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Dietary proteins with high isoflavone content or low methionine–glycine and lysine–arginine ratios are hypocholesterolaemic and lower the plasma homocysteine level in male Zucker fa/fa rats

Published online by Cambridge University Press:  08 March 2007

Oddrun A. Gudbrandsen*
Affiliation:
Institute of Medicine, Section of Medical Biochemistry, University of Bergen, Haukeland University Hospital, Bergen, Norway
Hege Wergedahl
Affiliation:
Institute of Medicine, Section of Medical Biochemistry, University of Bergen, Haukeland University Hospital, Bergen, Norway
Bjørn Liaset
Affiliation:
National Institute of Nutrition and Seafood Research, Bergen, Norway
Marit Espe
Affiliation:
National Institute of Nutrition and Seafood Research, Bergen, Norway
Rolf K. Berge
Affiliation:
Institute of Medicine, Section of Medical Biochemistry, University of Bergen, Haukeland University Hospital, Bergen, Norway
*
*Corresponding author: Dr Oddrun A. Gudbrandsen, fax +47 55973115, email [email protected]
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Abstract

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It has previously been demonstrated that soya protein, which contains isoflavones and low methionine–glycine and lysine–arginine ratios, has a hypocholesterolaemic effect. In the present study, the hypocholesterolaemic effects of an isoflavone-enriched casein diet (HDI) and a single-cell protein-based diet (SCP) devoid of isoflavones but with low methionine–glycine and lysine–arginine ratios were investigated in obese Zucker rats after 6 weeks of feeding. The control diet contained casein, which has high ratios of methionine–glycine and lysine–arginine. HDI and SCP feeding reduced the concentrations of total cholesterol and cholesteryl esters in plasma and liver, and changed the fatty acid composition of the hepatic cholesteryl esters. Faecal cholesterol and bile acid levels were markedly higher in SCP-fed rats than in controls, whereas HDI feeding had only minor effects. However, both HDI and SCP feeding increased the hepatic gene expression of cholesterol 7α hydroxylase. In contrast, the hepatic acyl-CoA synthetase and acyl-CoA:cholesterol acyltransferase activities and the gene expression of the LDL receptor were increased by HDI, but not by SCP feeding. The present results suggested that the cholesterol-lowering effect of SCP was related to the enterohepatic circulation, whereas HDI seemed to lower the plasma cholesterol via the circulation. Plasma homocysteine level was reduced in rats fed HDI and SCP compared to rats fed casein. In summary, diets enriched in isoflavones or containing proteins with low methionine–glycine and lysine–arginine ratios lowered the plasma cholesterol and homocysteine levels, changing the plasma profile from atherogenic to cardioprotective.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2005

References

Balmir, F, Staack, R, Jeffrey, E, Jimenez, MD, Wang, L & Potter, SM (1996) An extract of soy flour influences serum cholesterol and thyroid hormones in rats and hamsters. J Nutr 126, 30463053.CrossRefGoogle Scholar
Berge, RK, Flatmark, T & Osmundsen, H (1984) Enhancement of long-chain acyl-CoA hydrolase activity in peroxisomes and mitochondria of rat liver by peroxisomal proliferators. Eur J Biochem 141, 637644.CrossRefGoogle ScholarPubMed
Bersot, TP, Mahley, RW, Brown, MS & Goldstein, JL (1976) Interaction of swine lipoproteins with the low density lipoprotein receptor in human fibroblasts. J Biol Chem 251, 23952398.CrossRefGoogle ScholarPubMed
Blay, M, Peinado-Onsurbe, J, Julve, J, Rodriguez, V, Fernandez-Lopez, JA, Remesar, X & Alemany, M (2001) Anomalous lipoproteins in obese Zucker rats. Diabetes Obes Metab 3, 259270.CrossRefGoogle ScholarPubMed
Bligh, EG & Dyer, WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911917.CrossRefGoogle ScholarPubMed
Bray, GA (1977) The Zucker-fatty rat: a review. Fed Proc 36, 148153.Google ScholarPubMed
Brown, MS & Goldstein, JL (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232, 3447.CrossRefGoogle ScholarPubMed
Brown, MS, Goldstein, JL & Dietschy, JM (1979) Active and inactive forms of 3-hydroxy-3-methylglutaryl coenzyme A reductase in the liver of the rat. Comparison with the rate of cholesterol synthesis in different physiological states. J Biol Chem 254, 51445149.CrossRefGoogle Scholar
Carroll, KK & Hamilton, RMG (1975) Effects of dietary protein and carbohydrate on plasma cholesterol levels in relation to atherosclerosis. J Food Sci 40, 1823.CrossRefGoogle Scholar
Cohen, SA & Strydom, DJ (1988) Amino acid analysis utilizing phenylisothiocyanate derivatives. Anal Biochem 174, 116.CrossRefGoogle ScholarPubMed
Field, FJ, Albright, E & Mathur, S (1991) Inhibition of acylcoenzyme A: cholesterol acyltransferase activity by PD128O42: effect on cholesterol metabolism and secretion in CaCo-2 cells. Lipids 26, 18.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M, & Sloane Stanley, GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226, 497509.CrossRefGoogle ScholarPubMed
Fukui, K, Tachibana, N, Wanezaki, S, Tsuzaki, S, Takamatsu, K, Yamamoto, T, Hashimoto, Y & Shimoda, T (2002) Isoflavone-free soy protein prepared by column chromatography reduces plasma cholesterol in rats. J Agric Food Chem 50, 57175721.CrossRefGoogle ScholarPubMed
Goldstein, JL & Brown, MS (1974) Binding and degradation of low density lipoproteins by cultured human fibroblasts. Comparison of cells from a normal subject and from a patient with homozygous familial hypercholesterolemia. J Biol Chem 249, 51535162.CrossRefGoogle ScholarPubMed
Hermansen, K, Sondergaard, M, Hoie, L, Carstensen, M & Brock, B (2001) Beneficial effects of a soy-based dietary supplement on lipid levels and cardiovascular risk markers in type 2 diabetic subjects. Diabetes Care 24, 228233.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. J Clin Invest 101, 23312339.CrossRefGoogle ScholarPubMed
Huff, MW, Hamilton, RM & Carroll, KK (1977) Plasma cholesterol levels in rabbits fed low fat, cholesterol-free, semipurified diets: effects of dietary proteins, protein hydrolysates and amino acid mixtures. Atherosclerosis 28, 187195.CrossRefGoogle ScholarPubMed
Innerarity, TL & Mahley, RW (1978) Enhanced binding by cultured human fibroblasts of apo-E-containing lipoproteins as compared with low density lipoproteins. Biochemistry 17, 14401447.CrossRefGoogle ScholarPubMed
Kirk, EA, Sutherland, P, Wang, SA, Chait, A & LeBoeuf, RC (1998) Dietary isoflavones reduce plasma cholesterol and atherosclerosis in C57BL/6 mice but not LDL receptor-deficient mice. J Nutr 128, 954959.CrossRefGoogle Scholar
Kritchevsky, D, Tepper, SA, Czarnecki, SK & Klurfeld, DM (1982) Atherogenicity of animal and vegetable protein. Influence of the lysine to arginine ratio. Atherosclerosis 41, 429431.CrossRefGoogle ScholarPubMed
Lehmann, JM, Kliewer, SA, Moore, LB, Smith-Oliver, TA, Oliver, BB, Su, JL, Sundseth, SS, Winegar, DA, Blanchard, DE, Spencer, TA & Willson, TM (1997) Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J Biol Chem 272, 31373140.CrossRefGoogle ScholarPubMed
Liaset, B, Julshamn, K & Espe, M (2003) Chemical composition and theoretical nutritional evaluation of the produced fractions from enzymic hydrolysis of salmon frames with Protamex. Process Biochem 38, 17471759.CrossRefGoogle Scholar
Lin, RC (1985) Serum cholesterol, lecithin-cholesterol acyltransferase, and hepatic hydroxymethylglutaryl coenzyme A reductase activities of lean and obese Zucker rats. Metabolism 34, 1924.CrossRefGoogle ScholarPubMed
Madani, S, Lopez, S, Blond, JP, Prost, J & Belleville, J (1998) Highly purified soybean protein is not hypocholesterolemic in rats but stimulates cholesterol synthesis and excretion and reduces polyunsaturated fatty acid biosynthesis. J Nutr 128, 10841091.CrossRefGoogle Scholar
Mangold, HK (1969) In A Laboratory Handbook 2nd edition pp. 363421 (Sathl, E, editor). Berlin, Germany: Springer.Google Scholar
Morita, T, Oh-hashi, A, Takei, K, Ikai, M, Kasaoka, S & Kiriyama, S (1997) Cholesterol-lowering effects of soybean, potato and rice proteins depend on their low methionine contents in rats fed a cholesterol-free purified diet. J Nutr 127, 470477.CrossRefGoogle ScholarPubMed
Morrison, WR & Smith, LM (1964) Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J Lipid Res 5, 600608.CrossRefGoogle ScholarPubMed
Nagata, Y, Tanaka, K & Sugano, M (1981) Further studies on the hypocholesterolaemic effect of soya-bean protein in rats. Br J Nutr 45, 233241.CrossRefGoogle ScholarPubMed
Nagata, Y, Ishiwaki, N & Sugano, M (1982) Studies on the mechanism of antihypercholesterolemic action of soy protein and soy protein-type amino acid mixtures in relation to the casein counterparts in rats. J Nutr 112, 16141625.CrossRefGoogle Scholar
Nygard, O, Nordrehaug, JE, Refsum, H, Ueland, PM, Farstad, M & Vollset, SE (1997) Plasma homocysteine levels and mortality in patients with coronary artery disease. N Engl J Med 337, 230236.CrossRefGoogle ScholarPubMed
Peluso, MR, Winters, TA, Shanahan, MF & Banz, WJ (2000) A cooperative interaction between soy protein and its isoflavone-enriched fraction lowers hepatic lipids in male obese Zucker rats and reduces blood platelet sensitivity in male Sprague-Dawley rats. J Nutr 130, 23332342.CrossRefGoogle ScholarPubMed
Potter, SM (1995) Overview of proposed mechanisms for the hypocholesterolemic effect of soy. J Nutr 125, 606S611S.Google ScholarPubMed
Sirtori, CR, Even, R & Lovati, MR (1993) Soybean protein diet and plasma cholesterol: from therapy to molecular mechanisms. Ann N Y Acad Sci 676, 188201.CrossRefGoogle ScholarPubMed
Skrede, A, Berge, GM, Storebakken, T, Herstad, O, Aarstad, KG & Sundstøl, F (1998) Digestibility of bacterial protein grown on natural gas in mink, pigs, chicken and Atlantic salmon. Anim Feed Sci Technol 76, 103116.CrossRefGoogle Scholar
Suckling, KE, Benson, GM, Bond, B, Gee, A, Glen, A, Haynes, C & Jackson, B (1991) Cholesterol lowering and bile acid excretion in the hamster with cholestyramine treatment. Atherosclerosis 89, 183190.CrossRefGoogle ScholarPubMed
Svardal, AM, Mansoor, MA & Ueland, PM (1990) Determination of reduced, oxidized, and protein-bound glutathione in human plasma with precolumn derivatization with monobromobimane and liquid chromatography. Anal Biochem 184, 338346.CrossRefGoogle ScholarPubMed
Tanaka, K, Aso, B & Sugano, M (1984) Biliary steroid excretion in rats fed soybean protein and casein or their amino acid mixtures. J Nutr 114, 2632.CrossRefGoogle ScholarPubMed
Tang, PM, Finkelstein, JA & Chiang, JY (1988) Expression of hepatic microsomal cholesterol 7 alpha-hydroxylase activity in lean and obese Zucker rats. Biochem Biophys Res Commun 150, 853858.CrossRefGoogle ScholarPubMed
Tonstad, S, Smerud, K & Hoie, L (2002) A comparison of the effects of 2 doses of soy protein or casein on serum lipids, serum lipoproteins, and plasma total homocysteine in hypercholesterolemic subjects. Am J Clin Nutr 76, 7884.CrossRefGoogle ScholarPubMed
Wergedahl, H, Liaset, B, Gudbrandsen, OA, Lied, E, Espe, M, Muna, Z, Mork, S & Berge, RK (2004) Fish protein hydrolysate reduces plasma total cholesterol, increases the proportion of hdl cholesterol, and lowers acyl-CoA:cholesterol acyltransferase activity in liver of Zucker rats. J Nutr 134, 13201327.CrossRefGoogle ScholarPubMed