Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-23T07:25:46.224Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of short- and long-chain fatty acids on the expression of stearoyl-CoA desaturase and other lipogenic genes in bovine mammary epithelial cells

Published online by Cambridge University Press:  19 April 2013

A. A. A. Jacobs ,
J. Dijkstra ,
J. S. Liesman ,
M. J. VandeHaar ,
A. L. Lock ,
A. M. van Vuuren ,
W. H. Hendriks  and
J. van Baal
A. A. A. Jacobs
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
J. Dijkstra
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
J. S. Liesman
Affiliation:
Department of Animal Science, Michigan State University, East Lansing 48824, USA
M. J. VandeHaar
Affiliation:
Department of Animal Science, Michigan State University, East Lansing 48824, USA
A. L. Lock
Affiliation:
Department of Animal Science, Michigan State University, East Lansing 48824, USA
A. M. van Vuuren
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
W. H. Hendriks
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands Faculty of Veterinary Medicine, Utrecht University, PO Box 80163, 3508 TD Utrecht, The Netherlands
J. van Baal*
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
*
†E-mail: [email protected]
Get access

Abstract

Stearoyl-CoA desaturase (SCD) in the bovine mammary gland introduces a cis-double bond at the Δ9 position in a wide range of fatty acids (FA). Several long-chain polyunsaturated fatty acids (PUFA) inhibit expression of SCD, but information on the effect of short-chain fatty acids on mammary SCD expression is scarce. We used a bovine mammary cell line (MAC-T) to assess the effect of acetic acid (Ac) and β-hydroxybutyric acid (BHBA) in comparison with the effect of various long-chain fatty acids on the mRNA expression of the lipogenic enzymes SCD, acetyl-CoA carboxylase (ACACA), fatty acid synthase (FASN) and their associated gene regulatory proteins sterol regulatory element binding transcription factor 1 (SREBF1), insulin-induced gene 1 protein (INSIG1) and peroxisome proliferator-activated receptor alpha (PPARA)and peroxisome proliferator-activated receptor delta (PPARD) by quantitative real-time PCR. MAC-T cells were treated for 12 h without FA additions (CON) or with either 5 mM Ac, 5 mM BHBA, a combination of 5 mM Ac + 5 mM BHBA, 100 μM C16:0, 100 μM C18:0, 100 μM C18:1 cis-9, 100 μM C18:1 trans-11, 100 μM C18:2 cis-9,12 or 100 μM C18:3 cis-9,12,15. Compared with control, mRNA expression of SCD1 was increased by Ac (+61%) and reduced by C18:1 cis-9 (−61%), C18:2 cis-9,12 (−84%) and C18:3 cis-9,12,15 (−88%). In contrast to native bovine mammary gland tissue, MAC-T cells did not express SCD5. Expression of ACACA was increased by Ac (+44%) and reduced by C18:2 cis-9,12 (−48%) and C18:3 cis-9,12,15 (−49%). Compared with control, FASN expression was not significantly affected by the treatments. The mRNA level of SREBF1 was not affected by Ac or BHBA, but was reduced by C18:1 cis-9 (−44%), C18:1 trans-11 (−42%), C18:2 cis-9,12 (−62%) and C18:3 cis-9,12,15 (−68%) compared with control. Expression of INSIG1 was downregulated by C18:0 (−37%), C18:1 cis-9 (−63%), C18:1 trans-11 (−53%), C18:2 cis-9,12 (−81%) and C18:3 cis-9,12,15 (−91%). Both PPARA and PPARD expression were not significantly affected by the treatments. Our results show that Ac upregulated mRNA expression of SCD1 and ACACA in MAC-T cells. The opposite effect of the PUFA C18:2 cis-9,12 and C18:3 cis-9,12,15 on the these genes and the failure of Ac to mimic the PUFA-inhibited SREBF1 and INSIG1 mRNA expression, suggest that Ac can stimulate mammary lipogenesis via a transcriptional regulatory mechanism different from PUFA.

Keywords

mammary glandstearoyl-CoA desaturase (SCD)lipogenic gene expressionshort-chain fatty acids
Type
Physiology and functional biology of systems
Information
animal , Volume 7 , Issue 9 , September 2013 , pp. 1508 - 1516
Copyright
Copyright © The Animal Consortium 2013 

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

Bannink, A, Kogut, J, Dijkstra, J, France, J, Kebreab, E, Van Vuuren, AM, Tamminga, S 2006. Estimation of the stoichiometry of volatile fatty acid production in the rumen of lactating cows. Journal of Theoretical Biology 238, 36–51.CrossRefGoogle ScholarPubMed
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, 67–108.Google Scholar
Bhattacharya, A, Banu, J, Rahman, M, Causey, J, Fernandes, G 2006. Biological effects of conjugated linoleic acids in health and disease. Journal of Nutritional Biochemistry 17, 789–810.Google Scholar
Bionaz, M, Loor, JJ 2008. Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 9, 366.Google Scholar
Bligh, EG, Dyer, WJ 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.Google Scholar
Caldari-Torres, C, Lock, AL, Staples, CR, Badinga, L 2011. Performance, metabolic, and endocrine responses of periparturient Holstein cows fed 3 sources of fat. Journal of Dairy Science 94, 1500–1510.CrossRefGoogle ScholarPubMed
Chilliard, Y, Ferlay, A, Mansbridge, RM, Doreau, M 2000. Ruminant milk fat plasticity: nutritional control of saturated, polyunsaturated, trans and conjugated fatty acids. Annales de Zootechnie 49, 181–205.CrossRefGoogle Scholar
Dong, XY, Tang, SQ, Chen, JD 2012. Dual functions of Insig proteins in cholesterol homeostasis. Lipids in Health and Disease 18, 173.Google Scholar
Feige, JN, Gelman, L, Michalik, L, Desvergne, B, Wahli, W 2006. From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Progress in Lipid Research 45, 120–159.CrossRefGoogle ScholarPubMed
Forsberg, NE, Baldwin, RL, Smith, NE 1984. Roles of acetate and its interactions with glucose and lactate in cow mammary tissue. Journal of Dairy Science 67, 2247–2254.Google Scholar
Goselink, RM, van Baal, J, Widjaja, HC, Dekker, RA, Zom, RL, de Veth, MJ, van Vuuren, AM 2013. Effect of rumen-protected choline supplementation on liver and adipose gene expression during the transition period in dairy cattle. Journal of Dairy Science 96, 1102–1116.CrossRefGoogle ScholarPubMed
Harvatine, KJ, Bauman, DE 2006. SREBP-1 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.Google Scholar
Harvatine, KJ, Boisclair, YR, Bauman, DE 2009. Recent advances in the regulation of milk fat synthesis. Animal 3, 40–54.Google Scholar
Huynh, HT, Robitaille, G, Turner, JD 1991. Establishment of bovine mammary epithelial cells (MAC-T): an in vitro model for bovine lactation. Experimental Cell Research 197, 191–199.Google Scholar
Invernizzi, G, Thering, BJ, McGuire, MA, Savoini, G, 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
Jacobs, AAA, Dijkstra, J, Hendriks, WH, van Baal, J, van Vuuren, AM 2013. Comparison between stearoyl-CoA desaturase expression in milk somatic cells and in mammary tissue of lactating dairy cows. Journal of Animal Physiology and Animal Nutrition 97, 353–362.CrossRefGoogle ScholarPubMed
Jacobs, AAA, van Baal, J, Smits, MA, Taweel, HZH, Hendriks, WH, van Vuuren, AM, 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.Google Scholar
Jayan, G, Herbein, J 2000. “Healthier” dairy fat using trans-vaccenic acid. Nutrition & Food Science 30, 304–309.Google Scholar
Jump, DB, Clarke, SD 1999. Regulation of gene expression by dietary fat. Annual Review of Nutrition 19, 63–90.Google Scholar
Kadegowda, AKG, Bionaz, M, Piperova, LS, Erdman, RA, 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.Google Scholar
Kang, K, Hatano, B, Lee, CH 2007. PPAR delta agonists and metabolic diseases. Current Atherosclerosis Reports 9, 72–77.CrossRefGoogle ScholarPubMed
Kast-Woelbern, HR, Dana, SL, Cesario, RM, Sun, L, de Grandpre, LY, Brooks, ME, Osburn, DL, Reifel-Miller, A, Klausing, K, Leibowitz, MD 2004. Rosiglitazone induction of Insig-1 in white adipose tissue reveals a novel interplay of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein in the regulation of adipogenesis. Journal of Biological Chemistry 279, 23908–23915.Google Scholar
Keating, AF, Kennelly, JJ, Zhao, FQ 2006. Characterization and regulation of the bovine stearoyl-CoA desaturase gene promoter. Biochemical and Biophysical Research Communications 344, 233–240.CrossRefGoogle ScholarPubMed
Kelsey, JA, Corl, BA, Collier, RJ, Bauman, DE 2003. The effect of breed, parity, and stage of lactation on conjugated linoleic acid (CLA) in milk fat from dairy cows. Journal of Dairy Science 86, 2588–2597.Google Scholar
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, 3743–3755.CrossRefGoogle ScholarPubMed
Mosley, EE, Shafii, B, Moate, PJ, McGuire, MA 2006. Cis-9, trans-11 conjugated linoleic acid is synthesized directly from vaccenic acid in lactating dairy cattle. Journal of Nutrition 136, 570–575.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
Ntambi, JM, Miyazaki, M 2004. Regulation of stearoyl-CoA desaturases and role in metabolism. Progress in Lipid Research 43, 91–104.Google Scholar
Rakhshandehroo, M, Knoch, B, Müller, M, Kersten, S 2010. Peroxisome proliferator-activated receptor alpha target genes. PPAR Research, doi: 10.1155/2010/612089.Google Scholar
Reynolds, CM, Roche, HM 2010. Conjugated linoleic acid and inflammatory cell signaling. Prostaglandins, Leukotrienes and Essential Fatty Acids 82, 199–204.CrossRefGoogle Scholar
Sharma, I, Monga, R, Singh, N, Datta, TK, Singh, D 2012. Ovary-specific novel peroxisome proliferator activated receptors-gamma transcripts in buffalo. Gene 504, 245–252.Google Scholar
Singh, K, Hartley, DG, McFadden, TB, Mackenzie, DD 2004. Dietary fat regulates mammary stearoyl-coA desaturase expression and activity in lactating mice. Journal of Dairy Research 71, 1–6.CrossRefGoogle ScholarPubMed
Sørensen, BM, Chris Kazala, E, Murdoch, GK, Keating, AF, Cruz-Hernandez, C, Wegner, J, Kennelly, JJ, Okine, EK, Weselake, RJ 2008. Effect of CLA and other C18 unsaturated fatty acids on DGAT in bovine milk fat biosynthetic systems. Lipids 43, 903–912.Google Scholar
Takeuchi, Y, Yahagi, N, Izumida, Y, Nishi, M, Kubota, M, Teraoka, Y, Yamamoto, T, Matsuzaka, T, Nakagawa, Y, Sekiya, M, Iizuka, Y, Ohashi, K, Osuga, J, Gotoda, T, Ishibashi, S, Itaka, K, Kataoka, K, Nagai, R, Yamada, N, Kadowaki, T, Shimano, H 2010. Polyunsaturated fatty acids selectively suppress sterol regulatory element-binding protein-1 through proteolytic processing and autoloop regulatory circuit. Journal of Biological Chemistry 285, 11681–11691.Google Scholar
Teran-Garcia, M, Adamson, AW, Yu, G, Rufo, C, Suchankova, G, Dreesen, TD, Tekle, M, Clarke, SD, Gettys, TW 2007. Polyunsaturated fatty acid suppression of fatty acid synthase (FASN): evidence for dietary modulation of NF-Y binding to the FASN promoter by SREBP-1c. Biochemical Journal 402, 591–600.Google Scholar
Xu, J, Teran-Garcia, M, Park, JH, Nakamura, MT, Clarke, SD 2001. Polyunsaturated fatty acids suppress hepatic sterol regulatory element-binding protein-1 expression by accelerating transcript decay. Journal of Biological Chemistry 276, 9800–9807.Google Scholar
Yonezawa, T, Yonekura, S, Sanosaka, M, Hagino, A, Katoh, K, Obara, Y 2004. Octanoate stimulates cytosolic triacylglycerol accumulation and CD36 mRNA expression but inhibits acetyl coenzyme A carboxylase activity in primary cultured bovine mammary epithelial cells. Journal of Dairy Research 71, 398–404.Google Scholar
Supplementary material: File

Jacobs et al. supplementary material

Supplementary tables 1 and 2

Download Jacobs et al. supplementary material(File)
File 431.7 KB