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Fat metabolism is regulated by altered gene expression of lipogenic enzymes and regulatory factors in liver and adipose tissue but not in semimembranosus muscle of pigs during the fattening period

Published online by Cambridge University Press:  10 July 2009

P. Duran-Montgé ,
P. K. Theil ,
C. Lauridsen  and
E. Esteve-Garcia
P. Duran-Montgé
Affiliation:
CENTA, IRTA Building A – Finca Camps i Armet E-17121 Monells (Girona), Spain
P. K. Theil
Affiliation:
Department of Animal Health, Welfare, and Nutrition, University of Aarhus, Faculty of Agricultural Sciences, Research Centre Foulum, Tjele, Denmark
C. Lauridsen
Affiliation:
Department of Animal Health, Welfare, and Nutrition, University of Aarhus, Faculty of Agricultural Sciences, Research Centre Foulum, Tjele, Denmark
E. Esteve-Garcia*
Affiliation:
IRTA. Mas de Bover, Ctra. de Reus-El Morell km. 3, 8 E-43120 Constantí (Tarragona), Spain
*
†E-mail: [email protected]
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Abstract

It has been shown previously that lipid metabolism is regulated by fatty acids (FA) and that thyroid hormones are important regulators of energy metabolism. The effects of weight, dietary fat level and dietary FA profile on thyroid hormone levels and expression of lipogenic genes and tissue FA composition were studied. Sixty-one crossbred gilts weighing 62 ± 5.2 kg BW average were either slaughtered at the beginning of the trial (n = 5) or fed one of seven diets (n = 8 pigs per diet): a semi-synthetic diet formulated to contain a very low level of fat (NF) and six diets based on barley–soybean meal supplemented with approximately 10% fat of different origin and slaughtered at 100 kg BW. The supplemental fats were tallow, high-oleic sunflower oil, sunflower oil (SFO), linseed oil, fat blend (55% tallow, 35% sunflower oil, 10% linseed oil) and fish oil blend (40% fish oil, 60% linseed oil). In general, the dietary FA profiles altered the FA composition of liver, semimembranosus muscle and adipose tissues. Pigs fed the NF diet had the highest free and total triiodothyronine (T3) values followed by pigs fed SFO. Total T3 levels were higher in pigs at 60 kg than in pigs at 100 kg. Correlations between thyroid hormones and genes encoding enzymes of fat synthesis in adipose tissue (acetyl CoA carboxylase (ACACA), fatty acid synthase and stearoyl CoA desaturase (SCD)) and the large differences in expression of lipogenic genes at different weights (60 and 100 kg BW), suggest a role for thyroid hormones and for T3, in particular, in regulating whole animal fat metabolism, with effects brought about by altered expression of lipogenic genes. Liver sterol receptor element binding protein-1 (SREBP1) mRNA content was affected by dietary treatment (P < 0.001) and was correlated with ACACA and SCD, whereas adipose tissue SREBP1 was not correlated with the mRNA abundance of any lipogenic enzyme. Weight and tissue factors showed greater influence on mRNA abundance of genes related with lipid metabolism than diet and tissue FA composition. In the pig, FA synthesis appear to be of greater magnitude in adipose tissue than in the liver as suggested by the higher expression of lipogenic genes in adipose tissue.

Keywords

pigfatty acid compositiongene expressionlipogenesisthyroid hormones
Type
Full Paper
Information
animal , Volume 3 , Issue 11 , November 2009 , pp. 1580 - 1590
Copyright
Copyright © The Animal Consortium 2009

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References

Bergen, WG, Mersmann, HJ 2005. Comparative aspects of lipid metabolism: impact on contemporary research and use of animal models. Journal of Nutrition 135, 2499–2502.CrossRefGoogle ScholarPubMed
Bloomfield, DK, Bloch, K 1960. Formation of delta-9-unsaturated fatty acids. Journal of Biological Chemistry 235, 337–345.CrossRefGoogle ScholarPubMed
Brenner, RR 1971. The desaturation step in the animal biosynthesis of polyunsaturated fatty acids. Lipids 6, 567–575.CrossRefGoogle ScholarPubMed
Clarke, SD, Hembree, J 1990. Inhibition of triiodothyronines induction of rat-liver lipogenic enzymes by dietary-fat. Journal of Nutrition 120, 625–630.CrossRefGoogle ScholarPubMed
Chopra, IJ, Huang, TS, Beredo, A, Solomon, DH, Chua Teco, GN, Mead, JF 1985. Evidence for an inhibitor of extrathyroidal conversion of thyroxine to 3,5,3′-triiodothyronine in sera of patients with nonthyroidal illnesses. Journal of Clinical Endocrinology and Metabolism 60, 666–672.CrossRefGoogle ScholarPubMed
Chwalibog, A, Thorbek, G 2000. Estimation of net nutrient oxidation and lipogenesis in growing pigs. Archives of Animal Nutrition 53, 253–271.Google ScholarPubMed
Dozin, B, Magnuson, MA, Nikodem, VM 1986. Thyroid hormone regulation of malic enzyme synthesis. Dual tissue- specific control. Journal of Biological Chemistry 261, 10290–10292.CrossRefGoogle ScholarPubMed
Duran-Montgé, P, Lizardo, R, Torrallardona, D, Esteve-Garcia, E 2007. Fat and fatty acid digestibility of different fat sources in growing pigs. Livestock Science 109, 66–69.CrossRefGoogle Scholar
Duran-Montgé, P, Theil, PK, Lauridsen, C, Esteve-Garcia, E 2009. Dietary fat source affects metabolism of fatty acids in pigs as evaluated by altered expression of lipogenic genes in liver and adipose tissues. Animal 3, 535–542.CrossRefGoogle ScholarPubMed
Fisher, RA 1925. Table VA in statistical methods for research workers. Oliver and Boyd, Edinburgh, UK.Google Scholar
Folch, J, Lees, M, Stanley, GHS 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–509.CrossRefGoogle ScholarPubMed
Horton, JD, Shimomura, I, Brown, MS, Hammer, RE, Goldstein, JL, Shimano, H 1998. Activation of cholesterol synthesis in preference to fatty acid synthesis in liver and adipose tissue of transgenic mice overproducing sterol regulatory element-binding protein-2. Journal of Clinical Investigation 101, 2331–2339.CrossRefGoogle ScholarPubMed
Inoue, A, Yamamoto, N, Morisawa, Y, Uchimoto, T, Yukioka, M, Morisawa, S 1989. Unesterified long-chain fatty-acids inhibit thyroid-hormone binding to the nuclear receptor – solubilized receptor and the receptor in cultured-cells. European Journal of Biochemistry 183, 565–572.CrossRefGoogle Scholar
Iritani, N, Komiya, M, Fukuda, H, Sugimoto, T 1998. Lipogenic enzyme gene expression is quickly suppressed in rats by a small amount of exogenous polyunsaturated fatty acids. Journal of Nutrition 128, 967–972.CrossRefGoogle ScholarPubMed
Jump, DB, Botolin, D, Wang, Y, Xu, JH, Christian, B, Demeure, O 2005. Fatty acid regulation of hepatic gene transcription. Journal of Nutrition 135, 2503–2506.CrossRefGoogle ScholarPubMed
Kouba, M, Enser, M, Whittington, FM, Nute, GR, Wood, JD 2003. Effect of high-linolenic acid diet on lipogenic enzyme activities, fatty acid composition, and meat quality in the growing pig. Journal of Animal Science 81, 1967–1979.CrossRefGoogle ScholarPubMed
Leat, WMF, Cuthbert, A, Howard, AN, Gresham, GA 1964. Studies on pigs reared on semi-synthetic diets containing no fat beef, tallow and maize oil – composition of carcass and fatty acid composition of various depot fats. Journal of Agricultural Science 63, 311–317.CrossRefGoogle Scholar
Littell, RC, Milliken, GA, Stroup, WW, Wolfinger, RD 1996. SAS system for mixed models. SAS Institute Inc., Cary, NC, USA.Google Scholar
Matsuzaka, T, Shimano, H, Yahagi, N, Amemiya-Kudo, M, Yoshikawa, T, Hasty, AH, Tamura, Y, Osuga, J, Okazaki, H, Iizuka, Y, Takahashi, A, Sone, H, Gotoda, T, Ishibashi, S, Yamada, N 2002. Dual regulation of mouse delta(5)- and delta(6)-desaturase gene expression by SREBP-1 and PPAR alpha. Journal of Lipid Research 43, 107–114.CrossRefGoogle Scholar
Mersmann, HJ 1984. Effect of sex on lipogenic activity in swine adipose tissue. Journal of Animal Science 58, 600–604.CrossRefGoogle ScholarPubMed
Mersmann, HJ, Pond, WG, Yen, JT 1984. Use of carbohydrate and fat as energy source by obese and lean swine. Journal of Animal Science 58, 894–901.CrossRefGoogle ScholarPubMed
Mersmann, HJ, Allen, CD, Chai, EY, Brown, LJ, Fogg, TJ 1981. Factors influencing the lipogenic rate in swine adipose tissue. Journal of Animal Science 52, 1298–1305.CrossRefGoogle ScholarPubMed
Miyazaki, M, Kim, YC, Ntambi, JM 2001. A lipogenic diet in mice with a disruption of the stearoyl-CoA desaturase 1 gene reveals a stringent requirement of endogenous monounsaturated fatty acids for triglyceride synthesis. Journal of Lipid Research 42, 1018–1024.CrossRefGoogle ScholarPubMed
Morrison, WR, Smith, LM 1964. Preparation of fatty acid methyl esters+dimethylacetals from lipids with boron fluoride-methanol. Journal of Lipid Research 5, 600–608.CrossRefGoogle ScholarPubMed
Mourot, J, Peiniau, P, Mounier, A 1994. Effect of dietary linoleic-acid on lipogenesis in adipose-tissue of pig. Reproduction Nutrition Development 34, 213–220.CrossRefGoogle ScholarPubMed
Mourot, J, Chauvel, J, Le Denmat, M, Mounier, A, Peiniau, P 1991. Linoleic acid level in the diet of pigs: effects on fat deposition and on meat linoleic acid oxidation during storage. Journées de la Recherche Porcine en France 23, 357–364.Google Scholar
National Research Council (NRC) 1998. Nutrient requirements of swine, 10th revised edition. National Academic Press, Washington, DC, USA.Google Scholar
Nuernberg, K, Fischer, K, Nuernberg, G, Kuechenmeister, U, Klosowska, D, Eliminowska-Wenda, G, Fiedler, I, Ender, K 2005. Effects of dietary olive and linseed oil on lipid composition, meat quality, sensory characteristics and muscle structure in pigs. Meat Science 70, 63–74.CrossRefGoogle ScholarPubMed
O’Hea, EK, Leveille, GA 1969. Significance of adipose tissue and liver as sites of fatty acid synthesis in pig and efficiency of utilization of various substrates for lipogenesis. Journal of Nutrition 99, 338–394.CrossRefGoogle ScholarPubMed
O’Hea, EK, Leveille, GA, Sugahara, M 1970. Lipogenesis and enzyme activity in pig adipose tissue as influenced by dietary protein and fat. International Journal of Biochemistry 1, 173–178.CrossRefGoogle Scholar
Pfaffl, MW 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, 2002–2007.CrossRefGoogle ScholarPubMed
Roncari, DA, Murthy, VK 1975. Effects of thyroid hormones on enzymes involved in fatty acid and glycerolipid synthesis. Journal of Biological Chemistry 250, 4134–4138.CrossRefGoogle ScholarPubMed
Scott, BL, Bazan, NG 1989. Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. Proceedings of the National Academy of Sciences of the United States of America 86, 2903–2907.CrossRefGoogle Scholar
Scott, RA, Cornelius, SG, Mersmann, HJ 1981. Effects of age on lipogenesis and lipolysis in lean and obese swine. Journal of Animal Science 52, 505–511.CrossRefGoogle ScholarPubMed
Shimano, H, Horton, JD, Hammer, RE, Shimomura, I, Brown, MS, Goldstein, JL 1996. Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. Journal of Clinical Investigation 98, 1575–1584.CrossRefGoogle ScholarPubMed
Shimano, H, Horton, JD, Shimomura, I, Hammer, RE, Brown, MS, Goldstein, JL 1997. Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells. Journal of Clinical Investigation 99, 846–854.CrossRefGoogle ScholarPubMed
Takeuchi, H, Matsuo, T, Tokuyama, K, Suzuki, M 1995. Serum triiodothyronine concentration and Na+, K+-ATPase activity in liver and skeletal muscle are influenced by dietary fat type in rats. Journal of Nutrition 125, 2364–2369.CrossRefGoogle ScholarPubMed
Theil, PK, Lauridsen, C 2007. Interactions between dietary fatty acids and hepatic gene expression of pigs during the weaning period. Livestock Science 108, 26–29.CrossRefGoogle Scholar
Worgall, TS, Sturley, SL, Seo, T, Osborne, TF, Deckelbaum, RJ 1998. Polyunsaturated fatty acids decrease expression of promoters with sterol regulatory elements by decreasing levels of mature sterol regulatory element-binding protein. Journal of Biological Chemistry 273, 25537–25540.CrossRefGoogle ScholarPubMed
Xiong, S, Chirala, S, Hsu, M, Wakil, S 1998. Identification of thyroid hormone response elements in the human fatty acid synthase promoter. Proceedings of the National Academy of Sciences of the United States of America 95, 12260–12265.CrossRefGoogle ScholarPubMed
Xu, J, Nakamura, MT, Cho, HP, Clarke, SD 1999. Sterol Regulatory Element Binding Protein-1 expression is suppressed by dietary polyunsaturated fatty acids – a mechanism for the coordinate suppression of lipogenic genes by polyunsaturated fats. Journal of Biological Chemistry 274, 23577–23583.CrossRefGoogle ScholarPubMed
Xu, J, Cho, H, O’Malley, S, Park, JHY, Clarke, SD 2002. Dietary polyunsaturated fats regulate rat liver sterol regulatory element binding proteins-1 and -2 in three distinct stages and by different mechanisms. Journal of Nutrition 132, 3333–3339.CrossRefGoogle ScholarPubMed
Zhang, YQ, Yin, LY, Hillgartner, FB 2003. SREBP-1 integrates the actions of thyroid hormone, insulin, cAMP, and medium-chain fatty acids on ACC alpha transcription in hepatocytes. Journal of Lipid Research 44, 356–368.CrossRefGoogle Scholar