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Dietary cholesterol reduces lipoprotein lipase activity in the atherosclerosis-susceptible Bio F1B hamster

Published online by Cambridge University Press:  09 March 2007

Martina A. McAteer ,
David C. Grimsditch ,
Martin Vidgeon-Hart ,
G. Martin Benson  and
Andrew M. Salter
Martina A. McAteer
Affiliation:
Division of Nutritional Biochemistry, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, UK
David C. Grimsditch
Affiliation:
Atherosclerosis Department, GlaxoSmithKline Pharmaceuticals, Harlow, Essex CM19 5AW, UK
Martin Vidgeon-Hart
Affiliation:
Safety Assessment Department, GlaxoSmithKline Pharmaceuticals, Welwyn, Hertfordshire AL6 9AR, UK
G. Martin Benson
Affiliation:
Atherosclerosis Department, GlaxoSmithKline Pharmaceuticals, Harlow, Essex CM19 5AW, UK
Andrew M. Salter*
Affiliation:
Division of Nutritional Biochemistry, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD, UK
*
*Corresponding author: Dr Andrew M. Salter, fax +44 115 951 6122, email [email protected]
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Abstract

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We have compared lipoprotein metabolism in, and susceptibility to atherosclerosis of, two strains of male Golden Syrian hamster, the Bio F1B hybrid and the dominant spot normal inbred (DSNI) strain. When fed a normal low-fat diet containing approximately 40 g fat and 0·3 g cholestero/g, triacylglycerol-rich lipoprotein (chylomicron+VLDL) and HDL-cholesterol were significantly higher (P<0·001) in Bio F1B hamsters than DSNI hamsters. When this diet was supplemented with 150 g coconut oil and either 0·5 or 5·0 g cholestero/g, significant differences were seen in response. In particular, the high-cholesterol diet produced significantly greater increases in plasma cholesterol and triacylglycerol in the Bio F1B compared with the DSNI animals (P=0·002 and P<0·001 for cholesterol and triacylglycerol, respectively). This was particularly dramatic in non-fasting animals, suggesting an accumulation of chylomicrons. In a second experiment, animals were fed 150 g coconut oi/g and 5·0 g cholestero/g for 6 and 12 months. Again, the Bio F1B animals showed dramatic increases in plasma cholesterol and triacylglycerol, and this was confirmed as primarily due to a rise in chylomicron concentration. Post-heparin lipoprotein lipase activity was significantly reduced (P<0·001) in the Bio F1B compared with the DSNI animals at 6 months, and virtually absent at 12 months. Bio F1B animals were also shown to develop significantly more (P<0·001) atherosclerosis. These results indicate that, in the Bio F1B hybrid hamster, cholesterol feeding reduces lipoprotein lipase activity, thereby causing the accumulation of chylomicrons that may be associated with their increased susceptibility to atherosclerosis.

Keywords

Lipoprotein lipaseHepatic lipaseDominant spot normal inbred strainBio F1BDietary cholesterolAtherosclerosisHamster
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue 3 , March 2003 , pp. 341 - 350
Copyright
Copyright © The Nutrition Society 2003

References

Benlian, P, De Gennes, JL, Foubert, L, Zhang, H, Gagne, SE & Hay den, M (1996) Premature atherosclerosis in patients with familial chylomicronemia caused by mutations in the lipoprotein lipase gene. New England Journal of Medicine 335, 848–854.CrossRefGoogle ScholarPubMed
Bennett, AJ, Billett, MA, Salter, AM, Mangiapane, EH, Bruce, JS, Anderton, KL, Marenah, CB, Lawson, N & White, DA (1995) Modulation of hepatic apolipoprotein B, 3-hydroxy-3-methyl-glutaryl-CoA reductase and low density lipoprotein receptor mRNA and plasma lipoprotein concentrations by defined dietary fats. Biochemical Journal 311, 167–173.CrossRefGoogle Scholar
Billett, MA, Bruce, JS, White, DA, Bennett, AJ & Salter, AM (2000) Interactive effects of dietary cholesterol and different saturated fatty acids on lipoprotein metabolism in the hamster. British Journal of Nutrition 84, 439–447.CrossRefGoogle ScholarPubMed
Corey, JE & Zilversmit, DB (1977) Validation of a stable emulsion for the assay of lipoprotein lipase activity. Journal of Laboratory Clinical Medicine 89, 666–674.Google ScholarPubMed
Foxall, TL, Shwaery, GT, Stucchi, AF, Nicolosi, RJ & Wong, SS (1992) Dose-related effects of doxazosin on plasma lipids and aortic fatty streak formation in the hypercholesterolemic hamster model. American Journal of Pathology 140, 1357–1363.Google ScholarPubMed
Ginzinger, DG, Lewis, MES, Ma, Y, Jones, BR, Liu, G, Jones, SD & Hay den, MR (1996) A mutation in the lipoprotein lipase gene is the molecular basis of chylomicronemia in a colony of domestic cats. Journal of Clinical Investigation 97, 1257–1266.CrossRefGoogle Scholar
Groot, PHE, Pearce, NJ, Suckling, KE & Eisenberg, S (1992) Effects of cholestyramine on lipoproteins levels and metabolism in Syrian hamsters. Biochimica et Biophysica Acta 1123, 76–84.CrossRefGoogle ScholarPubMed
Groot, PH, van Vlijmen, BJ, Benson, GM, Hofker, MH, Schiffelers, R, Vidgeon-Hart, M & Havekes, LM (1996) Quantitative assessment of aortic atherosclerosis in APOE*3 Leiden transgenic mice and its relationship to serum cholesterol exposure. Arteriosclerosis, Thrombosis and Vascular Biology 16, 926–933.CrossRefGoogle ScholarPubMed
Kahlon, TS, Faye, I, Chow, MS, Delilah, W, Irving, BS & Sayre, RN (1996) Cholesterol response and foam cell formation in hamsters fed two levels of saturated fat and various levels of cholesterol. Nutrition Research 16, 1353–1368.CrossRefGoogle Scholar
Kim, JB & Spiegelman, BM (1996) ADD/REBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes and Development 10, 1096–1107.CrossRefGoogle Scholar
Kowala, MC, Mazzucco, CE, Hartl, KS, Seiler, SM, Warr, GA, Abid, S & Grove, RI (1993) Prostacyclin agonists reduce early atherosclerosis in hyperlipidemic hamsters. Arteriosclerosis and Thrombosis 13, 435–444.CrossRefGoogle ScholarPubMed
Kowala, MC, Nunnari, JJ, Durham, SK & Nicolosi, RJ (1991) Doxazosin and cholestyramine similarly decrease fatty streak formation in the aortic arch of hyperlipidemic hamsters. Atherosclerosis 91, 35–49.CrossRefGoogle ScholarPubMed
Mangiapane, EH, McAteer, MA, Benson, GM, White, DA & Salter, AM (1999) Modulation of the regression of atherosclerosis in the hamster by dietary lipids: comparison of coconut oil and olive oil. British Journal of Nutrition 82, 401–409.CrossRefGoogle ScholarPubMed
Nicolosi, RJ, Rogers, EJ, Kritchevsky, D, Scomeca, JA & Huth, PJ (1997) Dietary conjugated linoleic acid reduces plasma lipoproteins and early atherosclerosis in hypercholesterolemic hamsters. Artery 22, 266–277.Google ScholarPubMed
Nicolosi, RJ, Wilson, TA & Krausse, BR (1998 a) The ACAT inhibitor, CI-1011 is effective in the prevention and regression of aortic fatty streak area in hamsters. Atherosclerosis 137, 77–85.CrossRefGoogle ScholarPubMed
Nicolosi, RJ, Wilson, TA, Lawton, C, Rogers, EJ, Wiseman, SA, Tijburg, LBM & Kritchevsky, D (1998 b) The greater atherogenicity of nonpurified diets versus semipurified diets in hamsters is mediated via differences in plasma cholesterol distribution, LDL oxidative susceptibility and plasma α-tocopherol concentration. Journal of Nutritional Biochemistry 9, 591–597.CrossRefGoogle Scholar
Nicolosi, RJ, Wilson, TA, Rogers, EJ & Kritchevsky, D (1998 c) Effects of specific fatty acids (8:0, 14:0, cis-18:1, trans-18:1) on plasma lipoproteins, early atherogenic potential, and LDL oxidative properties in the hamster. Journal of Lipid Research 39, 1972–1980.CrossRefGoogle Scholar
Nistor, A, Bulla, A, Filip, DA & Radu, A (1987) The hyperlipidemic hamster as a model of experimental atherosclerosis. Atherosclerosis 68, 159–173.CrossRefGoogle Scholar
Otto, J, Ordovas, JM, Smith, D, van Dongen, D, Nicolosi, RJ & Schaefer, EJ (1995) Lovastatin inhibits diet induced atherosclerosis in F1B Golden Syrian hamsters. Atherosclerosis 114, 19–28.CrossRefGoogle ScholarPubMed
Paigen, B, Morrow, A, Holmes, PA, Mitchell, D & Williams, RA (1987) Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis 68, 231–240.CrossRefGoogle ScholarPubMed
Parker, RA, Sabrah, T, Cap, M & Gill, BT (1995) Relation of vascular oxidative stress, α-tocopherol, and hypercholesterolemia to early atherosclerosis in hamsters. Arteriosclerosis, Thrombosis and Vascular Biology 15, 349–358.CrossRefGoogle ScholarPubMed
Pitman, WA, Osgood, DP, Smith, D, Schaefer, EJ & Ordovas, JM (1998) The effect of diet and lovastatin on regression of fatty streak lesions and on hepatic and intestinal mRNA levels for LDL receptor and HMG CoA reductase in F1B hamsters. Atherosclerosis 138, 43–52.CrossRefGoogle ScholarPubMed
Salter, AM, Mangiapane, EH, Bennett, AJ, Bruce, JS, Billett, MA, Anderton, KL, Marenah, CB, Lawson, N & White, DA (1998) The effect of different dietary fatty acids on lipoprotein metabolism: concentration-dependent effects of diets enriched in oleic, myristic, palmitic and stearic acids. British Journal of Nutrition 79, 195–202.CrossRefGoogle ScholarPubMed
Savonen, R, Nordstoga, K, Christophersen, B, Lindberg, A, Shen, Y, Hultin, M, Olivecrona, T & Olivecrona, G (1999) Chylomicron metabolism in an animal model for hyperlipoproteinemia type I.. Journal of Lipid Research 40, 1336–1346.CrossRefGoogle Scholar
Schaffner, CP, Brill, DR, Singhal, AK, Bonner, DP, Goldstein, NI & Wang, GM (1981) Absence of cholesterolgenesis regulation in the liver and prostrate of the BIO 87.20 hamster. Lipids 16, 835–840.CrossRefGoogle Scholar
Schoonjans, K, Gelman, L, Haby, C, Briggs, M & Auwerx, J (2000) Induction of LPL gene expression by sterols is mediated by a sterol regulatory element and is independent of the presence of multiple E boxes. Journal of Molecular Biology 304, 323–334.CrossRefGoogle ScholarPubMed
Semenkovich, CE, Coleman, T & Daugherty, A (1998) Effects of heterozygous lipoprotein lipase deficiency on diet-induced atherosclerosis in mice. Journal of Lipid Research 39, 1141–1151.CrossRefGoogle ScholarPubMed
Sessions, VA & Salter, AM (1994) The effects of different dietary fats and cholesterol on serum lipoprotein concentrations in hamsters. Biochimica et Biophysica Acta 1211, 207–214.CrossRefGoogle ScholarPubMed
Shimano, HJ, Horton, JD, Hammer, RE, Shimomura, I, Brown, MS & Goldstein, JL (1996) Over-production of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. Journal of Clinical Investigation 98, 1575–1584.CrossRefGoogle Scholar
Shimano, HJ, 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, 1161–1169.CrossRefGoogle ScholarPubMed
Singhal, AK, Ayengar, NKN, May, PS & McSherry, CK (1983) Cholesterol metabolism in two strains of hamster. In Dietary Fats and Health, pp. 267 –277 [Perkins, EG and Visek, WJ, editors]. Champaign, IL: American Oil Chemists' Society.Google Scholar
Trautwein, EA, Liang, J & Hayes, KC (1993) Cholesterol gallstone induction in hamsters reflects strain differences in plasma lipoproteins and bile acid profiles. Lipids 28, 305–312.CrossRefGoogle ScholarPubMed
Xu, R, Yokoyama, WH, Irving, D, Rein, D, Walzem, RL & German, JB (1998) Effect of dietary catechin and vitamin E on aortic fatty streak accumulation in hypercholesterolemic hamsters. Atherosclerosis 137, 29–36.CrossRefGoogle ScholarPubMed
Yagyu, H, Ishibashi, S, Chen, Z, Osuga, J, Okazaki, M, Perrey, S, Kitamine, T, Shimanda, M, Ohashi, K, Harada, K, Shionoira, F, Yahagi, N, Gotoda, T, Yazaki, Y & Yamada, N (1999) Overexpressed lipoprotein lipase protects against atherosclerosis in apolipoprotein E knockout mice. Journal of Lipid Research 40, 1677–1685.CrossRefGoogle ScholarPubMed
Yang, W-S & Deeb, SS (1998) Sp1 and Sp3 transactivate the human lipoprotein lipase gene promoter through binding to a CT element: synergy with the sterol regulatory element binding protein and reduced transactivation of a naturally occurring promoter variant. Journal of Lipid Research 39, 2054–2064.CrossRefGoogle Scholar
Zhang, Y, Repa, JJ, Gauthier, K & Mangelsdorf, DJ (2001) Regulation of lipoprotein lipase by the oxysterol receptors, LXR alpha and LXR beta. Journal of Biological Chemistry 276, 43018–43024.CrossRefGoogle Scholar