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Dietary myristic acid modifies the HDL-cholesterol concentration and liver scavenger receptor BI expression in the hamster*

Published online by Cambridge University Press:  09 March 2007

Carole Loison
Affiliation:
Laboratoire de Physiologie de la Nutrition (laboratoire associé à l' INRA), Université Paris-Sud, Centre d'Orsay, bâtiment 447, 91405 Orsay Cedex, France
François Mendy
Affiliation:
Résidence du parc de Béarn, 2, rue du calvaire, 92120 Saint-Cloud, France
Colette Sérougne
Affiliation:
Laboratoire de Physiologie de la Nutrition (laboratoire associé à l' INRA), Université Paris-Sud, Centre d'Orsay, bâtiment 447, 91405 Orsay Cedex, France
Claude Lutton*
Affiliation:
Laboratoire de Physiologie de la Nutrition (laboratoire associé à l' INRA), Université Paris-Sud, Centre d'Orsay, bâtiment 447, 91405 Orsay Cedex, France
*
*Corresponding author: Professor Claude Lutton, fax +33 1 69 15 70 74, email [email protected]
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Abstract

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The influence of myristic acid in a narrow physiological range (0·5 to 2·4 % of total dietary energy) on the plasma and hepatic cholesterol metabolism was investigated in the hamster. The hamsters were fed on a diet containing 12·5 g fat/100 g and 0·05 g cholesterol/100 g with 0·5 % myristic acid (LA diet) for 3 weeks (pre-period). During the following 3 weeks (test period), they were divided into four dietary groups with 0·5 % (LA), 1·2 % (LM), 1·8 % (ML) or 2·4 % (M) myristic acid. Finally, half the hamsters in each group were again fed the LA diet for another 3 weeks (post-period). At the end of the test period, the hepatic expression of the scavenger receptor BI (SR-BI) was lower in the LM, ML and M groups than in the LA group whereas the hepatic cholesteryl ester concentration was higher. Cholesterol 7α hydroxylase activity was lower in the ML and M groups than in the LA and LM groups while the sterol 27 hydroxylase and 3-hydroxy-3-methyl glutaryl coenzyme A reductase activities were not modulated by dietary myristic acid. This is the first time a negative correlation has been observed between the HDL-cholesterol concentration and the hepatic mass of SR-BI (r -0·69; P<0·0001) under physiological conditions. An inverse linear regression was also shown between SR-BI and the percentage of myristic acid in the diet (r -0·75; P<0·0001). The hepatic mass of SR-BI in the M group had increased at the end of the post-period compared with the test-period values. The present investigation shows that myristic acid modulates HDL-cholesterol via a regulation of the SR-BI expression.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2002

Footnotes

*

Supported by a CERIN grant.

References

Acton, S, Rigotti, A, Landschulz, KR, Xu, S, Hobbs, H & Krieger, M (1996) Identification of scavenger receptor SR-B1 as high-density lipoprotein receptor. Science 271, 518520.CrossRefGoogle Scholar
Bennet, 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, 167173.CrossRefGoogle Scholar
Berner, LA (1993) Roundtable discussion on milk fat, Dairy foods, and coronary heart disease risk. Journal of Nutrition 123, 11751184.Google ScholarPubMed
Boutin, J (1997) Myristoylation. Cell Signal 91, 1535.CrossRefGoogle Scholar
Brendel, C, Fruchart, JC, Auwerx, J & Schoonjans, K (1998) Régulation transcriptionnelle du métabolisme du cholesterol (Transcriptional regulation of Cholestrol metabolism). Médecine/Sciences 15, 5662.CrossRefGoogle Scholar
Cheema, SK & Agellon, LB (1999) Metabolism of cholesterol is altered in the liver of C3H mice fed fats enriched with different C18 fatty acids. Journal of Nutrition 129, 17181724.CrossRefGoogle Scholar
Cheema, SK & Agellon, LB (2000) The murine and human cholesterol 7α hydroxylase gene promoters are differentially responsive to regulation by fatty acids mediated via peroxisome proliferator activated receptor α. Journal of Biochemical Chemistry 275, 1253012536.Google ScholarPubMed
Cheema, SK, Cikaluk, D & Agellon, LB (1997) Dietary fats modulate the regulatory potential of dietary cholesterol on cholesterol 7α-hydroxylase gene expression. Journal of Lipid Research 38, 315328.CrossRefGoogle Scholar
Chen, LD, Kushwaha, RS, Rice, KS, Carey, KD & McGill, HC (1998) Effect of dietary lipids on hepatic and extrahepatic sterol 27-hydroxylase activity in high- and low-responding baboons. Metabolism 47, 731738.CrossRefGoogle ScholarPubMed
Combettes-Souverain, M, Milliat, F, Sérougne, C, Férézou, J & Lutton, C (1999) SR-BI et métabolisme du cholestérol (SR-BI and cholesterol metabolism). Médecine/Sciences 15, 12521258.CrossRefGoogle Scholar
Einarsson, K, Angelin, B, Ewerth, S, Nilsell, K & Björkhem, I (1986) Bile acid synthesis in man: assay of hepatic microsomal cholesterol 7α-hydroxylase activity by isotope dilution-mass spectrometry. Journal of Lipid Research 27, 8288.CrossRefGoogle ScholarPubMed
Fielding, CJ & Young, SG (1999) The ABCs of cholesterol efflux. Nature Genetics 22, 316318.Google Scholar
Grundy, SM (1994) Influence of stearic acid on cholesterol metabolism relative to other long-chain fatty acids. American Journal of Clinical Nutrition 60, 986990.CrossRefGoogle ScholarPubMed
Grundy, SM (1997) What is the desirable ratio of saturated, polyunsaturated and monounsaturated fatty acid in the diet? American Journal of Clinical Nutrition 66, 988S990S.CrossRefGoogle ScholarPubMed
Hajri, T, Khosla, P, Pronczuk, A & Hayes, KC (1998 a) Myristic acid-rich fat raises plasma LDL by stimulating LDL production without affecting fractional clearance in gerbils fed a cholesterol-free diet. Journal of Nutrition 128, 477484.CrossRefGoogle ScholarPubMed
Hajri, T, Pronzuk, A & Hayes, KC (1998 b) Linoleic acid rich diet increases hepatic taurine and cholesterol 7 alpha hydroxylase activity in conjunction with altered bile acid composition and conjugation in gerbils. Journal of Nutrition Biochemistry 9, 249257.CrossRefGoogle Scholar
Hayes, KC & Khosla, P (1992) Dietary fatty acid thresholds and cholesterolemia. FASEB Journal 6, 26002607.CrossRefGoogle ScholarPubMed
Hegsted, DM, McGandy, RB, Myers, ML & Stare, FJ (1965) Quantitative effects of dietary fat on serum cholesterol in man. American Journal of Clinical Nutrition 17, 281295.CrossRefGoogle ScholarPubMed
Horton, JD, Cuthbert, JA & Spady, DK (1993) Dietary fatty acids regulate hepatic low density lipoprotein (LDL) transport by altering LDL receptor protein and mRNA levels. Journal of Clinical Investigation 92, 743749.CrossRefGoogle ScholarPubMed
Innis, SM, Quinlan, P & Diersen-Schade, D (1993) Saturated fatty acid chain length and positional distribution in infant formula: effects on growth and plasma lipids and ketones in piglets. American Journal of Clinical Nutrition 57, 382390.CrossRefGoogle ScholarPubMed
Jensen, RG (1996) The lipids in human milk. Lipids Research 35, 5392.CrossRefGoogle ScholarPubMed
Jensen, RG, Ferris, AM, Lammi-Keefe, CJ & Henderson, RA (1990) Lipids of bovine and human milks: a comparison. Journal of Dairy Science 73, 223240.CrossRefGoogle ScholarPubMed
Keys, A & Parlin, RW (1966) Serum cholesterol response to changes in dietary lipids. American Journal of Clinical Nutrition 19, 175181.CrossRefGoogle Scholar
Khosla, P, Hajri, T, Pronczuk, A & Hayes, KC (1997) Decreasing dietary lauric and myristic acids improves plasma lipids more favorably than decreasing palmitic acid in rhesus monkeys fed AHA step 1 type diet. Journal of Nutrition 127, 525S530S.CrossRefGoogle Scholar
Kosarsky, KF, Donahee, MH, Rigotti, A, Iqbal, SN, Edelman, ER & Krieger, M (1997) Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 387, 414417.CrossRefGoogle Scholar
Kovanen, PT, Brown, MJ & Goldstein, JL (1979) Increased binding of low density lipoprotein to liver membranes from rats treated with 17α-ethinyl estradiol. Journal of Biochemical Chemistry 254, 1136711373.Google Scholar
Kris-Etherton, PM & Dietschy, J (1997) Design criteria for studies examining individual fatty acids effects on cardiovascular disease risk factors: human and animal studies. American Journal of Clinical Nutrition 65S, 159S166S.Google Scholar
Kris-Etherton, PM & Yu, S (1997) Individual fatty acid effects on plasma lipids and lipoproteins: human studies. American Journal of Clinical Nutrition 65, 1628S1644S.CrossRefGoogle ScholarPubMed
Kushwaha, RS, Guntupalli, B, Rice, KS, Carey, KD & McGill, HC (1995) Effect of dietary cholesterol and fat on the expression of hepatic sterol 27-hydroxylase and other hepatic cholesterol-responsive genes in baboons (papio species). Arteriosclerosis Thrombosis and Vascular Biology 15, 14041411.CrossRefGoogle ScholarPubMed
Lindsey, S, Benattar, J, Pronczuk, A & Hayes, KC (1990) Dietary palmitic aid (16:0) enhances high density lipoprotein cholesterol and low density lipoprotein receptor mRNA abundance in hamsters. Proceedings of the Society of Experimental Biology and Medicine 195, 261269.CrossRefGoogle Scholar
Lopez, D & McLean, M (1999) Sterol regulatory element binding protein-1a binds to cis element in the promoter of the rat high density lipoprotein receptor SR-BI gene. Endocrinology 140, 56695681.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJ (1951) Protein measurement with Folin phenol reagent. Journal of Biochemical Chemistry 192, 265275.Google Scholar
Lutton, C (1990) Cholesterol and bile acids dynamics: comparative aspects. Reproduction Nutrition Development 30, 145160.CrossRefGoogle ScholarPubMed
Marrapodi, M & Chiang, JYL (2000) Peroxisome proliferator activated receptor α (PPARα) and agonist inhibit cholesterol 7α hydroxylase gene (CYP7A1) transcription. Journal of Lipid Research 41, 514520.CrossRefGoogle ScholarPubMed
Mensink, RP (1993) Effects of the individual saturated fatty acids on serum lipids and lipoproteins concentrations. American Journal of Clinical Nutrition 57, S711S714.CrossRefGoogle Scholar
Milliat, F, Grippois, D, Blouquit, MF, Ferezou, J, Serougne, C, Fidge, NH & Lutton, C (2000) Short and long-term effects of steptozotocin on dietary cholesterol absorption, plasma lipoproteins and liver lipoprotein receptors in rico rats. Experimental and Clinical Endocrinology and Diabetes 108, 436446.CrossRefGoogle Scholar
Mizutani, T, Yamada, K, Minegishi, T & Miyamoto, K (2000) Transcriptional regulation of rat scavenger receptor class B type I gene. Journal of Biochemical Chemistry 275, 2251222519.Google Scholar
Nelson, CM & Innis, SM (1999) Plasma lipoprotein fatty acids are altered by the positional distribution of fatty acids in infant formula triacylglycerols and human milk. American Journal of Clinical Nutrition 70, 6269.CrossRefGoogle ScholarPubMed
Nicolosi, RJ (1997) Dietary fat saturation effects on low-density lipoprotein concentrations and metabolism in various animal models. American Journal of Clinical Nutrition 65, 1617S1627S.CrossRefGoogle ScholarPubMed
Patel, DD, Knight, BL, Soutar, A, Gibbons, GF & Wade, DP (2000) The effect of peroxisome-proliferator-activated receptor α on the activity of the cholesterol 7α gene. Biochemical Journal 351, 747753.CrossRefGoogle Scholar
Philipp, BW & Shapiro, DJ (1979) Improved method for the assay and activation of 3-hydroxy-3-methylglutaryl CoA reductase. Journal of Lipid Research 20, 588593.CrossRefGoogle Scholar
Rader, DJ & Maugeais, C (2000) Genes influencing HDL metabolism: new perspectives and implications for atherosclerosis prevention. Molecular Medicine Today April, 170175.CrossRefGoogle Scholar
Rigotti, A, Trigatti, B, Penmam, M, Ray-Burn, H, Herz, J & Krieger, M (1997) A targeted mutation in the murine gene encoding the HDL receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proceedings of the National Academy of Sciences USA 94, 1261012615.CrossRefGoogle Scholar
Salter, AM, Mangiapane, EH, Bennet, AJ, Bruce, JS, Billet, MA, Anderton, KL, Marenah, CB, Lawson, N & White, DA (1998) The effect of different dietary fatty acids on lipoprotein metabolism: concentration-dependent effects of diet enriched in oleic, myristic, palmitic and stearic acids. British Journal of Nutrition 79, 195202.CrossRefGoogle ScholarPubMed
Schneider, WJ, Beisiegel, U, Goldstein, JL & Brown, MS (1982) Purification of the low density lipoprotein receptor, on acidic glycoprotein of 164000 molecular weight. Journal of Biochemical Chemistry 257, 26642673.Google Scholar
Small, DM (1991) The effects of glyceride structure on absorption and metabolism. Annual Review of Nutrition 11, 413434.CrossRefGoogle ScholarPubMed
Snook, JT, Williams, G, Tsai, YH & Lee, N (1999) Effect of synthetic triglyceride of myristic, palmitic and stearic acid on serum lipoprotein metabolism. European Journal of Clinical Nutrition 53, 597605.CrossRefGoogle ScholarPubMed
Souidi, M, Parquet, M & Lutton, C (1998) Improved assay of hepatic microsomal cholesterol 7α-hydroxylase activity by use of hydroxyl-β-cyclodextrin and an NADPH regenerating system. Clinica Chimica Acta 269, 201217.CrossRefGoogle Scholar
Souidi, M, Parquet, M, Férézou, J & Lutton, C (1999) Modulation of cholesterol 7α hydroxylase and sterol 27-hydroxylase activities by steroids and physiological conditions in hamster. Life Science 64, 15851593.CrossRefGoogle ScholarPubMed
Spady, DK & Dietschy, JM (1983) Sterol synthesis in vivo in 18 tissues of the squirrel monkey, guinea pig, rabbit, hamster and rat. Journal of Lipid Research 24, 303315.CrossRefGoogle Scholar
Spady, DK & Dietschy, JM (1988) Interaction of dietary cholesterol and triglycerides in the regulation of hepatic low-density lipoprotein transport in the hamster. Journal of Clinical Investigation 81, 300309.CrossRefGoogle ScholarPubMed
Spady, DK, Kearney, DM & Hobbs, HH (1999) Polyunsaturated fatty acids up-regulate hepatic scavenger receptor B1 (SR-B1) expression and HDL cholesteryl ester uptake in the Hamster. Journal of Lipid Research 40, 13841394.CrossRefGoogle Scholar
Stein, O & Stein, Y (1999) Atheroprotective mechanisms of HDL. Atheroslerosis 144, 285301.CrossRefGoogle ScholarPubMed
Temme, EHM, Mensink, RP & Hornstra, G (1997) Effects of medium chain fatty acids (MCFA), myristic acid, and oleic acid on serum lipoprotein in healthy subjects. Journal of Lipid Research 38, 17461754.CrossRefGoogle ScholarPubMed
Tholstrup, T, Marckmann, P, Jespersin, J, Vessby, B, Jart, A & Sandstrom, B (1994) Effect on blood lipids, coagulation, and fibrinolysis of a fat high in myristic and a fat high in palmitic acid. American Journal of Clinical Nutrition 60, 919925.CrossRefGoogle Scholar
Tsai, YH, Park, S, Kosavic, J & Snook, JT (1999) Mechanisms mediating lipoprotein responses to diets with medium-chain triglyceride and lauric acid. Lipids 34, 895905.CrossRefGoogle ScholarPubMed
Varban, ML, Rinninger, F & Wang, N (1998) Targeted mutation reveals a central role for SR-BI in hepatic selective uptake of high density lipoprotein cholesterol. Proceedings of the National Academy of Sciences USA 95, 46194625.CrossRefGoogle ScholarPubMed
Vlahcevic, ZR, Jairah, SK, Heuman, DM, Stravitz, RT, Hylemon, PB, Avadhani, NG & Pandak, WM (1996) Transcriptional regulation of hepatic sterol 27-hydroxylase by bile acids. American Journal of Physiology 270, G646G652.Google ScholarPubMed
Von Eckardstein, A & Assmann, G (2000) Prevention of coronary heart disease by raising high-density lipoprotein cholesterol? Current Opinion in Lipidology 11, 627637.CrossRefGoogle ScholarPubMed
Wang, N, Arai, T, Ji, Y, Rinninger, F & Tall, AR (1998) Liver-specific overexpression of SR-BI decreases levels of VLDL Lipoprotein apoB, LDL lipoprotein apoB and HDL lipoprotein in transgenic mice. Journal of Biochemical Chemistry 273, 3292032926.Google ScholarPubMed
Weigand, KW & Daggy, PB (1990) Quantification of high-density cholesterol in plasma from hamsters by differential precipitation. Clinical Chemistry 36, 575.CrossRefGoogle Scholar
Woolett, LA, Spady, DK & Dietschy, JM (1992) Regulatory effects of the saturated fatty acids 6 0 through 18 0 on hepatic low density lipoprotein receptor activity in the hamster. Journal of Clinical Investigation 89, 11331141.CrossRefGoogle Scholar
Worgall, TS, Shurley, SL, Seo, T, Osborne, TF & Deckelbaum, RJ (1998) Polyunsaturated fatty acids decrease expression of promoters with sterol regulatory elements by decreasing levels of mature sterol regulatory element binding protein. Journal of Biochemical Chemistry 273, 2553725540.Google ScholarPubMed
Zock, PL, De Vries, JHM, De Fouw, NJ & Katan, MB (1995) Positional distribution of fatty acids in dietary triglycerides: effects on fasting blood lipoprotein concentrations in humans. American Journal of Clinical Nutrition 61, 4855.CrossRefGoogle ScholarPubMed