid to grazing cows in early lactation. Journal of Dairy Science 93, 1126–1137.CrossRefGoogle ScholarPubMed
National Research Council (NRC) 2007. Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids. The National Academy Press, Washington, DC, USA. 384pp.Google Scholar
Oliveira, DE, Gama, MA, Fernandes, D, Tedeschi, LO and Bauman, DE 2012. An unprotected conjugated linoleic acid supplement decreases milk production and secretion of milk components in grazing dairy ewes. Journal of Dairy Science 95, 1437–1446.CrossRefGoogle ScholarPubMed
Park, Y, Albright, KJ, Storkson, JM, Liu, W, Cook, ME and Pariza, MW 1999. Changes in body composition in mice during feeding and withdrawal of dietary conjugated linoleic acid. Lipids 34, 243–248.CrossRefGoogle Scholar
Paton, CM and Ntambi, JM 2009. Biochemical and physiological function of stearoyl-CoA desaturase. The American Journal of Physiology – Endocrinology and Metabolism 297, 28–37.CrossRefGoogle ScholarPubMed
SAS 2009. User’s guide: statistics, version 9.2 edition. SAS Institute Inc., Cary, NC.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.CrossRefGoogle ScholarPubMed
Smith, KL, Stebulis, SE, Wadron, MR and Overton, TR 2007. Prepartum 2,4-thiazolidinedione alters metabolic dynamics and dry matter intake of dairy cows. Journal of Dairy Science 90, 3660–3670.CrossRefGoogle ScholarPubMed
Ticiani, E, Urio, M, Ferreira, R, Harvatine, KJ and Oliveira, DA 2016. Transcriptional regulation of acetyl-CoA carboxylase α isoforms in dairy ewes during conjugated linoleic acid induced milk fat depression. Animal 10, 1677–1683.Google ScholarPubMed
Tsiplakou, E, Flemetakis, E, Kouri, ED, Karalis, G, Sotirakoglou, K and Zervas, G 2015. The effect of long term under- and over-feeding on the expression of six major milk protein genes in the mammary tissue of sheep. Journal of Dairy Research 82, 257–264.CrossRefGoogle ScholarPubMed
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Roy, NV, De Paepe, A and Speleman, F 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, 1–12.CrossRefGoogle ScholarPubMed