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Decreasing dietary fat saturation lowers HDL-cholesterol and increases hepatic HDL binding in hamsters

Published online by Cambridge University Press:  09 March 2007

A. H. M. Terpstra*
Affiliation:
Department of Laboratory Animal Science Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
P. van den Berg
Affiliation:
Department of Biochemistry Cardiovascular Research Institute COEUR, Erasmus University, Rotterdam, The Netherlands
H. Jansen
Affiliation:
Department of Biochemistry Cardiovascular Research Institute COEUR, Erasmus University, Rotterdam, The Netherlands
A. C. Beynen
Affiliation:
Department of Laboratory Animal Science Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands
A. van Tol
Affiliation:
Department of Biochemistry Cardiovascular Research Institute COEUR, Erasmus University, Rotterdam, The Netherlands
*
*Corresponding author: Dr A. H. M. Terpstra, fax +31 30 253 7997, email [email protected]
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Abstract

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In order to study the mechanism by which increasing unsaturation of dietary fat lowers HDL-cholesterol levels, we studied various measures of HDL metabolism in hamsters fed with fats with different degrees of saturation. Hamsters were fed on a cholesterol-enriched (1 g/kg) semipurified diet containing 200 g/kg of maize oil, olive oil, or palm oil for 9 weeks. Increasing saturation of dietary fat resulted in increasing concentrations of total plasma cholesterol (4·29 (SD 0·51), 5·30 (sd 0·67) and 5·58 (sd 0·76) mmol/l respectively, n 12) and HDL-cholesterol (3·31 (sd 0·50), 3·91 (sd 0·12) and 3·97 (sd 0·43) mmol/l) and these concentrations were significantly higher (P < 0·05) in the palm-oil and olive-oil-fed hamsters compared with the maize-oil group. Total plasma triacylglycerol levels also increased with increasing fat saturation (1·01 (sd 0·59), 1·56 (sd 0·65) and 2·75 (sd 1·03) mmol/l) and were significantly higher (P < 0·05) in the palm-oil group compared with the olive-oil and maize-oil-fed hamsters. The three diets did not have differential effects on plasma activity levels of lecithin: cholesterol acyltransferase (LCAT) and cholesteryl ester transfer protein (CETP). Levels of phospholipid transfer protein (PLTP) tended to be higher with increasing fat saturation but this effect was not significant. The capacity of liver membranes to bind human HDL3 was significantly higher (P < 0·05) in the hamsters fed with maize oil (810 (sd 100) ng HDL3 protein/mg membrane protein, n 4) compared with those fed on palm oil (655 (sd 56) ng/mg), whereas the olive-oil group had intermediate values (674 (sd 26) ng/mg). The affinity of HDL3 for the binding sites was not affected by the type of dietary fat. Hepatic lipase (EC 3.1.1.3) activity, measured in liver homogenates, increased with increasing fat saturation. We conclude that dietary maize oil, when compared with either olive oil or palm oil, may lower HDL-cholesterol concentrations by enhancing HDL binding to liver membranes.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Ahn, Y-S, Smith, D, Osada, J, Li, Z, Schaefer, EJ and Ordovas, JM (1994) Dietary fat saturation affects apolipoprotein gene expression and high density lipoprotein size distribution in Golden Syrian hamster .Journal of Nutrition 124, 21472155.CrossRefGoogle Scholar
Allain, CC, Poon, LS, Chen, CGS and Richmond, W (1974) Enzymatic determination of total cholesterol. Clinical Chemistry 20, 476482.CrossRefGoogle Scholar
Baudet, MF and Jacotot, B (1988) Dietary fats and lecithin-cholesterol acyltransferase activity in healthy humans. Annals of Nutrition and Metabolism 32, 352359.CrossRefGoogle ScholarPubMed
Bensadoun, A and Berryman, DE (1996) Genetics and molecular biology of hepatic lipase. Current Opinion in Lipidology 7, 7781.CrossRefGoogle ScholarPubMed
Beynen, AC (1988) Dietary monounsaturated fatty acids and liver cholesterol. Artery 15, 170175.Google ScholarPubMed
Bravo, E, Cantafora, A, Calccabrini, A and Ortu, G (1994) Why prefer the Golden Syrian hamster (Mesocritus auratus) to the Wistar rat in experimental studies on plasma lipoprotein metabolism?. Comparative Biochemistry and Physiology 107, 347355.Google Scholar
Brown, MS and Goldstein, JL (1986) A receptor mediated pathway for cholesterol homeostasis. Science 232, 3437.CrossRefGoogle ScholarPubMed
Bucolo, G and David, H (1973) Quantitative determination of serum triglycerides by the use of enzymes. Clinical Chemistry 19, 476482.CrossRefGoogle ScholarPubMed
De Crom, MPG, van Haperen, MJ, Puchois, P Fruchart J-C, van Gent, T, van Tol, A and van der Kamp, AWM (1989) Binding characteristics of high density lipoprotein subclasses to porcine liver, adrenal and skeletal muscle plasma membranes. International Journal of Biochemistry 21, 649656.CrossRefGoogle ScholarPubMed
Dietschy, JM (1998) Dietary fatty acids and the regulation of plasma low density lipoprotein cholesterol concentrations. Journal of Nutrition 128, 444S448S.CrossRefGoogle ScholarPubMed
Dietschy, JM, Turley, SD and Spady, DK (1993) Role of liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. Journal of Lipid Research 34, 16371659.CrossRefGoogle ScholarPubMed
Dullaart, RPF, Sluiter, WJ, Dikkeschei, LD, Hoogenberg, K and van Tol, A (1994) Effect of adiposity on plasma lipid transfer protein activities: a possible link between insulin resistance and high density lipoprotein metabolism. European Journal of Clinical Investigation 24, 188194.CrossRefGoogle ScholarPubMed
Ebert, DL, Warren, RJ, Barter, PJ and Mitchell, A (1993) Infusion of atherogenic lipoprotein particles increases hepatic lipase activity in the rabbit. Journal of Lipid Research 34, 8994.CrossRefGoogle ScholarPubMed
Fernandez, ML and McNamara DJ (1991) Characterization of high-density lipoprotein binding to guinea pig hepatic membranes: effects of dietary fat quality and cholesterol feeding .Metabolism 40, 127134.CrossRefGoogle ScholarPubMed
Groener, JEM, Pelton, RW and Kostner, GM (1986) Improved estimation of cholesteryl ester transfer/exchange activity in serum or plasma. Clinical Chemistry 32, 283286.CrossRefGoogle ScholarPubMed
Groener, JEM, van Ramshorst, EM, Katan, MB, Mensink, RP and van Tol, A (1991) Diet-induced alteration in the activity of plasma lipid transfer protein in normolipidemic human subjects. Atherosclerosis 87, 221226.CrossRefGoogle ScholarPubMed
Jansen, H and Birkenhäger JC (1981) Liver lipase-like activity in human and hamster adrenocorticol tissue .Metabolism 30, 428430.CrossRefGoogle Scholar
Jansen, H, Lammers, R, Baggen, MGA, Wouters, NMH and Birkenhäger JC (1989) Circulating and liver-bound salt resistant hepatic lipases in the golden hamster. Biochimica et Biophysica Acta 1001, 4449.CrossRefGoogle ScholarPubMed
Jauhiainen, M, Metso, J, Pahlman, R, Blomqvist, S, van Tol, A and Ehnholm, C (1993) Human plasma lipid transfer protein causes high density lipoprotein conversion. Journal of Biological Chemistry 268, 40324036.CrossRefGoogle Scholar
Jones, PJH, Ridgen, JE and Benson, AP (1990) Influence of dietary fatty acid composition on cholesterol synthesis and esterification in hamsters .Lipids 25, 815820.CrossRefGoogle ScholarPubMed
Khosla, P and Sundram, K (1996) Effect of dietary fatty acid composition on plasma cholesterol. Progress in Lipid Research 35, 93132.CrossRefGoogle ScholarPubMed
Kowala, MC (1993) Effect of an atherogenic diet on lipoprotein cholesterol profile in the F1B hybrid hamster .Atherosclerosis 103, 293294.CrossRefGoogle Scholar
Kurushima, H, Hayaki, K, Shingu, T, Shingu, T, Kugu, Y, Ohtani, H, Okura, Y, Tanaka, K, Yasunobu, Y, Nomura, K and Kajiyama, G (1995) Opposite effects on cholesterol metabolism and their mechanisms induced by dietary oleic acid and palmitic acid in hamsters. Biochimica et Biophysica Acta 1258, 251256.Google ScholarPubMed
Lagrost, L, Mensink, RP Guyard-Dangremont V, Temme, EHM, Desmuraux, C, Athias, A, Hornstra, G and Gambert, P (1999) Variations in serum cholesteryl ester transfer and phospholipid transfer activities in healthy women and men consuming diets enriched in lauric, palmitic or oleic acids. Atherosclerosis 142, 395402.CrossRefGoogle ScholarPubMed
Lottenberg, AMP, Nunes, VS, Lottenberg, SA, Shimabukuro, AFM, Carrilho, AJF, Malagutti, S, Nakandakare, ER McPherson R and Quintao, ECR (1996) Plasma cholesteryl ester synthesis, cholesteryl ester transfer protein concentration and activity in hypercholesterolemic women. Effects of the degree of saturation of dietary fatty acids in the fasting and postprandial states. Atherosclerosis 126, 265275.CrossRefGoogle ScholarPubMed
McNamara DJ (1992) Dietary fatty acids, lipoproteins and cardiovascular disease. Advances in Lipid Research 36, 253351.Google Scholar
Mattson, FH and Grundy, SM (1985) Comparison of effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on plasma lipids and lipoproteins in man .Journal of Lipid Research 26, 194202.CrossRefGoogle ScholarPubMed
Meijer, GW, Demacker, PNM, van Tol, A, Groener, JEM, van der Palen, JGP, Stalenhoef, AFH, van Zutphen, LMF and Beynen, AC (1993) Plasma activities of lecithin:cholesterol acyltransferase, lipid transfer protein and post-heparin lipases in inbred strain of rabbits hypo- and hyper responsive to dietary cholesterol .Biochemical Journal 293, 729734.CrossRefGoogle Scholar
Mensink, RP and Katan, MB (1989) Effect of a diet enriched with monounsaturated or polyunsaturated fatty acids on levels of low-density and high-density lipoprotein cholesterol in healthy women and men. New England Journal of Medicine 321, 436441.CrossRefGoogle ScholarPubMed
Nestel, PJ (1970) Turnover of plasma esterified cholesterol: influence of dietary fat and carbohydrate and relation to plasma lipids and body weight. Clinical Science 38, 593600.CrossRefGoogle ScholarPubMed
Nicolosi, RJ, Wilson, TA, Lawton, C, Rogers, EJ, Wiseman, SA, Tijburg, LBM and Kritchevsky, D (1998) The greater atherogenicity of nonpurified diets versus semipurified diets in hamsters is mediated via differences in plasma lipoprotein cholesterol distribution, LDL oxidative susceptibility, and plasma α-tocopherol concentration .Journal of Nutritional Biochemistry 9, 591597.CrossRefGoogle Scholar
Quig, DW, Arbeeney, CM and Zilversmit, DB (1991) Effects of hyperlipidemias in hamsters on lipid transfer protein activity and unidirectional cholesteryl ester transfer in plasma. Biochimica et Biophysica Acta 1083, 257264.CrossRefGoogle ScholarPubMed
Schwab, US, Maliranta, HM, Sarkkinen, ES, Savolainen, MJ, Kesaniemi, YA and Uusitupa, MIJ (1996) Different effects of palmitic and stearic acid-enriched diets on serum lipids and lipoproteins and plasma cholesteryl ester transfer protein activity in healthy young women. Metabolism 45, 143149.CrossRefGoogle ScholarPubMed
Sessions, VA and Salter, AM (1995) Low density lipoprotein binding to monolayer cultures of hepatocytes isolated from hamsters fed different dietary fatty acids .Biochimica et Biophysica Acta 1258, 6169.CrossRefGoogle ScholarPubMed
Speijer, H, Groener, JEM, van Ramshorst, E and van Tol, A (1991) Different locations of cholesteryl ester transfer protein and phospholipid transfer protein activities in plasma .Atherosclerosis 90, 159168.CrossRefGoogle ScholarPubMed
Stein, Y, Dabach, Y, Hollander, G and Stein, O (1990) Cholesteryl ester transfer activity in hamster plasma: increase by fat and cholesterol rich diets. Biochimica et Biophysica Acta 1042, 138141.CrossRefGoogle ScholarPubMed
Swenson, TL (1992) Transfer proteins in reverse cholesterol transport. Current Opinion in Lipidology 3, 6774.CrossRefGoogle Scholar
Syvanne, M and Taskinen, M-R (1997) Lipids and lipoproteins as coronary risk factors in non-insulin-dependent diabetes mellitus. Lancet 350(Suppl.), 2023.CrossRefGoogle ScholarPubMed
Tall, AR, Krumholz, S, Olivecrona, T and Deckelbaum, RJ (1985) Plasma phospholipid transfer protein enhances transfer and exchange of phospholipids between very low density lipoproteins and high density lipoproteins during lipolysis. Journal of Lipid Research 26, 842851.CrossRefGoogle ScholarPubMed
Trautwein, EA, Liang, J and Hayes, KC (1993) Cholesterol gallstone induction in hamsters reflects strain differences in plasma lipoproteins and bile acid profiles. Lipids 28, 305312.CrossRefGoogle ScholarPubMed
Trautwein, EA Kunath-Rau A, Dietrich, J, Drusch, S and Erbersdobler, HF (1997) Effect of dietary fats rich in lauric, myristic, palmitic. oleic or linoleic acid on plasma, hepatic and biliary lipids in cholesterol-fed hamsters. British Journal of Nutrition 77, 605620.CrossRefGoogle ScholarPubMed
van Tol, A, Zock, PL van Gent, T, Scheek, LM and Katan, MB (1995) Dietary trans fatty acids increase serum cholesterylester transfer protein activity in man. Atherosclerosis 115, 129134.CrossRefGoogle ScholarPubMed
von Eckardstein, A, Jauhiainen, M, Huang, Y, Metso, J, Langer, C, Pussinen, P, Wu, S, Ehnholm, C and Assmann, G (1996) Phospholipid transfer protein mediated conversion of high density lipoproteins generates pre beta 1-HDL. Biochimica et Biophysica Acta 1301, 255262.CrossRefGoogle ScholarPubMed
Weingand, KW and Daggy, BP (1990) Quantification of high-density-lipoprotein cholesterol in plasma from hamsters by differential precipitation. Clinical Chemistry 36, 575.CrossRefGoogle ScholarPubMed