Abstract
The present study investigated the effects of dietary fish and sunflower oils as sources of n-3, n-6 polyunsaturated fatty acids (PUFA) on the expression of key lipogenic and cholesterologenic genes in subcutaneous adipose tissue (SAT) and tail adipose tissue (TAT) of fat-tailed sheep. Twenty-six male Afshari lambs were divided into 4 groups. Three groups were fed a high concentrate basal diet plus 100 g/lamb/day oil supplement (OS; 60 g sunflower oil and 40 g fish oil) beyond a 21-day adaptation period for 10, 20, and 30 days (groups OS10, OS20, and OS30; n = 6, each) until slaughter. A control group was slaughtered at the last day of adaptation (OS0; n = 4). Expression of PPARγ, SREBP-1c, and SREBP-2 were determined in TAT and SAT. All transcription factors had lower expression in SAT than TAT. Feeding OS induced a similar pattern of SREBP-1c expression in both TAT and SAT with highest values in OS20. SREBP-2 mRNA decreased by > 50% in TAT of OS30 compared to OS0, whereas the expression of SREBP-2 mRNA did not change in SAT in the same period. PPARγ expression was not affected over time either in SAT or TAT. Plasma concentrations of cholesterol and blood urea nitrogen increased in OS20. The comparison of gene expression responses to OS in TAT vs. SAT suggest that PUFA-mediated effects on lipid metabolism differ between SAT and TAT, which may be linked to the specific role of TAT in energy and water balance under arid conditions.
This is a preview of subscription content, log in via an institution to check access.
Data availability
On request.
References
Ahmadian M, Suh JM, Hah N et al. (2013) PPARγ signaling and metabolism: the good, the bad and the future. Nat Med 19, 557-566. https://doi.org/10.1038/nm.3159
Al-Hasani H, Joost HG (2005) Nutrition-/diet-induced changes in gene expression in white adipose tissue. Best pract Res Clin Endocrinol Metab 19, 589-603. https://doi.org/10.1016/j.beem.2005.07.005
Angulo J, Mahecha L, Nuernberg K et al. (2012) Effects of polyunsaturated fatty acids from plant oils and algae on milk fat yield and composition are associated with mammary lipogenic and SREBF1 gene expression. Animal 6, 1961-1972. https://doi.org/10.1017/s1751731112000845
Bahnamiri HZ, Zali A, Ganjkhanlou M et al. (2018) Regulation of lipid metabolism in adipose depots of fat-tailed and thin-tailed lambs during negative and positive energy balances. Gene 641, 203-211. https://doi.org/10.1016/j.gene.2017.10.065
Boden G, Salehi S, Cheung P et al. (2013) Comparison of in vivo effects of insulin on SREBP-1c activation and INSIG-1/2 in rat liver and human and rat adipose tissue. Obesity 21, 1208-1214. https://doi.org/10.1002/oby.20134
Chedid M, Jaber LS, Giger-Reverdin S et al. (2014) Review: Water stress in sheep raised under arid conditions. Can J Anim Sci 94, 243-257. https://doi.org/10.4141/cjas2013-188
Desvergne B, Michalik L, Wahli W (2006) Transcriptional regulation of metabolism. Physiol Rev 86, 465-514. https://doi.org/10.1152/physrev.00025.2005
DiGirolamo M, Fine JB, Tagra K et al. (1998) Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am. J. Physiol. Regul. Integr. Comp. Physiol 274, 1460-1467. https://doi.org/10.1152/ajpregu.1998.274.5.R1460
Epstein H (1985) The Awassi sheep with special reference to the improved dairy type. FAO Anim Health 57, 34-38.
Heibel SK. Transcriptional regulation of N-acetylglutamate synthase and its clinical relevance. University of Maryland, College Park, MD, PhD thesis.
Klopotek A, Hirche F, Eder K (2006) PPAR gamma ligand troglitazone lowers cholesterol synthesis in HepG2 and Caco-2 cells via a reduced concentration of nuclear SREBP-2. Exp Biol Med 231, 1365-1372. https://doi.org/10.1177/153537020623100810
Krey G, Braissant O, L’Horset F et al. (1997) Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay. Mol Endocrinol 11, 779-791. https://doi.org/10.1210/mend.11.6.0007
Lafontan M & Berlan M (2003) Do regional differences in adipocyte biology provide new pathophysiological insights? Trends Pharmacol. Sci 24, 276-283. https://doi.org/10.1016/S0165-6147(03)00132-9
Livak KJ & Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt. Methods 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Mashek DG, Bertics SJ, Grummer RR (2002) Metabolic fate of long-chain unsaturated fatty acids and their effects on palmitic acid metabolism and gluconeogenesis in bovine hepatocytes. J Dairy Sci 85, 2283-2289. https://doi.org/10.3168/jds.s0022-0302(02)74308-7
Meale SJ, Chaves AV, He ML et al. (2015) Effects of various dietary lipid additives on lamb performance, carcass characteristics, adipose tissue fatty acid composition, and wool characteristics. J Anim Sci 93, 3110-3120. https://doi.org/10.2527/jas.2014-8437
Mirzaei-Alamouti H, Mohammadi Z, Shahir MH et al. (2018) Effects of short-term feeding of different sources of fatty acids in premating diets on reproductive performance and blood metabolites of fat-tailed Iranian Afshari ewes. Theriogenology 113, 85-91. https://doi.org/10.1016/j.theriogenology.2018.02.007
Picard F & Auwerx J (2002) PPAR (gamma) and glucose homeostasis. Annu Rev Nutr 22, 167-197. https://doi.org/10.1146/annurev.nutr.22.010402.102808
Ronis MJ, Baumgardner JN, Marecki JC et al. (2012) Dietary fat source alters hepatic gene expression profile and determines the type of liver pathology in rats overfed via total enteral nutrition. Physiol Genomics 44, 1073-1089. https://doi.org/10.1152/physiolgenomics.00069.2012
Rosen ED & Spiegelman BM (2001) PPAR-gamma: a nuclear regulator of metabolism, differentiation and cell growth. J Biol Chem 276, 37731-37734. https://doi.org/10.1074/jbc.r100034200
Shimomura I, Shimano H, Horton JD et al. (1997) Differential expression of exons 1a and 1c in mRNAs for sterol regulatory element binding protein-1 in human and mouse organs and cultured cells. J Clin Inves 99, 838-845. https://doi.org/10.1172/jci119247
Tontonoz P, Hu E, Spiegelman BM (1994) Stimulation of adipogenesis in fibroblasts by PPARy2, a lipid-activated transcription factor. Cell Press 79, 1147-1156. https://doi.org/10.1016/0092-8674(94)90006-x
Way JM, Harrington WW, Brown KK et al. (2001) Comprehensive messenger ribonucleic acid profiling reveals that peroxisome proliferator-activated receptor gamma activation has coordinate effects on gene expression in multiple insulin-sensitive tissues. Endocrinol 142, 1269-1277. https://doi.org/10.1210/endo.142.3.8037
Worgall TS, Sturley SL, Seo T et al. (1998) Polyunsaturated fatty acids decrease expression of promoters with sterol regulatory elements by decreasing levels of mature sterol regulatory element-binding protein. J Biol Chem 273, 25537-25540. https://doi.org/10.1074/jbc.273.40.25537
Xu J, Cho H, O’Malley S et al. (2002) Dietary polyunsaturated fats regulate rat liver sterol regulatory element binding proteins-1 and -2 in three distinct stages and by different mechanisms. J Nutr 132, 3333-3339. https://doi.org/10.1093/jn/132.11.3333
Yahagi N, Shimano H, Hasty AH et al. (1999) A crucial role of sterol regulatory element-binding protein-1 in the regulation of lipogenic gene expression by polyunsaturated fatty acids. J Biol Chem 274, 35840-35844. https://doi.org/10.1074/jbc.274.50.35840
Zhou YP, Wu R, Shen W et al. (2018) Comparison of effects of oleic acid and palmitic acid on lipid deposition and mTOR/S6K1/SREBP-1c pathway in HepG2 cells. Zhonghua gan zang bing za zhi= Zhonghua ganzangbing zazhi= Chinese journal of hepatology 26(6), 451-456. https://doi.org/10.3760/cma.j.issn.1007-3418.2018.
Zsédely E, Király A, Szabó CS et al. (2012) Effect of dietary linseed oil soap on lamb meat. Int J Agric Biol 6, 67-70.
Acknowledgements
We cordially thank the employees of the Sheep Research Farm of the University of Zanjan for diligent help with animal care.
Funding
The study was funded by the Department of Animal Science, University of Zanjan, and the Ministry of Science, Iran.
Author information
Authors and Affiliations
Contributions
Conceptualization, fund acquisition, and supevision: H. Mirzaei-Alamouti; data curation: S. Elhami; methodology: M. Vazirigohar, T. Harakinejad, and M. Mansouryar; writing the original draft: M. Mansouryar and A. Abdollahi; writing and editing: H. Mirzaei-Alamouti, M. O. Nielson, J. R. Aschenbach, and M. Mansouryar.
Corresponding authors
Ethics declarations
Ethics approval
This study was undertaken with approval from the University of Zanjan Animal Care Committee (1253).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mirzaei-Alamouti, H., Elhami, S., Abdollahi, A. et al. Short communication: effect of dietary supplementation with a mixture of fish and sunflower oils on the expression of key lipogenic and cholesterologenic genes in adipose tissues with different metabolic functions. Trop Anim Health Prod 53, 522 (2021). https://doi.org/10.1007/s11250-021-02972-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-021-02972-0