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Transcriptional regulation of acetyl-CoA carboxylase α isoforms in dairy ewes during conjugated linoleic acid induced milk fat depression

Published online by Cambridge University Press:  26 April 2016

E. Ticiani ,
M. Urio ,
R. Ferreira ,
K. J. Harvatine  and
D. E. De Oliveira
E. Ticiani
Affiliation:
Department of Animal Production, Santa Catarina State University, Lages, Santa Catarina, 88520-000, Brazil
M. Urio
Affiliation:
Department of Animal Production, Santa Catarina State University, Lages, Santa Catarina, 88520-000, Brazil
R. Ferreira
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

Feeding trans-10, cis-12 CLA to lactating ewes reduces milk fat by down-regulating expression of enzymes involved in lipid synthesis in the mammary gland and increases adipose tissue lipogenesis. Acetyl-CoA carboxylase α (ACC-α) is a key regulated enzyme in de novo fatty acid synthesis and is decreased by CLA. In the ovine, the ACC-α gene is expressed from three tissue-specific promoters (PI, PII and PIII). This study evaluated promoter-specific ACC-α expression in mammary and adipose tissue of lactating cross-bred Lacaune/Texel ewes during milk fat depression induced by rumen-unprotected trans-10, cis-12 CLA supplement. In all, 12 ewes arranged in a completely randomized design were fed during early, mid and late lactation one of the following treatments for 14 days: Control (forage+0.9 kg of concentrate on a dry matter basis) and CLA (forage+0.9 kg of concentrate+27 g/day of CLA (29.9% trans-10, cis-12)). Mammary gland and adipose tissue biopsies were taken on day 14 for gene expression analysis by real-time PCR. Milk fat yield and concentration were reduced with CLA supplementation by 27%, 21% and 35% and 28%, 26% and 42% during early, mid and late lactation, respectively. Overall, our results suggest that trans-10, cis-12 CLA down-regulates mammary ACC-α gene expression by decreasing expression from PII and PIII in mammary gland and up-regulates adipose ACC-α gene expression by increasing expression from PI.

Keywords

gene expressionlactating ewemilk fat depression
Type
Research Article
Information
animal , Volume 10 , Issue 10 , October 2016 , pp. 1677 - 1683
Copyright
© The Animal Consortium 2016 

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References

Anderson, SM, Rudolph, MC, McManaman, JL and Neville, MC 2007. Secretory activation in the mammary gland: it’s not just about milk protein synthesis. Breast Cancer Research 9, 204–217.Google Scholar
Association of Official Analytical Chemists 2004. Official methods of analysis, vol. 2, 18th edition. AOAC, Arlington, VA, USA.Google Scholar
Baldin, M, Dresch, R, Martelo, L, Souza, J and Oliveira, DE 2013a. Dose–response relationship in dairy ewes fed a rumen unprotected CLA supplement. Livestock Science 158, 91–94.CrossRefGoogle Scholar
Baldin, M, Dresch, R, Souza, J, Fernandes, D, Gama, MAS, Harvatine, KJ and Oliveira, DE 2014. CLA induced milk fat depression reduced dry matter intake and improved energy balance in dairy goats. Small Ruminant Research 116, 44–50.Google Scholar
Baldin, M, Gama, MAS, Dresch, R, Harvatine, KJ and Oliveira, DE 2013b. A rumen unprotected conjugated linoleic acid supplement inhibits milk fat synthesis and improves energy balance in lactating goats. Journal of Animal Science 91, 3305–3314.Google Scholar
Barber, MC, Clegg, RA, Travers, MT and Vernon, RG 1997. Lipid metabolism in the lactating mammary gland. Biochimica et Biophysica Acta 1347, 101–126.Google Scholar
Barber, MC, Price, NT and Travers, MT 2005. Structure and regulation of acetyl-CoA carboxylase genes of metazoa. Biochimica et Biophysica Acta 1733, 1–28.CrossRefGoogle ScholarPubMed
Barber, MC and Travers, MT 1995. Cloning and characterisation of multiple acetyl-CoA carboxylase transcripts in ovine adipose tissue. Gene 154, 271–275.CrossRefGoogle ScholarPubMed
Barber, MC and Travers, MT 1998. Elucidation of a promoter activity that directs the expression of acetyl-CoA carboxylase a with an alternative N-terminus in a tissue-restricted fashion. The Biochemical Journal 333, 17–25.CrossRefGoogle Scholar
Barber, MC, Vallance, A, Kennedy, H and Travers, M 2003. Induction of transcripts derived from promoter III of the acetyl-CoA carboxylase-α gene in mammary gland is associated with recruitment of SREBP-1 to a region of the proximal promoter defined by a DNase I hypersensitive site. The Biochemical Journal 375, 489–501.CrossRefGoogle ScholarPubMed
Bauman, DE, Harvatine, KJ and Lock, AL 2011. Rumen-derived bioactive fatty acids, and the regulation of milk fat synthesis. Annual Review of Nutrition 31, 299–319.Google Scholar
Baumgard, LH, Corl, BA, Dwyer, DA, Sæbø, A and 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–R185.CrossRefGoogle ScholarPubMed
Brown, JM and McIntosh, MK 2003. Conjugated linoleic acid in humans: regulation of adiposity and insulin sensitivity. The Journal of Nutrition 133, 3041–3046.CrossRefGoogle ScholarPubMed
Castaneda-Gutierrez, E, Overton, TR, Butler, WR and Bauman, DE 2005. Dietary supplements of two doses of calcium salts of conjugated linoleic acid during the transition period and early lactation. Journal of Dairy Science 88, 1078–1089.Google Scholar
de Veth, MJ, Griinari, JM, Pfeiffer, AM and Bauman, DE 2004. Effect of CLA on milk fat synthesis in dairy cows: comparison of inhibition by methyl esters and free fatty acids, and relationships among studies. Lipids 39, 365–372.Google Scholar
Eberlé, D, Hegarty, B, Bossard, P, Ferré, P and Foufelle, F 2004. SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86, 839–848.Google Scholar
Fernandes, D, Gama, MAS, Ribeiro, CVDM, Lopes, FCF 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.Google Scholar
Goldstein, JL, DeBose-Boyd, RA and Brown, MS 2006. Protein sensors for membrane sterols. Cell 124, 35–46.CrossRefGoogle ScholarPubMed
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. The Journal of Nutrition 136, 2468–2474.Google Scholar
Harvatine, KJ, Perfield, JW II 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. The Journal of Nutrition 139, 849–854.Google Scholar
Horton, JD, Shah, NA and Warrington, JA 2003. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proceedings of the National Academy of Sciences of the United States of America 100, 12027–12032.CrossRefGoogle ScholarPubMed
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.Google Scholar
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
Kim, KH 1997. Regulation of mammalian acetyl-coenzyme A carboxylase. Annual Review of Nutrition 17, 77–99.CrossRefGoogle ScholarPubMed
Lengi, AJ and Corl, BA 2010. Factors influencing the differentiation of bovine preadipocytes in vitro. Journal of Animal Science 88, 1999–2008.Google Scholar
Mao, J, Marcos, S, Davis, S, Burzlaff, J and Seyfert, H 2001. Genomic distribution of three promoters of the bovine gene encoding acetyl-CoA carboxylase α and evidence that the nutritionally regulated promoter I contains a repressive element different from that in rat. The Biochemical Journal 358, 127–135.Google Scholar
Molenaar, A, Mao, J, Oden, K and Seyfert, HM 2003. All three promoters of the acetyl-coenzyme-A carboxylase α-encoding gene are expressed in mammary epithelial cells of ruminants. The Journal of Histochemistry and Cytochemistry 51, 1073–1081.CrossRefGoogle ScholarPubMed
National Research Council 2007. Nutrient requirements of small ruminants: sheep, goats, cervids, and new world camelids, 1st edition. National Academy Press, Washington, DC, USA.Google Scholar
Odens, LJ, Burgos, R, Innocenti, M, VanBaale, MJ and Baumgard, LH 2007. Effects of varying doses of supplemental conjugated linoleic acid on production and energetic variables during the transition period. Journal of Dairy Science 90, 293–305.Google Scholar
Oliveira, DE, Bauman, DE and Harvatine, KJ 2014. Conjugated linoleic acid (CLA) trans-10, cis-12 decreases ACC-α gene expression in lactating mammary gland by decreasing specific transcripts from different promoters. In: Joint Annual Meeting, 2014, Kansas City. Abstracts. Indianapolis: ADSA/ASAS, 2014. p. 607. Journal Animal of Science 97 (E-suppl. 1).Google Scholar
Oliveira, DE, Gama, MAS, 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
Rudolph, MC, Monks, J, Burns, V, Phistry, M, Marians, R, Foote, MR and 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, E918–E927.CrossRefGoogle ScholarPubMed
SAS Institute 2009. SAS/STAT: user’s guide, version 9.2. SAS Institute Inc., Cary, NC, USA.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.CrossRefGoogle ScholarPubMed
Travers, M, Vallance, A, Gourlay, H, Gill, C, Klein, I, Bottema, C and Barber, M 2001. Promoter I of the ovine acetyl-CoA carboxylase-α gene: an E-box motif at −114 in the proximal promoter binds upstream stimulatory factor (USF)-1 and USF-2 and acts as an insulin-response sequence in differentiating adipocytes. The Biochemical Journal 359, 273–284.Google Scholar
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Van Roy, N, 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, research0034.Google Scholar