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Metabolic effects of coconut, safflower, or menhaden oil feeding in lean and obese Zucker rats

Published online by Cambridge University Press:  09 March 2007

Pamarthi F. Mohan
Affiliation:
Hormel Institute, University of Minnesota, Austin, Minnesota 55912, USA
Frederick C. Phillips
Affiliation:
Hormel Institute, University of Minnesota, Austin, Minnesota 55912, USA
Margot P. Cleary
Affiliation:
Hormel Institute, University of Minnesota, Austin, Minnesota 55912, USA
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Abstract

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The aim of the present investigation was to study the effects of fish oil feeding in obese Zucker rats to establish its suitability as an animal model of hyperlipidaemia, and to understand the possible mechanism of fish oil-induced perturbations in cell metabolism. Lean and obese Zucker rats were fed on diets containing 180 g coconut, safflower, or menhaden oil/kg for 10 weeks. Body-weights and food intakes of lean coconut (LC), safflower (LS), and menhaden (LM) groups were similar. Obese menhaden (OM) rats had lower food intakes and body-weights compared with obese coconut (OC) and obese safflower (OS) groups, but values for all obese rats were higher than those for lean rats. Liver weights were higher in obese compared with lean rats, but on a percentage body-weight basis menhaden oil rats had higher values within genotype. Serum cholesterol and triacylglycerol levels were lower in the OM group compared with the OC and OS groups, and in the LM group compared with the LC group. Glucose and insulin levels were highest in OS rats followed by OC and OM rats and then the lean rats. Serum triiodothyronine and thyroxine were lower in OM rats compared with OC and OS rats. Liver mitochondrial state 3 rates with glutamate-malate and succinate were lower; mitochondrial β-oxidation was unaffected and peroxisomal β-oxidation was higher in menhaden oil rats compared with both coconut and safflower oil rats. In general, consumption of menhaden oil lowered hepatic malic enzyme (EC 1.1.1.38, 1.1.1.40), glucose-6-phosphate dehydrogenase (EC 1.1.1.49) and glutathione peroxidase (EC 1.11.1.9) activities and elevated long-chain fatty acyl-CoA hydrolase (EC 3.1.2.2) activity when compared with the two other diets. It is concluded that obese Zucker rats do respond like human subjects to fish oil feeding but not to vegetable oils. The hypolipidaemic effect of fish oil appears to be mediated through a lowering of lipogenic enzymes, glucose-6-phosphate dehydrogenase and malic enzyme.

Type
Lipid Metabolism
Copyright
Copyright © The Nutrition Society 1991

References

REFERENCES

Berge, R. K. & Farstad, M. (1981). Long-chain fatty acyl-CoA hydrolase from rat liver mitochondria. Methods in Enzymology 71, 234242.Google Scholar
Berge, R. K., Nilsson, A. & Husoy, A. M. (1988). Rapid stimulation of liver palmitoyl-CoA synthetase, carnitine palmitoyl transferase and glycerophosphate acyltransferase compared to peroxisomal β-oxidation and palmitoyl-CoA hydrolase in rats fed high-fat diets. Biochimica et Biophysica Acta 960, 417426.Google Scholar
Borkman, M., Chisholm, D. J., Furler, S. M., Storlien, L. H., Kraegen, E. W., Simons, L. A. & Chesterman, C. N. (1989). Effect of fish oil supplementation on glucose and lipid metabolism in NIDDM. Diabetes 38, 13141319.CrossRefGoogle ScholarPubMed
Clarke, S. D. & Armstrong, M. K. (1988). Suppression of rat liver fatty acid synthetase m-RNA level by dietary fish oil. Federation of the American Society, for Experimental Biology Journal 2, 852A.Google Scholar
Clarke, S. D., Benjamin, L., Bell, L. & Phinney, S. D. (1988). Fetal growth and fetal lung phospholipid content in rats fed safflower oil, menhaden oil or hydrogenated coconut oil. American Journal of Clinical Nutrition 47, 828835.CrossRefGoogle ScholarPubMed
Cleary, M. P. (1986). Consequences of restricted feeding/refeeding cycles in lean and obese female Zucker rats. Journal of Nutrition 116, 290303.CrossRefGoogle ScholarPubMed
Cleary, M. P., Vasselli, J. R. & Greenwood, M. R. C. (1980). Development of obesity in Zucker obese (fa/fa) rat in absence of hyperphagia. American Journal of Physiology 238, E284E292.Google Scholar
Clubb, F. J., Schmitz, J. M., Butler, M. M., Buja, L. M., Willerson, J. T. & Campbell, W. B. (1989). Effect of dietary omega-3 fatty acid on serum lipids, platelet function, and atherosclerosis in Watanabe heritable hyperlipidaemic rabbits. Arteriosclerosis 9, 529537.CrossRefGoogle Scholar
Dolphin, P. J., Amy, R. M., Koeslag, D. G., Limoges, B. F. & Russell, J. C. (1988). Reduction of hyperlipidaemia in the LA/N-corpulent rat by dietary fish oil containing n−3 fatty acids. Biochimica et Biophysica Acta 962, 317329.Google Scholar
Flatmark, T., Astrid, N., Jon, K., Thors, E. S., Miriam, H. F., Harald, K. & Erling, E. N. (1988). On the mechanism of induction of the enzyme systems for peroxisomal β-oxidation of fatty acids in rat liver by diets rich in partially hydrogenated fish oil. Biochimica et Biophysica Acta 962, 122130.CrossRefGoogle Scholar
Glauber, H., Wallace, P., Griver, K. & Brechtel, G. (1988). Adverse metabolic effect of omega-3 fatty acids in non-insulin dependent diabetes mellitus. Annals of Internal Medicine 108, 663668.Google Scholar
Glock, G. & McLean, P. (1953). Further studies on the properties and assay of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase of rat liver. Biochemical Journal 55, 400408.CrossRefGoogle ScholarPubMed
Goodridge, A. G. & Adelman, T. G. (1976). Regulation of malic enzyme synthesis by insulin, triiodothyronine and glucagon in liver cells in culture. Journal of Biological Chemistry 251, 30273032.CrossRefGoogle ScholarPubMed
Gower, J. D. (1988). A role for dietary lipids and antioxidants in the activation of carcinogens. Free Radical Biology and Medicine 5, 95111.CrossRefGoogle ScholarPubMed
Harris, W. S. (1989). Fish oils and plasma lipid and lipoprotein metabolism in humans: a critical review. Journal of Lipid Research 30, 785807.CrossRefGoogle ScholarPubMed
Harris, W. S., Connor, W. E. & McMurry, M. P. (1983). The comparative reductions of the plasma lipids and lipoproteins by dietary polyunsaturated fats: salmon oil versus vegetable oil. Metabolism 32, 179184.CrossRefGoogle Scholar
Herold, P. M. & Kinsella, J. E. (1986). Fish oil consumption and decreased risk of cardiovascular disease: a comparison of findings from animal and human feeding trials. American Journal of Clinical Nutrition 43, 566598.Google Scholar
Herzberg, G. R. & Rogerson, M. (1988). Hepatic fatty acid synthesis and triglyceride secretion in rats fed fructose- or glucose-based diets containing corn oil, tallow or marine oil. Journal of Nutrition 118, 10611067.CrossRefGoogle ScholarPubMed
Hoch, F. L. (1988). Lipids and thyroid hormones. Progress in Lipid Research 27, 199270.CrossRefGoogle ScholarPubMed
Iritani, N., Inoguchi, K., Endo, M., Fukuda, E. & Morita, M. (1980). Identification of shell fish fatty acids and their effects on lipogenic enzymes. Biochimica et Biophysica Acta 618, 378382.Google Scholar
Jen, K-L. C., Alexander, M., Zhong, S., Rose, K., Lin, P. K. H. & Kasim, S. E. (1989). Lipid lowering effect of omega-3 fatty acids in genetically obese Zucker rats. Nutrition Research 9, 12171228.Google Scholar
Johnson, B. J. & Berdanier, C. D. (1987). Effect of menhaden oil on the responses of rats to starvation-refeeding. Nutrition Reports International 36, 809817.Google Scholar
Kaduce, T. L., Awad, A. B., Fontenelle, L. J. & Spector, A. A. (1977). Effect of fatty acid saturation on α- aminoisobutyric acid transport in Ehrlich ascites cells. Journal of Biological Chemistry 252, 66246630.Google Scholar
Kinsella, J. E. (1987). Seafoods and Fish Oils in Human Health and Diseases. New York, NY: Marcel Dekker Inc.Google Scholar
Lazarow, P. B. (1981). Assay of peroxisomal β-oxidation of fatty acids. Methods in Enzymology 72, 315319.Google Scholar
Leaf, A. & Weber, P. C. (1988). Cardiovascular effects of n-3 fatty acids. New England Journal of Medicine 318, 549557.CrossRefGoogle ScholarPubMed
Lin, R. L. (1985). Serum cholesterol, lecithin-cholesterol acyltransferase, and hepatic hydroxy methylglutaryl Coenzyme A reductase activities of lean and obese Zucker rats. Metabolism 34, 1924.CrossRefGoogle ScholarPubMed
Martin, R. J. & Gahagan, J. (1977). Serum hormone levels and tissue metabolism in pair-fed lean and obese Zucker rats. Hormone and Metabolic Research 9, 181186.CrossRefGoogle ScholarPubMed
McCaleb, M. L. & Donner, D. B. (1981). Affinity of hepatic insulin receptor is influenced by membrane phospholipids. Journal of Biological Chemistry 256, 1105111057.Google Scholar
Mohan, P. F. & Cleary, M. P. (1988). Effect of short-term DHEA administration on liver metabolism of lean and obese rats. American Journal of Physiology 255, E1E8.Google Scholar
Nepokroeff, C. M., Lakshmahan, M. R., Ness, G. C., Moseing, R. A., Kleinsek, D. A. & Porter, J. W. (1976). Coordinate control of rat liver lipogenic enzymes by insulin. Archives of Biochemistry and Biophysics 162, 340344.CrossRefGoogle Scholar
Ochoa, S. (1955). Malic enzyme. Methods in Enzymology 1, 739741.Google Scholar
Osmundsen, H. (1981). Spectrophotometric procedure for measuring mitochondrial β-oxidation. Methods in Enzymology 72, 306314.Google Scholar
Osmundsen, H. & Jornstad, K. B. (1985). Inhibitory effects of sonic long-chain unsaturated fatty acids on mitochondrial β-oxidation. Biochemical Journal 230, 329337.CrossRefGoogle Scholar
Phillipson, B. E., Rothrock, D. W., Connor, W. E., Harris, W. S. & Illingworth, D. R. (1985). Reduction of plasma lipids, lipoproteins and apoproteins by dietary fish oil in patients with hypertriglyceridemia. New England Journal of Medicine 312, 12101216.CrossRefGoogle ScholarPubMed
Pilch, P. F., Thompson, P. A. & Czech, M. P. (1980). Coordinate modulation of d-glucose transport activity and bilayer fluidity in plasma membrane derived from control and insulin-treated adipocytes. Proceedings of the National Academy of Sciences U.S.A. 77, 915918.Google Scholar
Popp-Snijders, S. C., Schouten, J. A., Heine, R. J., van der Meer, J. & van der Veen, E. A. (1987). Dietary supplementation of omega-3 polyunsaturated fatty acids improves insulin sensitivity in non-insulin-dependent diabetes. Diabetes Research 4, 141147.Google Scholar
Rich, S., Miller, J. F. Jr, Charous, S., Davis, H. R., Shanks, P., Glasov, S. & Lands, W. E. (1989). Development of atherosclerosis in genetically hyperlipidaemic rabbits during chronic fish oil ingestion. Arterioselerosis 9, 189194.Google Scholar
Roman, I., Maj, P. G., Nowicka, C. & Angielski, S. (1979). Regulation of Ca2+ efflux from kidney and liver mitochondria by unsaturated fatty acids and Na+ ion. European Journal of Biochemistry 102, 615623.Google Scholar
Sanderman, H. Jr (1978). Regulation of membrane enzymes by lipids. Biochimica et Biophysica Acta 515, 209237.Google Scholar
Strum-Odin, R., Adkins-Finke, B., Blake, W. L., Phinney, S. D. & Clarke, S. D. (1987). Modification of fatty acid composition of membrane phospholipid in hepatocyte monolayer with n–3, n–6 and n–9 fatty acids and its relationship to triacylglycerol production. Biochimica et Biophysica Acta 921, 378391.Google Scholar
Tanaka, T., Hosaka, K. & Numa, S. (1981). Long chain acyl-CoA synthetase from rat liver. Methods in Enzymology 71, 334341.Google Scholar
Tappel, A. L. (1978). Glutathione peroxidase and hydroperoxides. Methods in Enzymology 52, 506513.Google Scholar
Vanrollins, M., Frade, P. D. & Carretero, O. A. (1988). Oxidation of 5,8,11,14,17-eicosapentaenoic acid by hepatic and renal microsomes. Biochimica et Biophysica Acta 966, 133149.CrossRefGoogle Scholar
Winberry, L., Nakayama, R., Wolfe, R. & Holten, D. (1980). Regulation of glucose-6-phosphate dehydrogenase activity in primary rat hepatocyte cultures. Biochemical and Biophysical Research Communications 96, 748755.Google Scholar
Winer, B. J. (1971). Factorial experiments in which some of the interactions are confounded. Statistical Principles in Experimental Design, chapt 8, pp. 606676. New York: McGraw-Hill.Google Scholar
Wong, S. H., Nestel, P. J., Trimble, R. P., Storer, G. B., Illman, R. J. & Topping, D. L. (1984). The adaptive effects of dietary fish and safflower oil on lipid and lipoprotein metabolism in perfused rat liver. Biochimica et Biophysica Acta 792, 103109.Google Scholar
Yamaoka, S., Urade, R. & Kito, M. (1988). Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. Journal of Nutrition 118, 290296.Google Scholar
Yamazaki, R. K., Shen, T. & Schade, G. B. (1987). A diet rich in (n–3) fatty acids increases peroxisomal β-oxidation activity and lowers plasma triacylglycerols without inhibiting glutathione-dependent detoxication activities in the rat liver. Biochimica et Biophysica Acta 920, 6267.Google Scholar
Zucker, L. M. (1965). Hereditary obesity in the rat associated with hyperlipidaemia. Annals of the New York Academy of Sciences 131, 447458.CrossRefGoogle Scholar
Zucker, T. F. & Zucker, L. M. (1962). Hereditary obesity in the rats associated with high serum fat and cholesterol. Proceedings of the Society for Experimental Biology and Medicine 110, 165171.CrossRefGoogle Scholar