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Dietary n-3 fatty acids affect mRNA level of brown adipose tissue uncoupling protein 1, and white adipose tissue leptin and glucose transporter 4 in the rat

Published online by Cambridge University Press:  09 March 2007

Yoko Takahashi
Affiliation:
Laboratory of Nutrition Biochemistry, National Food Research Institute, Ministry of Agriculture, Forestry and Fisheries, 2-1-2 Kannondai, Tsukuba Science City, Ibaraki 305-8642, Japan
Takashi Ide*
Affiliation:
Laboratory of Nutrition Biochemistry, National Food Research Institute, Ministry of Agriculture, Forestry and Fisheries, 2-1-2 Kannondai, Tsukuba Science City, Ibaraki 305-8642, Japan
*
*Corresponding author: Dr Takashi Ide, fax +81 298 38 7996, email idetaka@[email protected]
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Abstract

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We examined the effect of dietary fats rich in n-3 polyunsaturated fatty acids (PUFA) on mRNA levels in white and brown adipose tissues in rats. Four groups of rats were fed on a low-fat diet (20 g safflower oil/kg) or a high-fat diet (200 g/kg) containing safflower oil, which is rich in n-6 PUFA (linoleic acid), or perilla (α-linolenic acid) or fish oil (eicosapentaenoic and docosahexaenoic acids), both of which are rich in n-3 PUFA, for 21 d. Energy intake was higher in rats fed on a high-safflower-oil diet than in those fed on low-fat or high-fish-oil diet, but no other significant differences were detected among the groups. Perirenal white adipose tissue weight was higher and epididymal white adipose tissue weight tended to be higher in rats fed on a high-safflower-oil diet than in those fed on a low-fat diet. However, high-fat diets rich in n-3 PUFA, compared to a low-fat diet, did not increase the white adipose tissue mass. High-fat diets relative to a low-fat diet increased brown adipose tissue uncoupling protein 1 mRNA level. The increases were greater with fats rich in n-3 PUFA than with n-6 PUFA. A high-safflower-oil diet, compared to a low-fat diet, doubled the leptin mRNA level in white adipose tissue. However, high-fat diets rich in n-3 PUFA failed to increase it. Compared to a low-fat diet, high-fat diets down-regulated the glucose transporter 4 mRNA level in white adipose tissue. However, the decreases were attenuated with high-fat diets rich in n-3 PUFA. It is suggested that the alterations in gene expression in adipose tissue contribute to the physiological activities of n-3 PUFA in preventing body fat accumulation and in regulating glucose metabolism in rats.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

American Institute of Nutrition (1977) Report of the American Institute of Nutritionad hoc. Committee on Standards for Nutritional Studies. Journal of Nutrition 107, 13401348.CrossRefGoogle Scholar
Belzung, F, Raclot, T and Groscolas, R (1993) Fish oil. n-3 fatty acids selectively limit the hypertrophy of abdominal fat depots in growing rats fed high-fat diets. American Journal of Physiology 264, R1111R1118.Google ScholarPubMed
Benhizia, F, Hainault, I, Serougne, C, Lagrange, D, Hajduch, E, Guichard, C, Malewiak, MI, Quignard-Boulange, A, Lavau, M and Griglio, S (1994) Effects of a fish oil–lard diet on rat plasma lipoproteins, liver FAS, and lipolytic enzymes. American Journal of Physiology 267, E975E982.Google ScholarPubMed
Bouillaud, F, Ricquier, D, Thibault, J and Weissenbach, J (1985) Molecular approach to thermogenesis in brown adipose tissue: cDNA cloning of the mitochondrial uncoupling protein. Proceedings of the National Academy of Sciences of the USA 82, 445448.CrossRefGoogle ScholarPubMed
Bouillaud, F, Weissenbach, J and Ricquier, D (1986) Complete cDNA-derived amino acid sequence of rat brown fat uncoupling protein. Journal of Biological Chemistry 261, 14871490.CrossRefGoogle ScholarPubMed
Brault, D, Noe, L, Etienne, J, Hamelin, J, Raisonnier, A, Souli, A, Chuat, JC, Dugail, I, Quignard-Boulange, A, Lavau, M and Galibert, F (1992) Sequence of rat lipoprotein lipase-encoding cDNA. Gene 121, 237246.CrossRefGoogle ScholarPubMed
Campfield, LA, Smith, FJ and Burn, P (1996) The OB protein (leptin) pathway — a link between adipose mass and central neural networks. Hormone and Metabolic Research 28, 619632.CrossRefGoogle ScholarPubMed
Chomczynski, P and Sacchi, N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Analytical Biochemistry 162, 156159.CrossRefGoogle ScholarPubMed
Collins, S and Surwit, RS (1996) Pharmacologic manipulation of. ob expression in a dietary model of obesity. Journal of Biological Chemistry 271, 94379440.CrossRefGoogle Scholar
Ezaki, O, Tsuji, E, Momomura, K, Kasuga, M and Itakura, H (1992) Effect of fish and safflower oil feeding on subcellular glucose transporter distributions in rat adipocytes. American Journal of Physiology 263, E94E101.Google ScholarPubMed
Falcou, R, Bouillaud, F, Mory, G, Apfelbaum, M and Ricquier, D (1985) Increase of uncoupling protein and its mRNA in brown adipose tissue of rats fed on 'cafeteria diet'. Biochemical Journal 231, 241244.CrossRefGoogle ScholarPubMed
Fleury, C, Neverova, M, Collins, S, Raimbault, S, Champigny, O, Levi-Meyrueis, C, Bouillaud, F, Seldin, MF, Surwit, RS, Ricquier, D and Warden, CH (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nature Genetics 15, 269272.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M and Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497509.CrossRefGoogle ScholarPubMed
Giraudo, SQ, Kotz, CM, Grace, MK, Levine, AS and Billington, CJ (1994) Rat hypothalamic NPY mRNA and brown fat uncoupling protein mRNA after high-carbohydrate or high-fat diets. American Journal of Physiology 266, R1578R1583.Google ScholarPubMed
Gong, DW, He, Y, Karas, M and Reitman, M (1997) Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, β3-adrenergic agonists, and leptin. Journal of Biological Chemistry 272, 2412924132.CrossRefGoogle ScholarPubMed
Himms-Hagen, J (1990) Brown adipose tissue thermogenesis: interdisciplinary studies. FASEB Journal 4, 28902898.CrossRefGoogle ScholarPubMed
Huang, YJ, Fang, VS, Juan, CC, Chou, YC, Kwok, CF and Ho, LT (1997) Amelioration of insulin resistance and hypertension in a fructose-fed rat model with fish oil supplementation. Metabolism 46, 12521258.CrossRefGoogle Scholar
Hwang, CS, Loftus, TM, Mandrup, S and Lane, MD (1997) Adipocyte differentiation and leptin expression. Annual Review of Cell and Developmental Biology 13, 231259.CrossRefGoogle ScholarPubMed
Ide, T, Kano, S, Murata, M, Yanagita, T and Sugano, M (1994) Dietary modifications of the biliary bile acid glycine: taurine ratio and activity of hepatic bile acid-CoA: amino acid. N-acyltransferase (EC 2·3·1) in the rat. British Journal of Nutrition 72, 93100.CrossRefGoogle ScholarPubMed
Ide, T, Okamatsu, H and Sugano, M (1978) Regulation by dietary fats of 3-hydroxy-3-methylglutaryl-coenzyme A reductase in rat liver. Journal of Nutrition 108, 601612.CrossRefGoogle ScholarPubMed
Jacobsson, A, Stadler, U, Glotzer, MA and Kozak, LP (1985) Mitochondrial uncoupling protein from mouse brown fat. Molecular cloning, genetic mapping, and mRNA expression. Journal of Biological Chemistry 260, 1625016254.CrossRefGoogle ScholarPubMed
James, DE, Strube, M and Mueckler, M (1989) Molecular cloning and characterization of an insulin-regulatable glucose transporter. Nature 338, 8387.CrossRefGoogle ScholarPubMed
Kahn, BB (1994) Dietary regulation of glucose transporter gene expression: tissue specific effects in adipose cells and muscle. Journal of Nutrition 124, 1289S1295S.CrossRefGoogle ScholarPubMed
Kawada, T, Kayahashi, S, Hida, Y, Koga, K, Nadachi, Y and Fushiki, T (1998) Fish (Bonito) oil supplementation enhances the expression of uncoupling protein in brown adipose tissue of rat. Journal of Agricultural and Food Chemistry 46, 12251227.CrossRefGoogle Scholar
Kirchgessner, TG, Svenson, KL, Lusis, AJ and Schotz, MC (1987) The sequence of cDNA encoding lipoprotein lipase. A member of a lipase gene family. Journal of Biological Chemistry 262, 84638466.CrossRefGoogle ScholarPubMed
Luo, J, Rizkalla, SW, Boillot, J, Alamowitch, C, Chaib, H, Bruzzo, F, Desplanque, N, Dalix, AM, Durand, G and Slama, G (1996) Dietary (n-3) polyunsaturated fatty acids improve adipocyte insulin action and glucose metabolism in insulin-resistant rats: relation to membrane fatty acids. Journal of Nutrition 126, 19511958.Google ScholarPubMed
Martin, I, Giralt, M, Viñas, O, Iglesias, R, Mampel, T and Villarroya, F (1995) Co-ordinate decrease in the expression of the mitochondrial genome and nuclear genes for mitochondrial proteins in the lactation-induced mitochondrial hypotrophy of rat brown fat. Biochemical Journal 308, 749752.CrossRefGoogle ScholarPubMed
Matsuda, J, Hosoda, K, Itoh, H, Son, C, Doi, K, Tanaka, T, Fukunaga, Y, Inoue, G, Nishimura, H, Yoshimasa, Y, Yamori, Y and Nakao, K (1997) Cloning of rat uncoupling protein-3 and uncoupling protein-2 cDNAs: their gene expression in rats fed high-fat diet. FEBS Letters 418, 200204.CrossRefGoogle ScholarPubMed
Masuzaki, H, Ogawa, Y, Hosoda, K, Kawada, T, Fushiki, T and Nakao, K (1995) Augmented expression of the. obese gene in the adipose tissue from rats fed high-fat diet. Biochemical and Biophysical Research Communications 216, 355358.CrossRefGoogle ScholarPubMed
Mercer, SW and Trayhurn, P (1987) Effect of high fat diets on energy balance and thermogenesis in brown adipose tissue of lean and genetically obese. ob/ob mice. Journal of Nutrition 117, 21472153.CrossRefGoogle ScholarPubMed
Miura, T, Ohnishi, Y, Takagi, S, Sawamura, M, Yasuda, N, Ishida, H, Tanigawa, K, Yamori, Y and Seino, Y (1997) A comparative study of high-fat diet containing fish oil or lard on blood glucose in genetically diabetic (db/db) mice. Journal of Nutritional Science and Vitaminology 43, 225231.CrossRefGoogle ScholarPubMed
Nelson, GJ, Kelly, DS, Schmidt, PC and Serrato, CM (1987) The influence of dietary fat on the lipogenic activity and fatty acid composition of rat white adipose tissue. Lipids 22, 338344.CrossRefGoogle ScholarPubMed
Nicholls, DG and Locke, RM (1984) Thermogenic mechanisms in brown fat. Physiological Reviews 64, 164.CrossRefGoogle ScholarPubMed
Ogawa, Y, Masuzaki, H, Isse, N, Okazaki, T, Mori, K, Shigemoto, M, Satoh, N, Tamura, N, Hosoda, K, Yoshimasa, Y, Jingami, H, Kawada, T and Nakao, K (1995) Molecular cloning of rat. obese cDNA and augmented gene expression in genetically obese Zucker fatty (fa/fa) rats. Journal of Clinical Investigation 96, 16471652.CrossRefGoogle ScholarPubMed
Okuno, M, Kajiwara, K, Imai, S, Kobayashi, T, Honma, N, Maki, T, Suruga, K, Goda, T, Takase, S, Muto, Y and Moriwaki, H (1997) Perilla oil prevents the excessive growth of visceral adipose tissue in rats by down-regulating adipocyte differentiation. Journal of Nutrition 127, 17521757.CrossRefGoogle ScholarPubMed
Oudart, H, Groscolas, R, Calgari, C, Nibbelink, M, Leray, C, Maho, YL and Malan, A (1997) Brown fat thermogenesis in rats fed high-fat diets enriched with. n-3 polyunsaturated fatty acids. International Journal of Obesity 21, 955962.CrossRefGoogle ScholarPubMed
Pedersen, O, Kahn, CR, Flier, JS and Kahn, BB (1991) High fat feeding causes insulin resistance and a marked decrease in the expression of glucose transporters (Glut 4) in fat cells of rats. Endocrinology 129, 771777.CrossRefGoogle Scholar
Qureshi, A and Kopelman, PG (1997) Leptin - fat messenger or fat controller?. Clinical Endocrinology 47, 169171.CrossRefGoogle ScholarPubMed
Raclot, T, Groscolas, R, Langin, D and Ferré, P (1997) Site-specific regulation of gene expression by n-3 polyunsaturated fatty acids in rat white adipose tissues. Journal of Lipid Research 38, 19631972.CrossRefGoogle ScholarPubMed
Ramsay, TG (1996) Fat cells. Endocrinology and Metabolism Clinics of North America 25, 847870.CrossRefGoogle ScholarPubMed
Ricquier, D, Bouillaud, F, Toumelin, P, Mory, G, Bazin, R, Arch, J and Pénicaud, L (1986) Expression of uncoupling protein mRNA in thermogenic or weakly thermogenic brown adipose tissue. Evidence for a rapid β-adrenoreceptor mediated and transcriptionally regulated step during activation of thermogenesis. Journal of Biological Chemistry 261, 1390513910.CrossRefGoogle ScholarPubMed
Ricquier, D, Mory, G, Bouillaud, F, Thibault, J and Weissenbach, J (1984) Rapid increase of mitochondrial uncoupling protein and its mRNA in stimulated brown adipose tissue. FEBS Letters 178, 240244.CrossRefGoogle ScholarPubMed
Rousseau, V, Becker, DJ, Ongemba, LN, Rahier, J, Henquin, JC and Brichard, SM (1997) Developmental and nutritional changes of ob and PPAR gamma 2 gene expression in rat white adipose tissue. Biochemical Journal 321, 451456.CrossRefGoogle Scholar
Semenkovich, CF, Chen, SH, Wims, M, Luo, CC, Li, WH and Chan, L (1989) Lipoprotein lipase and hepatic lipase mRNA tissue specific expression, developmental regulation, and evolution. Journal of Lipid Research 30, 423431.CrossRefGoogle ScholarPubMed
Sevilla, L, Gumà, A, Enrique-Tarancòn, G, Mora, S, Muñz, P, Palacín, M, Testar, X and Zorzano, A (1997) Chronic high-fat feeding and middle-aging reduce in an additive fashion Glut4 expression in skeletal muscle and adipose tissue. Biochemical and Biophysical Research Communications 235, 8993.CrossRefGoogle Scholar
Snedecor, GW & Cochran, WG (1989) Statistical Methods, 8th ed. Ames, IA: Iowa State University Press.Google Scholar
Takahashi, M, Funahashi, T, Shimomura, I, Miyazaki, K and Matsuzawa, Y (1996) Plasma leptin levels and body fat distribution. Hormone and Metabolic Research 28, 751762.CrossRefGoogle ScholarPubMed
Zhang, Y, Proenca, R, Maffei, M, Barone, M, Leopold, L and Friedman, JM (1994) Positional cloning of the mouse. obese gene and its human homologue. Nature 372, 425432.CrossRefGoogle ScholarPubMed