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Genetic determinants of plasma lipid response to dietary intervention: the role of the APOA1/C3/A4 gene cluster and the APOE gene

Published online by Cambridge University Press:  09 March 2007

Jose M. Ordovas*
Affiliation:
Lipid Metabolism Laboratory, JM-USDA-Human Nutrition Research Center on Aging at Tufts University, 711 Washington Street, Boston, MA, 02111, USA
Ernst J. Schaefer
Affiliation:
Lipid Metabolism Laboratory, JM-USDA-Human Nutrition Research Center on Aging at Tufts University, 711 Washington Street, Boston, MA, 02111, USA
*
*Corresponding author: Jose M. Ordovas, fax +1 617 556 3103, email: [email protected]
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Abstract

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Polymorphisms at the APOA1/C3/A4 gene cluster and the APOE gene have been extensively studied in order to examine their potential association with plasma lipid levels, coronary heart disease risk and more recently with inter-individual variability in response to dietary therapies. Although the results have not been uniform across studies, the current research supports the concept that variation at these genes explains a significant, but still rather small, proportion of the variability in fasting and postprandial plasma lipid responses to dietary interventions. This information constitutes the initial frame to develop panels of genetic markers that could be used to predict individual responsiveness to dietary therapy for the prevention of coronary heart disease. Future progress in this complex area will come from experiments carried out using animal models, and from carefully controlled dietary protocols in humans that should include the assessment of several other candidate gene loci coding for products that play a relevant role in lipoprotein metabolism (i.e. APOB, CETP, LPL, FABP2, SRBI, ABC1 and CYP7).

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Angotti, E, Mele, E, Costanzo, F & Avvedimento, EV (1994) A polymorphism (G → A transition) in the - 78 position of the apolipoprotein A-I promoter increases transcription efficiency. Journal of Biological Chemistry 269, 1737117374.CrossRefGoogle Scholar
Beisiegel, U, Weber, W, Ihrke, G, Herz, J & Stanley, KK (1989) The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 341, 162164.CrossRefGoogle ScholarPubMed
Blaauwwiekel, EE, Beusekamp, BJ, Sluiter, WJ, Hoogenberg, K & Dullaart, RPF (1998) Apolipoprotein E genotype is a determinant of low-density lipoprotein cholesterol and of its response to a low-cholesterol diet in type 1 diabetic patients with elevated urinary albumin excretion. Diabetic Medicine 15, 10311035.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Boerwinkle, E, Brown, SA, Rohrbach, K, Gotto, AM & Patsch, W (1991) Role of apolipoprotein E and B gene variation in determining response of lipid, lipoprotein, and apolipoprotein levels to increased dietary cholesterol. American Journal Human Genetics 49, 11451154.Google Scholar
Bruns, GA, Karathanasis, SK & Breslow, JL (1984) Human apolipoprotein AI-CIII gene complex is located in chromosome 11. Arteriosclerosis 4, 97104.CrossRefGoogle Scholar
Carmena, R, Roederer, G, Mailloux, H, Lussier-Cacan, S & Davignon, J (1993) The response to lovastatin treatment in patients with heterozygous familial hypercholesterolemia is modulated by apolipoprotein E polymorphism. Metabolism 42, 895901.CrossRefGoogle ScholarPubMed
Carmena-Ramon, RF, Ascaso, JF, Real, JT, Ordovas, JM & Carmena, R (1998) Genetic variation at the ApoA-IV gene locus and response to diet in familial hypercholesterolemia. Arteriosclerosis, Thrombosis and Vascular Biology 18, 12661274.CrossRefGoogle ScholarPubMed
Carmena-Ramon, RF, Ordovas, JM, Ascaso, JF, Real, J, Priego, MA & Carmena, R (1998) Influence of genetic variation at the apoA-I gene locus on lipid levels and response to diet in familial hypercholesterolemia. Atherosclerosis 139, 107113.Google Scholar
Clifton, PM, Abbey, M, Noakes, M, Beltrame, S, Rumbelow, N & Nestel, PJ (1995) Body fat distribution is a determinant of the high-density lipoprotein response to dietary fat and cholesterol in women. Arteriosclerosis, Thrombosis and Vascular Biology 15, 10701078.CrossRefGoogle ScholarPubMed
Cobb, MM, Teitlebaum, H, Risch, N, Jekel, J & Ostfeld, A (1992) Influence of dietary fat, apolipoprotein E phenotype, and sex on plasma lipoprotein levels. Circulation 86, 849857.CrossRefGoogle ScholarPubMed
Cobb, MM & Risch, N (1993) Low-density lipoprotein cholesterol responsiveness to diet in normolipidemic subjects. Metabolism 42, 713.Google Scholar
Dammerman, M, Sandkuijl, LA, Halaas, JL, Chung, W & Breslow, JL (1993) An apolipoprotein CIII haplotype protective against hypertriglyceridemia is specified by promoter and 3′ untranslated region polymorphisms. Proceedings of the National Academy of Sciences, USA 90, 45624566.CrossRefGoogle ScholarPubMed
Danek, GM, Valenti, M, Baralle, FE & Romano, M (1998) The A/G polymorphism in the - 78 position of the apolipoprotein A-I promoter does not have a direct effect on transcriptional efficiency. Biochimica et Biophysica Acta 1398, 6774.CrossRefGoogle Scholar
Davignon, J, Gregg, RE & Sing, CF (1988) Apolipoprotein E polymorphism and atherosclerosis. Arteriosclerosis 8, 121.CrossRefGoogle ScholarPubMed
Dixon, LB, Shannon, BM, Tershakovec, AM, Bennett, MJ, Coates, PM & Cortner, JA (1997) Effects of family history of heart disease, apolipoprotein E phenotype, and lipoprotein(a) on the response of children's plasma lipids to change in dietary lipids. American Journal of Clinical Nutrition 66, 12071217.CrossRefGoogle ScholarPubMed
Dreon, DM, Fernstrom, HA, Miller, B & Krauss, RM (1995) Apolipoprotein E isoform phenotype and LDL subclass response to a reduced-fat diet. Arteriosclerosis and Thrombosis 15, 105111.CrossRefGoogle ScholarPubMed
Fielding, CJ, Shore, VG & Fielding, PE (1972) A protein co-factor of lecithin:cholesterol acyltransferase. Biochemical & Biophysical Research Communications 46, 14931498.CrossRefGoogle Scholar
Fisher, EA, Blum, CB, Zannis, VI & Breslow, JL (1983) Independent effects of dietary saturated fat and cholesterol on plasma lipids, lipoproteins, and apolipoprotein E. Journal of Lipid Research 24, 10391048.CrossRefGoogle ScholarPubMed
Fisher, RM, Burke, H, Nicaud, V, Ehnholm, C & Humphries, SE (1999) Effect of variation in the apoA-IV gene on body mass index and fasting and postprandial lipids in the European Atherosclerosis Research Study II. Journal of Lipid Research 40, 287294.CrossRefGoogle ScholarPubMed
Gaddi, A, Ciarrocchi, A, Matteucci, A, Rimondi, S, Ravaglia, G, Descovich, GC & Sirtori, CR (1991) Dietary treatment for familial hypercholesterolemia — differential effects of dietary soy protein according to the apolipoprotein E phenotypes. American Journal of Clinical Nutrition 53, 11911196.CrossRefGoogle Scholar
Hunninghake, DB, Stein, EA, Dujovne, CA, Harris, WS, Feldman, EB, Miller, VT, Tobert, JA, Laskarzewski, PM, Quiter, E, Held, J, Taylor, AM, Hopper, S, Leonard, SB & Brewer, BK (1993) The efficacy of intensive dietary therapy alone or combined with lovastatin in outpatients with hypercholesterolemia. New England Journal of Medicine 328, 12131219.CrossRefGoogle ScholarPubMed
Jansen, S, Lopez-Miranda, J, Ordovas, JM, Zambrana, JL, Marin, C, Ostos, MA, Castro, P, McPherson, R, Lopez Segura, F, Blanco, A, Jimenez Pereperez, JA & Perez-Jimenez, F (1997) Effect of 360His mutation in apolipoprotein A-IV on plasma HDL-cholesterol response to dietary fat. Journal of Lipid Research 38, 19952002.CrossRefGoogle ScholarPubMed
Jansen, S, Lopez-Miranda, J, Salas, J, Ordovas, JM, Castro, P, Marin, C, Ostos, MA, Lopez-Segura, F, Jimenez-Pereperez, JA, Blanco, A & Perez-Jimenez, F (1997) Effect of 347-serine mutation in apoprotein A-IV on plasma LDL cholesterol response to dietary fat. Arteriosclerosis, Thrombosis & Vascular Biology 17, 15321538.Google Scholar
Jeenah, M, Kessling, A, Miller, N & Humphries, SE (1990) G to A substitution in the promoter region of the apolipoprotein AI gene is associated with elevated serum apolipoprotein AI and high density lipoprotein cholesterol concentrations. Molecular Biology & Medicine 7, 233241.Google ScholarPubMed
Jenkins, DJA, Hegele, RA, Jenkins, AL, Connelly, PW, Hallak, K, Bracci, P, Kashtan, H, Corey, P, Pintilia, M, Stern, H & Bruce, R (1993) The apolipoprotein E gene and the serum low-density lipoprotein cholesterol response to dietary fiber. Metabolism 42, 585593.CrossRefGoogle ScholarPubMed
Juo, SHH, Wyszynski, DF, Beaty, TH, Huang, HY & Bailey-Wilson, JE (1999) Mild association between the A/G polymorphism in the promoter of the apolipoprotein A-I gene and aplipoprotein A-I levels: a meta-analysis. American Journal of Medical Genetics 82, 235241.Google Scholar
Karathanasis, SK (1985) Apolipoprotein multigene family: tandem organization of human apolipoprotein. A-I, C-III and A-IV genes. Proceedings of the National Academy of Sciences, USA 82, 63746378.CrossRefGoogle Scholar
Lefevre, M, Ginsberg, HN, Kris-Etherton, PM, Elmer, PJ, Stewart, PW, Ershow, A, Pearson, TA, Roheim, PS, Ramakrishnan, R, Derr, J, Gordon, DJ & Reed, R (1997) ApoE genotype does not predict lipid response to changes in dietary saturated fatty acids in a heterogeneous normolipidemic population. The DELTA Research Group. Dietary Effects on Lipoproteins and Thrombogenic Activity. Arteriosclerosis, Thrombosis & Vascular Biology 17, 29142923.Google Scholar
Lehtimaki, T, Moilanen, T, Solakivi, T, Laippala, P & Ehnholm, C (1992) Cholesterol-rich diet induced changes in plasma lipids in relation to apolipoprotein E phenotype in healthy students. Annals of Medicine 24, 6166.Google Scholar
Lehtimaki, T, Frankberg-Lakkala, H, Solakivi, T, Koivisto, A, Laippala, P, Ehnholm, C, Jokela, H, Koivula, T & Nikkari, T (1997) The effect of short-term fasting, apolipoprotein E gene polymorphism, and sex on plasma lipids. American Journal of Clinical Nutrition 66, 599605.CrossRefGoogle ScholarPubMed
Li, WW, Dammerman, MM, Smith, JD, Metzger, S, Breslow, JL & Leff, T (1995) Common genetic variation in the promoter of the human apo CIII gene abolishes regulation by insulin and may contribute to hypertriglyceridemia. Journal of Clinical Investigation 96, 26012605.CrossRefGoogle ScholarPubMed
Loktionov, A, Bingham, SA, Vorster, H, Jerling, JC, Runswick, SA & Cummings, JH (1998) Apolipoprotein E genotype modulates the effect of black tea drinking on blood lipids and blood coagulation factors: a pilot study. British Journal of Nutrition 79, 133139.CrossRefGoogle ScholarPubMed
Lopez-Miranda, J, Ordovas, JM, Espino, A, Marin, C, Salas, J, Lopez-Segura, F, Jimenez-Pereperez, J & Perez-Jimenez, F (1994) Influence of mutation in human apolipoprotein A-1 gene promoter on plasma LDL cholesterol response to dietary fat. Lancet 343, 12461249.CrossRefGoogle ScholarPubMed
Lopez-Miranda, J, Ordovas, JM, Mata, P, Lichtenstein, AH, Clevidence, B, Judd, JT & Schaefer, EJ (1994) Effect of apolipoprotein E phenotype on diet-induced lowering of plasma low density lipoprotein cholesterol. Journal of Lipid Research 35, 19651975.CrossRefGoogle ScholarPubMed
Lopez-Miranda, J, Jansen, S, Ordovas, JM, Salas, J, Marin, C, Castro, P, Ostos, MA, Cruz, G, Lopez-Segura, F, Blanco, A, Jimenez-Pereperez, J & Perez-Jimenez, F (1997) Influence of the SstI polymorphism at the apolipoprotein C-III gene locus on the plasma low-density-lipoprotein-cholesterol response to dietary monounsaturated fat. American Journal of Clinical Nutrition 66, 97103.CrossRefGoogle ScholarPubMed
Mahley, RW (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240, 622630.Google Scholar
Manttari, M, Kosninen, P, Enholm, C, Huttunen, JK & Manninen, V (1991) Apolipoprotein E polymorphism influences the serum cholesterol response to dietary intervention. Metabolism 40, 217221.Google Scholar
Marshall, HW, Morrison, LC, Wu, LL, Anderson, JL, Corneli, PS, Stauffer, DM, Allen, A, Karagounis, LA & Ward, RH (1994) Apolipoprotein polymorphisms fail to define risk of coronary artery disease: results of a prospective, angiographically controlled study. Circulation 89, 567577.CrossRefGoogle ScholarPubMed
Martin, LJ, Connelly, PW, Nancoo, D, Wood, N, Zhang, ZJ, Maguire, G, Quinet, E, Tall, AR, Marcel, YL & McPherson, R (1993) Cholesteryl ester transfer protein and high density lipoprotein responses to cholesterol feeding in men: relationship to apolipoprotein E genotype. Journal of Lipid Research 34, 437446.Google Scholar
Mata, P, Ordovas, JM, Lopez-Miranda, J, Lichtenstein, AH, Clevidence, B, Judd, JT & Schaefer, EJ (1994) ApoA-IV phenotype affects diet-induced plasma LDL cholesterol lowering. Arteriosclerosis and Thrombosis 14, 884891.CrossRefGoogle ScholarPubMed
Mata, P, Lopez-Miranda, J, Pocovi, M, Alonso, R, Lahoz, C, Marin, C, Garces, C, Cenarro, A, Perez-Jimenez, F, De Oya, M & Ordovas, JM (1998) Human apolipoprotein A-I gene promoter mutation influences plasma low density lipoprotein cholesterol response to dietary fat saturation. Atherosclerosis 137, 367376.CrossRefGoogle ScholarPubMed
McCombs, RJ, Marcadis, DE, Ellis, J & Weinberg, RB (1994) Attenuated hypercholesterolemic response to a high-cholesterol diet in subjects heterozygous for the apolipoprotein A-IV-2 allele. New England Journal of Medicine 331, 706710.Google Scholar
Meng, QH, Pajukanta, P, Valsta, L, Aro, A, Pietinen, P & Tikkanen, MJ (1997) Influence of apolipoprotein A-1 promoter polymorphism on lipid levels and responses to dietary change in Finnish adults. Journal of Internal Medicine 241, 373378.CrossRefGoogle ScholarPubMed
Miettinen, TA, Gylling, H & Vanhanen, H (1988) Serum cholesterol response to dietary cholesterol and apoprotein E phenotype. Lancet 2, 1261.CrossRefGoogle ScholarPubMed
Miettinen, TA, Gylling, H, Vanhanen, H & Ollus, A (1992) Cholesterol absorption, elimination, and synthesis related to LDL kinetics during varying fat intake in men with different apoprotein E phenotypes. Arteriosclerosis and Thrombosis 12, 10441052.CrossRefGoogle ScholarPubMed
Nemeth, A, Szakmary, KA, Kramer, J, Dinya, E, Pados, G, Fust, G & Huettinger, M (1995) Apolipoprotein E and complement C3 polymorphism and their role in the response to gemfibrozil and low fat low cholesterol therapy. European Journal of Clinical Chemistry and Clinical Biochemistry 33, 799804.Google ScholarPubMed
Nestel, P, Simons, L, Barter, P, Clifton, P, Colquhoun, D, Hamilton-Craig, I, Sikaris, K & Sullivan, D (1997) A comparative study of the efficacy of simvastatin and gemfibrozil in combined hyperlipoproteinemia: predicition of response by baseline lipids, apoE genotype, lipoprotein(a) and insulin. Atherosclerosis 129, 231239.CrossRefGoogle Scholar
Ordovas, JM (1999 a) The genetics of serum lipid responsiveness to dietary interventions. Proceedings of the Nutrition Society 58, 171187.Google Scholar
Ordovas, JM & Schaefer, EJ (1999 b) Genes, variation of cholesterol and fat intake and serum lipids. Current Opinion In Lipidology 10, 1522.CrossRefGoogle ScholarPubMed
Ordovas, JM & Schaefer, EJ (1999) Treatment of dyslipidemia: genetic interactions with diet and drug therapy. Current Atherosclerosis Reports 1, 1623.Google Scholar
Ordovas, JM, Litwack-Klein, L, Wilson, PWF, Schaefer, MM & Schaefer, EJ (1987) Apolipoprotein E isoform phenotyping methodology and population frequency with identification of apoE1 and apoE5 isoforms. Journal of Lipid Research 28, 371380.CrossRefGoogle ScholarPubMed
Ordovas, JM, Cassidy, DK, Civeira, F, Bisgaier, CL & Schaefer, EJ (1989) Familial apolipoprotein A-I, C-III, and A-IV deficiency and premature atherosclerosis due to deletion of a gene complex on chromosome 11. Journal of Biological Chemistry 264, 1633916342.CrossRefGoogle ScholarPubMed
Ordovas, JM, Civeira, F, Genest, J, Craig, S, Robbins, AH, Meade, T, Pocovi, M, Frossard, PM, Masharani, U & Wilson, PW et al. (1991) Restriction fragment length polymorphisms of the apolipoprotein A-I, C-III, A-IV gene locus. Relationships with lipids, apolipoproteins, and premature coronary artery disease. Atherosclerosis 87, 7586.Google Scholar
Ordovas, JM, Lopez-Miranda, J, Perez-Jimenez, F, Rodriguez, CR, Park, J, Cole, T & Schaefer, EJ (1995) Effect of apolipoprotein E and A-IV phenotypes on the low density lipoprotein response to HMG-CoA reductase inhibitor therapy. Atherosclerosis 113, 157166.CrossRefGoogle ScholarPubMed
Ostos, MA, Lopez-Miranda, J, Ordovas, JM, Marin, C, Blanco, A, Castro, P, Lopez-Segura, F, Jimenez, Pereperez, JA, & Perez-Jimenez, F (1998) Dietary fat clearance is modulated by genetic variation in apolipoprotein A-IV gene locus. Journal of Lipid Research 39, 24932500.CrossRefGoogle ScholarPubMed
Park, S, Snook, JT, Bricker, L, Morroco, M, Van Voorhis, R, Stasny, E & Lee, MS (1996) Relative effects of high saturated fatty acid levels in meat, dairy products,and tropical oils on serum lipoproteins and low-density lipoprotein degradation by mononuclear cells in healthy males. Metabolism 45, 550558.CrossRefGoogle ScholarPubMed
Pasagian-Macaulay, A, Aston, CE, Ferrell, RE, McAllister, A, Wing, RR & Kuller, LH (1997) A dietary and behavioral intervention designed to lower coronary heart disease. Risk factors are unaffected by variation at the APOE gene locus. Atherosclerosis 132, 221227.CrossRefGoogle ScholarPubMed
Paul-Hayase, H, Rosseneu, M, Van Bervliet, JP, Deslypere, JP & Humphries, SE (1992) Polymorphisms in the apolipoprotein (apo) AI-CIII-AIV gene cluster: detection of genetic variation determining plasma apo AI, apo CIII and apo AIV concentrations. Human Genetics 88, 439446.Google Scholar
Reichl, D & Miller, NE (1989) Pathophysiology of reverse cholesterol transport: insights from inherited disorders of lipoprotein metabolism. Arteriosclerosis 9, 785797.CrossRefGoogle ScholarPubMed
Salas, J, Jansen, S, Lopez-Miranda, J, Ordovas, JM, Castro, P, Marin, C, Ostos, MA, Bravo, MD, Jimenez Pereperez, JA, Blanco, A, Lopez-Segura, F & Perez-Jimenez, F (1998) The SstI polymorphism of the apolipoprotein C-III gene determines the insulin response to an oral glucose tolerance test after consumption of a diet rich in saturated fats. American Journal of Clinical Nutrition 68, 396401.CrossRefGoogle Scholar
Sarkkinen, ES, Uusitupa, MIJ, Pietinen, P, Aro, A, Ahola, I, Penttilä, I, Kervinen, K & Kesäniemi, YA (1994) Long-term effects of three fat-modified diets in hypercholesterolemic subjects. Atherosclerosis 105, 923.CrossRefGoogle ScholarPubMed
Sarkkinen, E, Korhonen, M, Erkkila, A, Ebeling, T & Uusitupa, M (1998) Effect of apolipoprotein E polymorphism on serum lipid response to the separate modification of dietary fat and dietary cholesterol. American Journal of Clinical Nutrition 68, 12151222.Google Scholar
Savolainen, MJ, Rantala, M, Kervinen, K, Jarvi, L, Suvanto, K, Rantala, T & Kesaniemi, YA (1991) Magnitude of dietary effects on plasma cholesterol concentration: role of sex and apolipoprotein E phenotype. Atherosclerosis 86, 145152.CrossRefGoogle ScholarPubMed
Schaefer, EJ, Gregg, RE, Ghiselli, G, Forte, TM, Ordovas, JM, Zech, LA, Lindgren, FT & Brewer HB, Jr (1986) Familial apolipoprotein E deficiency. Journal of Clinical Investigation 78, 12061219.Google Scholar
Schaefer, EJ, Lamon-Fava, S, Johnson, S, Ordovas, JM, Schaefer, MM, Castelli, WP & Wilson, PWF (1994) Apolipoprotein E phenotype affects plasma lipoprotein levels in a gender- and menopausal status-dependent manner. Arteriosclerosis and Thrombosis 4, 11051113.CrossRefGoogle Scholar
Schaefer, EJ, Lichtenstein, AH, Lamon-Fava, S, Contois, JH, Li, Z, Rasmussen, H, McNamara, JR & Ordovas, JM (1995) Efficacy of a National Cholesterol Education Program Step 2 diet in normolipidemic and hypercholesterolemic middle-aged and elderly men and women. Arteriosclerosis, Thrombosis and Vascular Biology 15, 10791085.CrossRefGoogle ScholarPubMed
Smith, JD, Brinton, EA & Breslow, JL (1992) Polymorphism in the human apolipoprotein A-I gene promoter region. Association of the minor allele with decreased production rate in vivo and promoter activity in vitro. Journal of Clinical Investigation 89, 17961800.CrossRefGoogle ScholarPubMed
Tall, A, Welch, C, Applebaum-Bowden, D & Wassef, M (1997) Interaction of diet and genes in atherogenesis. Report of an NHLBI working group. Arteriosclerosis, Thrombosis and Vascular Biology 17, 33263331.CrossRefGoogle ScholarPubMed
Tikkanen, MJ, Huttunen, JK, Enholm, C & Pietinen, P (1990) Apolipoprotein E4 homozygosity predisposes to serum cholesterol elevation during high fat diet. Arteriosclerosis 10, 285288.CrossRefGoogle ScholarPubMed
Tso, TK, Park, S, Tsai, YH, Williams, G & Snook, JT (1998) Effect of apolipoprotein E polymorphism on serum lipoprotein response to saturated fatty acids. Lipids 33, 139148.CrossRefGoogle ScholarPubMed
Tuteja, R, Tuteja, N, Melo, C, Casari, G & Baralle, FE (1992) Transcription efficiency of human apolipoprotein A-I promoter varies with naturally occurring A to G transition. FEBS Letters 304, 98101.CrossRefGoogle ScholarPubMed
Tybjaerg-Hansen, A, Nordestgaard, BG, Gerdes, LU, Faergeman, O & Humphries, S (1993) Genetic markers in the apo AI-CIII-AIV gene cluster for combined hyperlipidemia, hypertriglyceridemia, and predisposition to atherosclerosis. Atherosclerosis 100, 157169.CrossRefGoogle ScholarPubMed
Uusitupa, MIJ, Ruuskanen, E, Mäkinen, E, Laitinen, J, Toskala, E, Kervinen, K & Kesäniemi, YA (1992) A controlled study on the effect of beta-glucan-rich oat bran on serum lipids in hypercholesterolemic subjects: relation to apolipoprotein E phenotype. Journal of the American College of Nutrition 11, 651659.CrossRefGoogle Scholar
Wang, XL, Badenhop, RB, Sim, AS & Wilcken, DEL (1998) The effect of transcription efficiency of the apolipoprotein AI gene of DNA variants at the 5′ untranslated region. International Journal of Clinical and Laboratory Research 28, 235241.CrossRefGoogle ScholarPubMed
Waterworth, DM, Ribalta, J, Nicaud, V, Dallongeville, J, Humphries, SE & Talmud, P (1999) ApoCIII gene variants modulate postprandial response to both glucose and fat tolerance tests. Circulation 99, 18721877.CrossRefGoogle ScholarPubMed
Xu, C-F, Angelico, F, Del, Ben, M, & Humphries, S (1993) Role of genetic variation at the apo AI-CIII-AIV gene cluster in determining plasma apo AI levels in boys and girls. Genetic Epidemiology 10, 113122.CrossRefGoogle ScholarPubMed
Zambón, D, Ros, E, Casals, E, Sanllehy, C, Bertomeu, A & Campero, I (1995) Effect of apolipoprotein E polymorphism on the serum lipid response to a hypolipidemic diet rich in monounsaturated fatty acids in patients with hypercholesterolemia and combined hyperlipidemia. American Journal of Clinical Nutrition 61, 141148.CrossRefGoogle Scholar