Epipolymorphisms within lipoprotein genes contribute independently to plasma lipid levels in familial hypercholesterolemia

Epigenetics

Volumn 9, Issue 5, 2014, Pages 718-729

  Guay, Simon Pierre ^a,b   Brisson, Diane ^b,c   Lamarche, Benoit ^d   Gaudet, Daniel ^b,c   Bouchar, Luigi ^a,b  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b CHICOUTIMI HOSPITAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

Candidate genes; Coronary artery disease; DNA methylation; Missing heritability; Plasma lipid levels

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; CHOLESTEROL ESTER TRANSFER PROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIPOPROTEIN; LIPOPROTEIN LIPASE; LIVER TRIACYLGLYCEROL LIPASE; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; PHOSPHOLIPID TRANSFER PROTEIN; SCAVENGER RECEPTOR BI; STAT5 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1; UPSTREAM STIMULATORY FACTOR; ABC TRANSPORTER; ABCG1 PROTEIN, HUMAN; LIPH PROTEIN, HUMAN; PLTP PROTEIN, HUMAN; SCARB1 PROTEIN, HUMAN; SCAVENGER RECEPTOR B; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE;

ADULT; ARTICLE; BLOOD SAMPLING; CHOLESTEROL BLOOD LEVEL; CORONARY ARTERY DISEASE; CPG ISLAND; DNA METHYLATION; DNA POLYMORPHISM; DNA PURIFICATION; FAMILIAL HYPERCHOLESTEROLEMIA; FEMALE; GENE LOCUS; HUMAN; HUMAN CELL; LIPID BLOOD LEVEL; LIPOPROTEIN METABOLISM; MAJOR CLINICAL STUDY; MALE; REAL TIME POLYMERASE CHAIN REACTION; TRIACYLGLYCEROL BLOOD LEVEL; BLOOD; COMPLICATION; GENETIC EPIGENESIS; GENETIC POLYMORPHISM; GENETICS; MIDDLE AGED; SEX DIFFERENCE;

ADULT; ATP-BINDING CASSETTE TRANSPORTERS; CHOLESTEROL, HDL; CHOLESTEROL, LDL; CORONARY ARTERY DISEASE; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENETIC LOCI; HUMANS; HYPERLIPOPROTEINEMIA TYPE II; LIPASE; LIPOPROTEINS; MALE; MIDDLE AGED; PHOSPHOLIPID TRANSFER PROTEINS; POLYMORPHISM, GENETIC; SCAVENGER RECEPTORS, CLASS B; SEX FACTORS; TRIGLYCERIDES;

EID: 84899893593     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.27981     Document Type: Article

References (55)

1. Lamarche B, Després JP, Moorjani S, Cantin B, Dagenais GR, Lupien PJ.Triglycerides and HDLcholesterol as risk factors for ischemic heart disease.Results from the Québec cardiovascular study.Atherosclerosis 1996; 119:235-45.PMID:8808500; http://dx.doi.org/10.1016/0021-9150(95)05653-X.
2. Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, McQueen M, Budaj A, Pais P, Varigos J, et al.; INTERHEART Study Investigators.Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study.Lancet 2004; 364:937-52.PMID:15364185; http://dx.doi.org/10.1016/S0140-6736(04)17018-9.
3. Heller DA, de Faire U, Pedersen NL, Dahlén G, McClearn GE.Genetic and environmental influences on serum lipid levels in twins.N Engl J Med 1993; 328:1150-6.PMID:8455681; http://dx.doi.org/10.1056/NEJM199304223281603.
4. Almgren P, Lehtovirta M, Isomaa B, Sarelin L, Taskinen MR, Lyssenko V, Tuomi T, Groop L; Botnia Study Group.Heritability and familiality of type 2 diabetes and related quantitative traits in the Botnia Study.Diabetologia 2011; 54:2811-9.PMID:21826484; http://dx.doi.org/10.1007/s00125-011-2267-5.
5. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, Pirruccello JP, Ripatti S, Chasman DI, Willer CJ, et al.Biological, clinical and population relevance of 95 loci for blood lipids.Nature 2010; 466:707-13.PMID:20686565; http://dx.doi.org/10.1038/nature09270.
6. Asselbergs FW, Guo Y, van Iperen EP, Sivapalaratnam S, Tragante V, Lanktree MB, Lange LA, Almoguera B, Appelman YE, Barnard J, et al.; LifeLines Cohort Study.Large-scale gene-centric meta-analysis across 32 studies identifies multiple lipid loci.Am J Hum Genet 2012; 91:823-38.PMID:23063622; http://dx.doi.org/10.1016/j.ajhg.2012.08.032.
7. Eichler EE, Flint J, Gibson G, Kong A, Leal SM, Moore JH, Nadeau JH.Missing heritability and strategies for finding the underlying causes of complex disease.Nat Rev Genet 2010; 11:446-50.PMID:20479774; http://dx.doi.org/10.1038/nrg2809.
8. Henikoff S, Matzke MA.Exploring and explaining epigenetic effects.Trends Genet 1997; 13:293-5.PMID:9260513; http://dx.doi.org/10.1016/S0168-9525(97)01219-5.
9. Bird A.DNA methylation patterns and epigenetic memory.Genes Dev 2002; 16:6-21.PMID:11782440; http://dx.doi.org/10.1101/gad.947102.
10. Craig JM, Bickmore WA.The distribution of CpG islands in mammalian chromosomes.Nat Genet 1994; 7:376-82.PMID:7920655; http://dx.doi.org/10.1038/ng0794-376.
11. Baccarelli A, Wright R, Bollati V, Litonjua A, Zanobetti A, Tarantini L, Sparrow D, Vokonas P, Schwartz J.Ischemic heart disease and stroke in relation to blood DNA methylation.Epidemiology 2010; 21:819-28.PMID:20805753; http://dx.doi.org/10.1097/EDE.0b013e3181f20457.
12. Cash HL, McGarvey ST, Houseman EA, Marsit CJ, Hawley NL, Lambert-Messerlian GM, Viali S, Tuitele J, Kelsey KT.Cardiovascular disease risk factors and DNA methylation at the LINE-1 repeat region in peripheral blood from Samoan Islanders.Epigenetics 2011; 6:1257-64.PMID:21937883; http://dx.doi.org/10.4161/epi.6.10.17728.
13. Talens RP, Jukema JW, Trompet S, Kremer D, Westendorp RG, Lumey LH, Sattar N, Putter H, Slagboom PE, Heijmans BT; PROSPER Group.Hypermethylation at loci sensitive to the prenatal environment is associated with increased incidence of myocardial infarction.Int J Epidemiol 2012; 41:106-15.PMID:22101166; http://dx.doi.org/10.1093/ije/dyr153.
14. Pearce MS, McConnell JC, Potter C, Barrett LM, Parker L, Mathers JC, Relton CL.Global LINE-1 DNA methylation is associated with blood glycaemic and lipid profiles.Int J Epidemiol 2012; 41:210-7.PMID:22422454; http://dx.doi.org/10.1093/ije/dys020.
15. Zhang Y, Kent JW 2nd, Lee A, Cerjak D, Ali O, Diasio R, Olivier M, Blangero J, Carless MA, Kissebah AH.Fatty acid binding protein 3 (fabp3) is associated with insulin, lipids and cardiovascular phenotypes of the metabolic syndrome through epigenetic modifications in a Northern European family population.BMC Med Genomics 2013; 6:9.PMID:23510163; http://dx.doi.org/10.1186/1755-8794-6-9.
16. Guay SP, Brisson D, Munger J, Lamarche B, Gaudet D, Bouchard L.ABCA1 gene promoter DNA methylation is associated with HDL particle profile and coronary artery disease in familial hypercholesterolemia.Epigenetics 2012; 7:464-72.PMID:22419126; http://dx.doi.org/10.4161/epi.19633.
17. Guay SP, Brisson D, Lamarche B, Marceau P, Vohl MC, Gaudet D, Bouchard L.DNA methylation variations at CETP and LPL gene promoter loci: new molecular biomarkers associated with blood lipid profile variability.Atherosclerosis 2013; 228:413-20.PMID:23623643; http://dx.doi.org/10.1016/j.atherosclerosis.2013.03.033.
18. Out R, Hoekstra M, Habets K, Meurs I, de Waard V, Hildebrand RB, Wang Y, Chimini G, Kuiper J, Van Berkel TJ, et al.Combined deletion of macrophage ABCA1 and ABCG1 leads to massive lipid accumulation in tissue macrophages and distinct atherosclerosis at relatively low plasma cholesterol levels.Arterioscler Thromb Vasc Biol 2008; 28:258-64.PMID:18006857; http://dx.doi.org/10.1161/ATVBAHA.107.156935.
19. Connelly PW.The role of hepatic lipase in lipoprotein metabolism.Clin Chim Acta 1999; 286:243-55.PMID:10511296; http://dx.doi.org/10.1016/S0009-8981(99)00105-9.
20. Hegele RA, Vezina C, Moorjani S, Lupien PJ, Gagne C, Brun LD, Little JA, Connelly PW.A hepatic lipase gene mutation associated with heritable lipolytic deficiency.J Clin Endocrinol Metab 1991; 72:730-2.PMID:1671786; http://dx.doi.org/10.1210/jcem-72-3-730.
21. Brunzell JD, Zambon A, Deeb SS.The effect of hepatic lipase on coronary artery disease in humans is influenced by the underlying lipoprotein phenotype.Biochim Biophys Acta 2012; 1821:365-72.PMID:21986251; http://dx.doi.org/10.1016/j.bbalip.2011.09.008.
22. Cheung MC, Wolfbauer G, Albers JJ.Plasma phospholipid mass transfer rate: relationship to plasma phospholipid and cholesteryl ester transfer activities and lipid parameters.Biochim Biophys Acta 1996; 1303:103-10.PMID:8856039; http://dx.doi.org/10.1016/0005-2760(96)00082-3.
23. Edmondson AC, Braund PS, Stylianou IM, Khera AV, Nelson CP, Wolfe ML, Derohannessian SL, Keating BJ, Qu L, He J, et al.Dense genotyping of candidate gene loci identifies variants associated with high-density lipoprotein cholesterol.Circ Cardiovasc Genet 2011; 4:145-55.PMID:21303902; http://dx.doi.org/10.1161/CIRCGENETICS.110.957563.
24. Bell JT, Tsai PC, Yang TP, Pidsley R, Nisbet J, Glass D, Mangino M, Zhai G, Zhang F, Valdes A, et al.; MuTHER Consortium.Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population.PLoS Genet 2012; 8:e1002629.PMID:22532803; http://dx.doi.org/10.1371/journal.pgen.1002629.
25. Guay SP, Voisin G, Brisson D, Munger J, Lamarche B, Gaudet D, Bouchard L.Epigenome-wide analysis in familial hypercholesterolemia identified new loci associated with high-density lipoprotein cholesterol concentration.Epigenomics 2012; 4:623-39.PMID:23244308; http://dx.doi.org/10.2217/epi.12.62.
26. Xu Y, Wang W, Zhang L, Qi LP, Li LY, Chen LF, Fang Q, Dang AM, Yan XW.A polymorphism in the ABCG1 promoter is functionally associated with coronary artery disease in a Chinese Han population.Atherosclerosis 2011; 219:648-54.PMID:21722899; http://dx.doi.org/10.1016/j.atherosclerosis.2011.05.043.
27. Furuyama S, Uehara Y, Zhang B, Baba Y, Abe S, Iwamoto T, Miura S, Saku K.Genotypic Effect of ABCG1 gene promoter-257T>G polymorphism on coronary artery disease severity in Japanese men.J Atheroscler Thromb 2009; 16:194-200.PMID:19556716; http://dx.doi.org/10.5551/jat.E380.
28. Abellán R, Mansego ML, Martínez-Hervás S, Morcillo S, Pineda-Alonso M, Carmena R, Real JT, Redon J, Rojo-Martínez G, Martín-Escudero JC, et al.Dietary polyunsaturated fatty acids may increase plasma LDL-cholesterol and plasma cholesterol concentrations in carriers of an ABCG1 gene single nucleotide polymorphism: study in two Spanish populations.Atherosclerosis 2011; 219:900-6.PMID:21978921; http://dx.doi.org/10.1016/j.atherosclerosis.2011.09.018.
29. Olivier M, Tanck MW, Out R, Villard EF, Lammers B, Bouchareychas L, Frisdal E, Superville A, Van Berkel T, Kastelein JJ, et al.Human ATP-binding cassette G1 controls macrophage lipoprotein lipase bioavailability and promotes foam cell formation.Arterioscler Thromb Vasc Biol 2012; 32:2223-31.PMID:22772754; http://dx.doi.org/10.1161/ATVBAHA.111.243519.
30. Van Eck M, Zimmermann R, Groot PH, Zechner R, Van Berkel TJ.Role of macrophage-derived lipoprotein lipase in lipoprotein metabolism and atherosclerosis.Arterioscler Thromb Vasc Biol 2000; 20:E53-62.PMID:10978269; http://dx.doi.org/10.1161/01.ATV.20.9.e53.
31. Wilson K, Fry GL, Chappell DA, Sigmund CD, Medh JD.Macrophage-specific expression of human lipoprotein lipase accelerates atherosclerosis in transgenic apolipoprotein e knockout mice but not in C57BL/6 mice.Arterioscler Thromb Vasc Biol 2001; 21:1809-15.PMID:11701470; http://dx.doi.org/10.1161/hq1101.097805.
32. Albers JJ, Vuletic S, Cheung MC.Role of plasma phospholipid transfer protein in lipid and lipoprotein metabolism.Biochim Biophys Acta 2012; 1821:345-57.PMID:21736953; http://dx.doi.org/10.1016/j.bbalip.2011.06.013.
33. Kaess BM, Tomaszewski M, Braund PS, Stark K, Rafelt S, Fischer M, Hardwick R, Nelson CP, Debiec R, Huber F, et al.Large-scale candidate gene analysis of HDL particle features.PLoS One 2011; 6:e14529.PMID:21283740; http://dx.doi.org/10.1371/journal.pone.0014529.
34. Ayyappa KA, Ghosh S, Mohan V, Radha V.Association of hepatic lipase gene polymorphisms with hypertriglyceridemia and low high-density lipoprotein-cholesterol levels among South Indian subjects without diabetes.Diabetes Technol Ther 2013; 15:503-12.PMID:23550552; http://dx.doi.org/10.1089/dia.2012.0302.
35. Fang DZ, Liu BW.Polymorphism of HL +1075C, but not-480T, is associated with plasma high density lipoprotein cholesterol and apolipoprotein AI in men of a Chinese population.Atherosclerosis 2002; 161:417-24.PMID:11888526; http://dx.doi.org/10.1016/S0021-9150(01)00652-9.
36. Toperoff G, Aran D, Kark JD, Rosenberg M, Dubnikov T, Nissan B, Wainstein J, Friedlander Y, Levy-Lahad E, Glaser B, et al.Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood.Hum Mol Genet 2012; 21:371-83.PMID:21994764; http://dx.doi.org/10.1093/hmg/ddr472.
37. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al.Human DNA methylomes at base resolution show widespread epigenomic differences.Nature 2009; 462:315-22.PMID:19829295; http://dx.doi.org/10.1038/nature08514.
38. Peloso GM, Demissie S, Collins D, Mirel DB, Gabriel SB, Cupples LA, Robins SJ, Schaefer EJ, Brousseau ME.Common genetic variation in multiple metabolic pathways influences susceptibility to low HDL-cholesterol and coronary heart disease.J Lipid Res 2010; 51:3524-32.PMID:20855565; http://dx.doi.org/10.1194/jlr.P008268.
39. Willer CJ, Sanna S, Jackson AU, Scuteri A, Bonnycastle LL, Clarke R, Heath SC, Timpson NJ, Najjar SS, Stringham HM, et al.Newly identified loci that influence lipid concentrations and risk of coronary artery disease.Nat Genet 2008; 40:161-9.PMID:18193043; http://dx.doi.org/10.1038/ng.76.
40. Faggin E, Zambon A, Puato M, Deeb SS, Bertocco S, Sartore S, Crepaldi G, Pessina AC, Pauletto P.Association between the--514 C-->T polymorphism of the hepatic lipase gene promoter and unstable carotid plaque in patients with severe carotid artery stenosis.J Am Coll Cardiol 2002; 40:1059-66.PMID:12354428; http://dx.doi.org/10.1016/S0735-1097(02)02116-2.
41. Ghatreh Samani K, Noori M, Nobar MR, Chaleshtory MH, Farrokhi E, Amin MD.The-514C/T Polymorphism of Hepatic Lipase Gene among Iranian Patients with Coronary Heart Disease.Iran J Public Health 2012; 41:59-65.PMID:23113123.
42. Fan YM, Raitakari OT, Kähönen M, Hutri-Kähönen N, Juonala M, Marniemi J, Viikari J, Lehtimäki T.Hepatic lipase promoter C-480T polymorphism is associated with serum lipids levels, but not subclinical atherosclerosis: the Cardiovascular Risk in Young Finns Study.Clin Genet 2009; 76:46-53.PMID:19558527; http://dx.doi.org/10.1111/j.1399-0004.2009.01180.x
43. van Acker BA, Botma GJ, Zwinderman AH, Kuivenhoven JA, Dallinga-Thie GM, Sijbrands EJ, Boer JM, Seidell JC, Jukema JW, Kastelein JJ, et al.; REGRESS Study Group.High HDL cholesterol does not protect against coronary artery disease when associated with combined cholesteryl ester transfer protein and hepatic lipase gene variants.Atherosclerosis 2008; 200:161-7.PMID:18164013; http://dx.doi.org/10.1016/j.atherosclerosis.2007.11.019
44. Rufibach LE, Duncan SA, Battle M, Deeb SS.Transcriptional regulation of the human hepatic lipase (LIPC) gene promoter.J Lipid Res 2006; 47:1463-77.PMID:16603721; http://dx.doi.org/10.1194/jlr.M600082-JLR200
45. van Deursen D, Jansen H, Verhoeven AJ.Glucose increases hepatic lipase expression in HepG2 liver cells through upregulation of upstream stimulatory factors 1 and 2.Diabetologia 2008; 51:2078-87.PMID:18758746; http://dx.doi.org/10.1007/s00125-008-1125-6
46. van Deursen D, van Leeuwen M, Vaulont S, Jansen H, Verhoeven AJ.Upstream Stimulatory Factors 1 and 2 activate the human hepatic lipase promoter via E-box dependent and independent mechanisms.Biochim Biophys Acta 2009; 1791:229-37.PMID:19416648; http://dx.doi.org/10.1016/j.bbalip.2009.01.017.
47. Bélanger AS, Tojcic J, Harvey M, Guillemette C.Regulation of UGT1A1 and HNF1 transcription factor gene expression by DNA methylation in colon cancer cells.BMC Mol Biol 2010; 11:9.PMID:20096102; http://dx.doi.org/10.1186/1471-2199-11-9.
48. Rangel-Salazar R, Wickström-Lindholm M, Aguilar-Salinas CA, Alvarado-Caudillo Y, Døssing KB, Esteller M, Labourier E, Lund G, Nielsen FC, Rodríguez-Ríos D, et al.Human native lipoprotein-induced de novo DNA methylation is associated with repression of inflammatory genes in THP-1 macrophages.BMC Genomics 2011; 12:582.PMID:22118513; http://dx.doi.org/10.1186/1471-2164-12-582.
49. Chen KC, Liao YC, Hsieh IC, Wang YS, Hu CY, Juo SH.OxLDL causes both epigenetic modification and signaling regulation on the microRNA-29b gene: novel mechanisms for cardiovascular diseases.J Mol Cell Cardiol 2012; 52:587-95.PMID:22226905; http://dx.doi.org/10.1016/j.yjmcc.2011.12.005.
50. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlén SE, Greco D, Söderhäll C, Scheynius A, Kere J.Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility.PLoS One 2012; 7:e41361.PMID:22848472; http://dx.doi.org/10.1371/journal.pone.0041361.
51. Gaudet D, Arsenault S, Bélanger C, Hudson T, Perron P, Bernard M, Hamet P.Procedure to protect confidentiality of familial data in community genetics and genomic research.Clin Genet 1999; 55:259-64.PMID:10361987; http://dx.doi.org/10.1034/j.1399-0004.1999.550408.x.
52. Friedewald WT, Levy RI, Fredrickson DS.Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge.Clin Chem 1972; 18:499-502.PMID:4337382
53. Carrol ED, Salway F, Pepper SD, Saunders E, Mankhambo LA, Ollier WE, Hart CA, Day P.Successful downstream application of the Paxgene Blood RNA system from small blood samples in paediatric patients for quantitative PCR analysis.BMC Immunol 2007; 8:20.PMID:17850649; http://dx.doi.org/10.1186/1471-2172-8-20.
54. Spinsanti G, Zannolli R, Panti C, Ceccarelli I, Marsili L, Bachiocco V, Frati F, Aloisi AM.Quantitative Real-Time PCR detection of TRPV1-4 gene expression in human leukocytes from healthy and hyposensitive subjects.Mol Pain 2008; 4:51.PMID:18983665; http://dx.doi.org/10.1186/1744-8069-4-51
55. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T.MatInspector and beyond: promoter analysis based on transcription factor binding sites.Bioinformatics 2005; 21:2933-42.PMID:15860560; http://dx.doi.org/10.1093/bioinformatics/bti473