Hei Yi Zhuang is an isolated subgroup of the Zhuang minority in China. Little is known about the distribution of apolipoprotein (apo) E genetic variations and its role in lipid metabolism in this population. The present study was undertaken to compare the effect of apoE gene polymorphism on serum lipid levels between the Guangxi Hei Yi Zhuang and Han populations. A total of 873 subjects of Hei Yi Zhuang and 867 participants of Han Chinese were surveyed by a stratified randomized cluster sampling. Genotyping of apoE was performed using polymerase chain reaction and restriction fragment length polymorphism. The frequencies of 2, 3, and 4 alleles were 15.23%, 79.84%, and 4.93% in Hei Yi Zhuang, and 9.23%, 81.43%, and 9.34% in Han (P < 0.001); respectively. The frequencies of 2/ 2, 2/ 3, 2/ 4, 3/ 3, 3/ 4, and 4/ 4 genotypes were 4.70%, 17.86%, 3.21%, 68.16%, 5.50%, and 0.57% in Hei Yi Zhuang, and 2.54%, 9.23%, 4.15%, 70.70%, 12.23%, and 1.15% in Han (P < 0.001); respectively. Total cholesterol (TC), triglyceride (TG), low-density lipoprotein cholesterol (LDL-C), and apoB levels were lower in Hei Yi Zhuang than in Han (P < 0.01–0.001), but high-density lipoprotein cholesterol (HDL-C) levels and the ratio of apoA-I to apoB were higher in Hei Yi Zhuang than in Han (P < 0.001 for each). There were significant differences in TC, HDL-C, LDL-C, and apoB levels among the six genotypes in both ethnic groups (P < 0.01–0.001). Hyperlipidemia was positively correlated with age, body mass index, hypertension, alcohol consumption, and apoE allele in both populations (P < 0.05–0.001). TC, LDL-C, and apoB levels were positively correlated, and HDL-C levels were negatively associated with apoE genotypes in both ethnic groups (P < 0.001 for all). The differences in the lipid profiles between Hei Yi Zhuang and Han Chinese might partly attribute to the differences in apoE genotypic and allelic frequencies.
Get full access to this article
View all access options for this article.
References
1.
Kim HK, Chang SA, Choi EK, Kim YJ, Kim HS, Sohn DW, Oh BH, Lee MM, Park YB, Choi YS. Association between plasma lipids, and apolipoproteins and coronary artery disease: a cross-sectional study in a low-risk Korean population. Int J Cardiol101:435–440, 2005.
2.
Hokanson JE, Austin MA. Plasma triglyceride level is a risk factor for cardiovascular disease independent of high-density lipoprotein cholesterol level: a meta-analysis of population-based prospective studies. J Cardiovasc Risk3:213–319, 1996.
3.
Marz W, Scharnagl H, Winkler K, Tiran A, Nauck M, Boehm BO, Winkelmann BR. Low-density lipoprotein triglycerides associated with low-grade systemic inflammation, adhesion molecules, and angiographic coronary artery disease: the Ludwigshafen Risk and Cardiovascular Health study. Circulation110:3068–3074, 2004.
4.
Walldius G, Jungner I, Holme I, Aastveit AH, Kolar W, Steiner E. High apolipoprotein B, low apolipoprotein A-I, and improvement in the prediction of fatal myocardial infarction (AMORIS study): a prospective study. Lancet358:2026–2033, 2001.
5.
Boden WE. High-density lipoprotein cholesterol as an independent risk factor in cardiovascular disease: assessing the data from Framingham to the Veterans Affairs High-Density Lipoprotein Intervention Trail. Am J Cardiol86:19L–22L, 2000.
6.
Kowal RC, Herz J, Goldstein JL, Esser V, Brown MS. Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc Natl Acad Sci U S A86:5810–5814, 1989.
7.
Miettinen TA, Gylling H, Vanhanen H, Ollus A. Cholesterol absorption, elimination, and synthesis related to LDL kinetics during fat intake in men with different apoprotein E phenotypes. Arterioscler Thromb12:1044–1052, 1992.
8.
Mahley RW. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science240:622–630, 1988.
9.
Das HK, McPherson J, Bruns GAP, Karathanasis SK, Breslow JL. Isolation, characterization and mapping to chromosome 19 of the human apolipoprotein E gene. J Biol Chem260:6240–6247, 1985.
10.
Davignon J, Gregg RE, Sing CF. Apolipoprotein E polymorphism and atherosclerosis. Arteriosclerosis8:1–21, 1988.
Eichner JE, Dunn ST, Perveen G, Thompson DM, Stewart KE, Stroehla BC. Apolipoprotein E polymorphism and cardiovascular disease: A HuGE Review. Am J Epidemiol155:487–495, 2002.
13.
Braeckman L, De Bacquer D, Rosseneu M, De Backer G. Apolipoprotein E polymorphism in middle-aged Belgian men: phenotype distribution and relation to serum lipids and lipoproteins. Atherosclerosis120:67–73, 1996.
14.
Mahley RW, Pepin J, Palaoglu KE, Malloy MJ, Kane JP, Bersot TP. Low levels of high density lipoproteins in Turks, a population with elevated hepatic lipase: high density lipoprotein characterization and gender-specific effects of apolipoprotein E genotype. J Lipid Res41:1290–1301, 2000.
15.
Ruixing Y, Fengbing H, Shangling P, Dezhai Y, Weixiong L, Tangwei L, Yuming C, Jinzhen W, Limei Y, Jiandong H. Prevalence of hyperlipidemia and its risk factors for the middle-aged and elderly in the Guangxi Hei Yi Zhuang and Han populations. J Investig Med54:191–200, 2006.
16.
Ruixing Y, Yuming C, Shangling P, Fengbing H, Tangwei L, Dezhai Y, Jinzhen W, Limei Y, Weixiong L, Rongshan L, Jiandong H. Effects of demographic, dietary, and other lifestyle factors on the prevalence of hyperlipidemia in Guangxi Hei Yi Zhuang and Han populations. Eur J Cardiovasc Prev Rehabil13:977–984, 2006.
17.
Ruixing Y, Rongshan L, Weixiong L, Dezhai Y, Shangling P. Effect of the MTP–493 G/T polymorphism on the lipid profiles of the Guangxi Hei Yi Zhuang and Han populations. Eur J Lipid Sci Technol108:561–568, 2006.
18.
Ruixing Y, Guangqin C, Yong W, Weixiong L, Dezhai Y, Shangling P. Effect of the 3′APOB-VNTR polymorphism on the lipid profiles in the Guangxi Hei Yi Zhuang and Han populations. BMC Med Genet8:45–58, 2007.
19.
Hixson JE, Vernier DT. Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J Lipid Res31:545–548, 1990.
20.
Emi M, Wu LL, Robertson MA, Myers RL, Hegele RA, Williams RR, White R, Lalouel JM. Genotyping and sequence analysis of apolipoprotein E isoforms. Genomics3:373–379, 1988.
21.
Ruixing Y, Limei Y, Yuming C, Dezhai Y, Weixiong L, Muyan L, Fengping H, Jinzhen W, Guangqing Y, Zhenbiao N. Prevalence, awareness, treatment, control and risk factors of hypertension in the Guangxi Hei Yi Zhuang and Han populations. Hypertens Res29:423–432, 2006.
22.
Ruixing Y, Jiaqiang D, Dezhai Y, Weixiong L, Shangling P, Jinzhen W, Jiandong H, Xiuyan L. Effects of demographic characteristics, health-related behaviors and lifestyle factors on the prevalence of hypertension for the middle-aged and elderly in the Guangxi Hei Yi Zhuang and Han populations. Kidney Blood Press Res29:312–320, 2006.
23.
Cooperative Meta-analysis Group of China Obesity Task Force. Predictive values of body mass index and waist circumference to risk factors of related diseases in Chinese adult population. Zhonghua Liu Xing Bing Xue Za Zhi23:5–10, 2002.
24.
Hamsten A, Iselius L, Dahlén G, de Faire U. Genetic and cultural inheritance of serum lipids, low and high density lipoprotein cholesterol and serum apolipoproteins A-I, A-II and B. Atherosclerosis60:199–208, 1986.
25.
Gerdes LU, Klausen IC, Sihm I, Faergeman O. Apolipoprotein E polymorphism in a Danish population compared to findings in 45 other study populations around the world. Genet Epidemiol9:155–167, 1992.
26.
Menzel HJ, Kladetzky RG, Assmann G. Apolipoprotein E-polymorphism and coronary artery disease. Arteriosclerosis3:310–315, 1983.
27.
Utermann G, Kindermann I, Kaffarnik H, Steinmetz A. Apolipoprotein E phenotypes and hyperlipidemia. Hum Genet65:232–236, 1984.
28.
Zannis VI, Breslow JL. Human very low density lipoprotein apolipoprotein E isoprotein polymorphism is explained by genetic variation and posttranslational modification. Biochemistry20:1033–1041, 1981.
29.
Havel RJ. Familial dysbetalipoproteinemia: new aspects of pathogenesis and diagnosis. Med Clin North Am66:441–454, 1982.
30.
Ghiselli G, Gregg RE, Zech LA, Schaefer EJ, Brewer HB Jr. Phenotype study of apolipoprotein E isoforms in hyperlipoproteinaemic patients. Lancet2:405–407, 1982.
31.
Wardell MR, Suckling PA, Janus ED. Genetic variation in human apolipoprotein E. J Lipid Res23:1174–1182, 1982.
32.
Cumming AM, Robertson FW. Polymorphism at the apoprotein-E locus in relation to risk of coronary disease. Clin Genet25:310–313, 1984.
33.
Eggertsen G, Tegelman R, Ericsson S, Angelin B, Berglund L. Apolipoprotein E polymorphism in a healthy Swedish population: variation of allele frequency with age and relation to serum lipid concentrations. Clin Chem39:2125–2129, 1993.
34.
Ehnholm C, Lukka M, Kuusi T, Nikkila E, Utermann G. Apolipoprotein E polymorphism in the Finnish population: gene frequencies and relation to lipoprotein concentrations. J Lipid Res27:227–235, 1986.
35.
Lehtimaki T, Moilanen T, Viikari J, Akerblom HK, Ehnholm C, Ronnemaa T, Marniemi J, Dahlen G, Nikkari T. Apolipoprotein E phenotypes in Finnish youths: a cross-sectional and 6-year follow-up study. J Lipid Res31:487–495, 1990.
36.
Nakayama S, Kuzuhara S. Apolipoprotein E phenotypes in healthy normal controls and demented subjects with Alzheimer’s disease and vascular dementia in Mie Prefecture of Japan. Psychiatry Clin Neurosci53:643–648, 1999.
37.
Tsukamoto K, Watanabe T, Matsushima T, Kinoshita M, Kato H, Hashimoto Y, Kurokawa K, Teramoto T. Determination by PCR-RFLP of apo E genotype in a Japanese population. J Lab Clin Med121:598–602, 1993.
38.
Eto M, Watanabe K, Ishii K. A racial difference in apolipoprotein E allele frequencies between the Japanese and Caucasian populations. Clin Genet30:422–427, 1986.
39.
Kim KW, Jhoo JH, Lee KU, Lee DY, Lee JH, Youn JY, Lee BJ, Han SH, Woo JI. Association between apolipoprotein E polymorphism and Alzheimer’s disease in Koreans. Neurosci Lett277:145–148, 1999.
40.
Kim HC, Kim DK, Choi IJ, Kang KH, Yi SD, Park J, Park YN. Relation of apolipoprotein E polymorphism to clinically diagnosed Alzheimer’s disease in the Korean population. Psychiatry Clin Neurosci55:115–120, 2001.
41.
Kim HS, Kamboh MI. Genetic polymorphisms of apolipoproteins A-IV, E and H in Koreans. Hum Hered48:313–317, 1998.
42.
Svobodova H, Kucera F, Stulc T, Vrablik M, Amartuvshin B, Altannavch Ts, Ceska R. Apolipoprotein E gene polymorphism in the Mongolian population. Folia Biol (Praha)53:138–142, 2007.
43.
Tsunoda K, Harihara S, Dashnyam B, Semjidmaa D, Yamaguchi Y, Tanabe Y, Sakai N, Sato A, Sato K. Apolipoprotein E and H polymorphisms in Mongolian Buryat: allele frequencies and relationship with plasma lipid levels. Hum Biol74:659–671, 2002.
44.
Thelma BK, Juyal RC, Dodge HH, Pandav R, Chandra V, Ganguli M. APOE polymorphism in a rural older population-based sample in India. Hum Biol73:135–144, 2001.
45.
Singh P, Singh M, Gerdes U, Mastana SS. Apolipoprotein E polymorphism in India: high APOE*E3 allele frequency in Ramgarhia of Punjab. Anthropol Anz59:27–34, 2001.
46.
Tan CE, Tai ES, Tan CS, Chia KS, Lee J, Chew SK, Ordovas JM. APOE polymorphism and lipid profile in three ethnic groups in the Singapore population. Atherosclerosis170:253–260, 2003.
47.
Kobori S, Nakamura N, Uzawa H, Shichiri M. Influence of apolipoprotein E polymorphism on plasma lipid and apolipoprotein levels, and clinical characteristics of type III hyperlipoproteinemia due to apolipoprotein E phenotype E2/2 in Japan. Atherosclerosis69:81–88, 1988.
48.
Kao JT, Tsai KS, Chang CJ, Huang PC. The effects of apolipoprotein E polymorphism on the distribution of lipids and lipoproteins in the Chinese population. Atherosclerosis114:55–59, 1995.
49.
Zhang JG, Dong XZ, Yang WJ, Lu Q, He L. Population distributions of allele frequency of apolipoprotein E by age and gender in Han Chinese. Zhongguo Yao Li Xue Bao20:218–222, 1999.
50.
Jin ZQ, Fan YS, Ding J, Chen M, Fan W, Zhang GJ, Zhang BH, Yu SJ, Zhang YS, Ji WF, Zhang JG. Association of apolipoprotein E4 polymorphism with cerebral infarction in Chinese Han population. Acta Pharmacol Sin25:352–356, 2004.
51.
Hsieh MC, Lin SR, Yang YC, Chen HC, Lin JN, Shin SJ. Higher frequency of apolipoprotein E2 allele in type 2 diabetic patients with nephropathy in Taiwan. J Nephrol15:368–373, 2002.
52.
Sepehrnia B, Kamboh MI, Adams-Campbell LL, Bunker CH, Nwankwo M, Majumder PP, Ferrell RE. Genetic studies of human apolipoproteins. X. The effect of the apolipoprotein E polymorphism on quantitative levels of lipoproteins in Nigerian blacks. Am J Hum Genet45:586–591, 1989.
53.
Hallman DM, Boerwinkle E, Saha N, Sandholzer C, Menzel HJ, Csazar A, Utermann G. The apolipoprotein E polymorphism: a comparison of allele frequencies and effects in nine populations. Am J Hum Genet49:338–349, 1991.
54.
Pedersen JC, Berg K. Interaction between low density lipoprotein receptor (LDLR) and apolipoprotein E (apoE) alleles contributes to normal variation in lipid level. Clin Genet35:331–337, 1989.
55.
Utermann G. Apolipoprotein E polymorphism in health and disease. Am Heart J113:433–440, 1987.
56.
Sing CF, Davignon J. Role of the apolipoprotein E polymorphism in determining normal plasma lipid and lipoprotein variation. Am J Hum Genet37:268–285, 1985.
57.
Boerwinkle E, Utermann G. Simultaneous effects of the apolipoprotein E polymorphism, apolipoprotein B, and cholesterol metabolism. Am J Hum Genet42:104–112, 1988.
58.
Dallongeville J, Lussier-Cacan S, Davignon J. Modulation of plasma triglyceride levels by apoE phenotype: a meta-analysis. J Lipid Res33:447–454, 1992.
59.
Eto M, Watanabe K, Ishii K. Reciprocal effects of apolipoprotein E alleles (epsilon 2 and epsilon 4) on plasma lipid levels in normolipidemic subjects. Clin Genet29:477–484, 1986.
60.
Ordovas JM, Litwack-Klein L, Wilson PW, Schaefer MM, Schaefer EJ. Apolipoprotein E isoform phenotyping methodology and population frequency with identification of apoE1 and apoE5 isoforms. J Lipid Res28:371–380, 1987.
61.
Gregg RE, Zech LA, Schaefer EJ, Stark D, Wilson D, Brewer HB Jr. Abnormal in vivo metabolism of apolipoprotein E4 in humans. J Clin Invest78:815–821, 1986.
62.
Smit M, de Knijff P, Rosseneu M, Bury J, Klasen E, Frants R, Havekes L. Apolipoprotein E polymorphism in The Netherlands and its effect on plasma lipid and apolipoprotein levels. Hum Genet80:287–292, 1988.
63.
de Knijff P, Johansen LG, Rosseneu M, Frants RR, Jespersen J, Havekes LM. Lipoprotein profile of a Greenland Inuit population. Influence of anthropometric variables, Apo E and A4 polymorphism, and lifestyle. Arterioscler Thromb12:1371–1379, 1992.
64.
de Knijff P, Havekes LM. Apolipoprotein E as a risk factor for coronary heart disease: a genetic and molecular biology approach. Curr Opin Lipidol7:59–63, 1996.
