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Dietary fish protein alters blood lipid concentrations and hepatic genes involved in cholesterol homeostasis in the rat model

Published online by Cambridge University Press:  08 March 2007

Anjali Shukla ,
Anja Bettzieche ,
Frank Hirche ,
Corinna Brandsch ,
Gabriele I. Stangl  and
Klaus Eder
Anjali Shukla
Affiliation:
Institute of Nutritional Sciences, Martin-Luther-University of Halle-Wittenberg, Emil-Abderhalden-Strasse 26, D-06108 Halle/Saale, Germany
Anja Bettzieche
Affiliation:
Institute of Nutritional Sciences, Martin-Luther-University of Halle-Wittenberg, Emil-Abderhalden-Strasse 26, D-06108 Halle/Saale, Germany
Frank Hirche
Affiliation:
Institute of Nutritional Sciences, Martin-Luther-University of Halle-Wittenberg, Emil-Abderhalden-Strasse 26, D-06108 Halle/Saale, Germany
Corinna Brandsch
Affiliation:
Institute of Nutritional Sciences, Martin-Luther-University of Halle-Wittenberg, Emil-Abderhalden-Strasse 26, D-06108 Halle/Saale, Germany
Gabriele I. Stangl
Affiliation:
Institute of Nutritional Sciences, Martin-Luther-University of Halle-Wittenberg, Emil-Abderhalden-Strasse 26, D-06108 Halle/Saale, Germany
Klaus Eder*
Affiliation:
Institute of Nutritional Sciences, Martin-Luther-University of Halle-Wittenberg, Emil-Abderhalden-Strasse 26, D-06108 Halle/Saale, Germany
*
*Corresponding author: Dr K. Eder, fax +49 345 5527124, email klaus.eder@landw.uni-halle.de
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Abstract

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It is known that various dietary plant proteins are capable of influencing the lipid metabolism of human subjects and animals when compared with casein. Less, however, is known about the effects of fish protein on the cholesterol and triacylglycerol metabolism. Therefore, two experiments were conducted in which rats were fed diets containing 200 g of either fish protein, prepared from Alaska pollack fillets, or casein, which served as control, per kilogram, over 20 and 22 d, respectively. As parameters of lipid metabolism, the concentrations of cholesterol and triacylglycerols in the plasma and liver, the faecal excretion of bile acids and the hepatic expression of genes encoding proteins involved in lipid homeostasis were determined. In both experiments, rats fed fish protein had higher concentrations of cholesteryl esters in the liver, a lower concentration of cholesterol in the HDL fraction (ρ>1·063 kg/l) and lower plasma triacylglycerol concentrations than rats fed casein (P<0.05). The gene expression analysis performed in experiment 2 showed that rats fed fish protein had higher relative mRNA concentrations of sterol regulatory element-binding protein (SREBP)-2, 3-hydroxy-3-methylglutaryl coenzyme A reductase, LDL receptor, apo AI, scavenger receptor B1 and lecithin-cholesterol-acyltransferase in their liver than did rats fed casein (P<0·05). The faecal excretion of bile acids and the mRNA concentrations of cholesterol 7α-hydroxylase, SREBP-1c and corresponding target genes were not altered. These findings show that fish protein had multiple effects on plasma and liver lipids that were at least in part caused by an altered expression of the hepatic genes involved in lipid homeostasis.

Keywords

Fish proteinPlasma lipidsHepatic genesRat
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 4 , October 2006 , pp. 674 - 682
Copyright
Copyright © The Nutrition Society 2006

References

Acton, S, Rigotti, A, Landschulz, KT, Xu, S, Hobbs, HH & Krieger, M (1996) Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271, 518–520.CrossRefGoogle ScholarPubMed
Ait, Yahia, D, Madani, S, Prost, J, Bouchenak, M, Belleville J (2005) Fish protein improves blood pressure but alters HDL2 and HDL3 composition and tissue lipoprotein lipase activities in spontaneously hypertensive rats. Eur J Nutr 44, 10–17.CrossRefGoogle Scholar
Ait, Yahia, D, Madani, S, Prost, E, Prost, J, Bouchenak, M, Belleville J (2003) Tissue antioxidant status differs in spontaneously hypertensive rats fed fish protein or casein. J Nutr 133, 479–482.Google Scholar
Anderson, JW, Johnstone, BM, Cook-Newell, ME (1995) Meta-analysis of the effects of soy protein intake on serum lipids. N Engl J Med 333, 276–282.CrossRefGoogle ScholarPubMed
Bakhit, RM, Klein, BP, Essex-Sorlie, D, Ham, JO, Erdman, JW, Jr, Potter SM (1994) Intake of 25 g soybean protein reduces plasma cholesterol in men with elevated cholesterol concentrations. J Nutr 124, 213–222.CrossRefGoogle Scholar
Bassler, R & Buchholz, H (1993) Methodenbuch Band III. Die chemische Untersuchung von Futtermitteln. [Analytical Methods III. The Chemical Analysis of Feed] Darmstadt VDLUFA-PressGoogle Scholar
Bergeron, N, Dishies, Y & Jacques, H (1992) Dietary fish protein modulates high density lipoprotein cholesterol and lipoprotein lipase activity in rabbits. J Nutr 122, 1731–1737.CrossRefGoogle ScholarPubMed
Chang, TY, Chang, CC & Cheng, D (1997) Acyl-coenzyme A:cholesterol acyltransferase. Ann Rev Biochem 86, 613–638.CrossRefGoogle Scholar
Chang, TY, Chang, CC, Lu, X & Lin, S (2001) Catalysis of ACAT may be completed within the plane of the membrane: a working hypothesis. J Lipid Res 42, 1933–1938.CrossRefGoogle ScholarPubMed
De Hoff, JL, Davidson, JH & Kritchevsky, D (1978) An enzymatic assay for determining free and total cholesterol in tissues. Clin Chem 24, 433–435.CrossRefGoogle Scholar
Dongowski, G, Huth, M, Gebhardt, E & Flamme, W (2002) Dietary fiber-rich barley products beneficially affect the intestinal tract of rats. J Nutr 132, 3704–3714.CrossRefGoogle ScholarPubMed
Eder, K, Peganova, S & Kluge, H (2001) Studies on the tryptophan requirement of piglets. Arch Anim Nutr 55, 281–297.Google ScholarPubMed
Field, FJ, Albright, E & Mathur, SN (1987) Regulation of cholesterol esterification by micellar cholesterol in CaCo-2 cells. J Lipid Res 28, 1057–1066.CrossRefGoogle ScholarPubMed
Fontaine, J, Bech-Andersen, S, Bütikofer, U, De Froidmont-Görtz, I (1998) Determination of tryptophan in feed by HPLC – development of an optimal hydrolysis and extraction procedure by the EU Commission DG XII in three international collaborative studies. Agribiol Res 51, 97–108.CrossRefGoogle Scholar
Gascon, A, Jacques, H, Moorjani, S, Deshaies, Y, Brun, LD & Julien, P (1996) Plasma lipoprotein profile and lipolytic activities in response to the substitution of lean white fish for other animal protein sources in premenopausal women. Am J Clin Nutr 63, 315–321.CrossRefGoogle Scholar
Genest, J, Jr, Marcil, M, Denis, M, Yu L (1999) High density lipoprotein in health and disease. J Invest Med 47, 31–42.Google Scholar
Giudetti, AM, Beynen, AC, Lemmens, AG, Gnoni, GV & Geelen, MJH (2003) Hepatic fatty acid metabolism in rats fed diets with different contents of C 18: 0, C 18: 1 cis and C 18: 1 trans isomers. Br J Nutr 90, 887–893.CrossRefGoogle Scholar
Hara, A & Radin, NS (1978) Lipid extraction of tissues with a low toxicity solvent. Anal Biochem 90, 420–426.CrossRefGoogle ScholarPubMed
Hojnacki, JL, Nicolosi, RJ & Hayes, KC (1976) Densitometric quantitation of neutral lipids on ammonium sulfate impregnated thin-layer chromatograms. J Chromatogr 128, 133–139.CrossRefGoogle ScholarPubMed
Horton, JD, Bashmakov, Y, Shimomura, I & Shimano, H (1998) Regulation of sterol regulatory element binding proteins in livers of fasted and refed mice. Proc Natl Acad Sci USA 95, 5987–5992.CrossRefGoogle ScholarPubMed
Horton, JD, Goldstein, JL & Brown, MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109, 1125–1131.CrossRefGoogle ScholarPubMed
Kritchevsky, D, Tepper, SA, Czarnecki, SK & Klurfeld, DM (1982) Atherogenicity of animal and vegetable protein. Influence of the lysine to arginine ratio. Atherosclerosis 41, 429–431.CrossRefGoogle ScholarPubMed
Lange, Y, Ye, J & Steck, TL (2004) How cholesterol homeostasis is regulated by plasma membrane cholesterol in excess of phospholipids. Proc Natl Acad Sci USA 101, 11664–11667.CrossRefGoogle ScholarPubMed
Marlett, JA & Fischer, MH (2002) A poorly fermented gel from psyllium seed husk increases excreta moisture and bile acid excretion in rats. J Nutr 132, 2638–2643.CrossRefGoogle ScholarPubMed
Meddings, J, Spady, D & Dietschy, J (1986) Kinetic constants for receptor-dependent and receptor-independent low density lipoprotein transport in the tissues of the rat and hamster. J Clin Invest 77, 1474–1481.Google Scholar
Morita, T, Oh-Hashi, A, Takei, K, Ikai, M, Ksaoka, S & Kiriyama, S (1997) Cholesterol-lowering effects of soybean, potato and rice proteins depend on their low methionine contents in rat fed a cholesterol-free purified diet. J Nutr 127, 470–477.CrossRefGoogle ScholarPubMed
Murata, M, Sano, Y, Bannai, S, Ishihara, K, Matsushima, R & Uchida, M (2004) Fish protein stimulated the fibrinolysis in rats. Ann Nutr Metab 48, 348–356.CrossRefGoogle ScholarPubMed
Naumann, C & Basler, R (1993) Methodenbuch Band III. Die chemische Untersuchung von Futtermitteln. [Analytical Methods III. The Chemical Analysis of Feed] Darmstadt VDLUFA-PressGoogle Scholar
Osborne, TF (2000) Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J Biol Chem 275, 32379–32382.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH, Fahey, GC Jr (1993) AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 1939–1951.CrossRefGoogle Scholar
Schuster, R (1988) Determination of amino acids in biological, pharmaceutical, plant and food samples by automated precolumn derivatization and high-performance liquid chromatography. J Chromatogr 431, 271–284.CrossRefGoogle ScholarPubMed
Shimano, H, Yahagik, N, Amemiya-Kudo, M (1999) Sterol regulatory element-binding protein-1 as a key transcription factor for nutritional induction of lipogenic enzyme genes. J Biol Chem 274, 35832–35839.CrossRefGoogle ScholarPubMed
Sirtori, CR, Lovati, MR, Manzoni, C, Castiglioni, S, Duranti, M, Magni, C, Moranti, S, D'Agostina, A & Arnoldi, A (2004) Proteins of white lupin seed, a naturally isoflavone-poor legume, reduced cholesterolemia in rats and increase LDL receptor activity in HepG2 cells. J Nutr 134, 18–23.CrossRefGoogle Scholar
Sirtori, CR, Lovati, MR, Manzoni, C, Gianazza, E, Bondioli, A, Staels, B & Auwerx, J (1998) Reduction of serum cholesterol by soybean proteins: clinical experience and potential molecular mechanisms. Nutr Metab Cardiovasc Dis 8, 334–340.Google Scholar
Sparks, JD, Phung, TL, Bolognino, M, Cianci, J, Khurana, R, Peterson, RG, Sowden, MP, Corsetti, JP & Sparks, CE (1998) Lipoprotein alterations in 10- and 20-week-old Zucker diabetic fatty rats: hyperinsulinemic versus insulinopenic hyperglycemia. Metabolism 47, 1315–1324.CrossRefGoogle ScholarPubMed
Sugiyama, K, Ohkawa, S & Muramatsu, K (1986) Relationship between amino acid composition of diet and plasma cholesterol level in growing rats fed a high cholesterol diet. J Nutr Sci Vitaminol 32, 413–423.CrossRefGoogle ScholarPubMed
Tachibana, N, Matsumoto, I, Fukui, K, Arai, S, Kato, H, Abe, K & Takamatsu, K (2005) Intake of soy protein isolate alters hepatic gene expression in rats. J Agric Food Chem 53, 4253–4257.CrossRefGoogle ScholarPubMed
Vallett, SM, Sanchez, HB, Rosenfeld, JM & Osborne, TF (1996) A direct role of sterol regulatory element binding protein in activation of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene. J Biol Chem 271, 12247–12253.CrossRefGoogle ScholarPubMed
Vester, B & Rasmussen, K (1991) High performance liquid chromatography method for rapid and accurate determination of homocysteine in plasma and serum. Eur J Clin Biochem 29, 549–554.Google ScholarPubMed
Vlahecevic, ZR, Pandak, WM & Stravitz, RT (1999) Regulation of bile acid biosynthesis. Gastroenterol Clin N Am 28, 1–25.CrossRefGoogle Scholar
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, 1320–1327.CrossRefGoogle ScholarPubMed
Woo, CWH, Siow, YL, Pierce, GN, Choy, PC, Minuk, GY, Mymin, D & Karmin, O (2005) Hyperhomocysteinemia induces hepatic cholesterol biosynthesis and lipid accumulation via activation of transcription factors. Am J Physiol Endocrinol Metab 288, E1002–E1010.CrossRefGoogle ScholarPubMed
Zhang, X & Beynen, AC (1993) Influence of dietary fish proteins on plasma and liver cholesterol concentrations in rats. Br J Nutr 69, 767–777.CrossRefGoogle ScholarPubMed