DNA Methylation of Lipid-Related Genes Affects Blood Lipid Levels

Circulation: Cardiovascular Genetics

Volumn 8, Issue 2, 2015, Pages 334-342

  Pfeiffer, Liliane ^a,b   Wahl, Simone ^a,b,e   Pilling, Luke C ^f   Reischl, Eva ^a,b   Sandling, Johanna K ^g,v,w   Kunze, Sonja ^a,b   Holdt, Lesca M ^h   Kretschmer, Anja ^a,b,i   Schramm, Katharina ^c,j   Adamski, Jerzy ^d   Klopp, Norman ^k   Illig, Thomas ^k   Hedman, Åsa K ^l,v,x   Roden, Michael ^m,n   Hernandez, Dena G ^p   Singleton, Andrew B ^p   Thasler, Wolfgang E ^h   Grallert, Harald ^a,b,e   Gieger, Christian ^a   Herder, Christian ^m,n,o   Teupser, Daniel ^h   Meisinger, Christa ^b   Spector, Timothy D ^q   Kronenberg, Florian ^r   Prokisch, Holger ^c,j   Melzer, David ^f   Peters, Annette ^a,b,s   Deloukas, Panos ^g,t,u   Ferrucci, Luigi ^p   Waldenberger, Melanie ^a,b   more..

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Institute of Epidemiology II   (Germany)

^c Institute of Human Genetics   (Germany)

^d Institute of Experimental Genetics   (Germany)

^e GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^f UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

^g WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^h LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

ⁱ UNIVERSITY OF KIEL   (Germany)

^j TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^k HANNOVER MEDICAL SCHOOL   (Germany)

^l UNIVERSITY OF OXFORD   (United Kingdom)

^m LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

ⁿ HEINRICH HEINE UNIVERSITY   (Germany)

^o UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^p NATIONAL INSTITUTE ON AGING   (United States)

^q KING'S COLLEGE LONDON   (United Kingdom)

^r INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^s DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^t QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^u KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^v King Abdulaziz University ^*  (Sweden)

^w SCIENCE FOR LIFE LABORATORY   (Sweden)

^x UPPSALA UNIVERSITY   (Sweden)

more..

Author keywords

ABCG1; DNA methylatio; epidemiology; gene expression; myocardial infarction

Indexed keywords

ABC TRANSPORTER G1; C REACTIVE PROTEIN; CHOLESTEROL; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PROTEIN; PROTEIN MIR33B; PROTEIN SREBF1; PROTEIN TNIP1; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ABC TRANSPORTER; ABCG1 PROTEIN, HUMAN; LIPID; SREBF1 PROTEIN, HUMAN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ADIPOSE TISSUE; ADULT; AGED; ARTICLE; BLOOD SAMPLING; CHOLESTEROL BLOOD LEVEL; CPG ISLAND; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HEART INFARCTION; HUMAN; HUMAN CELL; HYPERTENSION; LIPID BLOOD LEVEL; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; TRIACYLGLYCEROL BLOOD LEVEL; BIOSYNTHESIS; BLOOD; CLINICAL TRIAL; COHORT ANALYSIS; GENE LOCUS; GENETIC EPIGENESIS; GENETICS; GERMANY; MIDDLE AGED; MULTICENTER STUDY; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ATP-BINDING CASSETTE TRANSPORTERS; COHORT STUDIES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENETIC LOCI; GERMANY; HUMANS; LIPIDS; MALE; MIDDLE AGED; MYOCARDIAL INFARCTION; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

EID: 84942908108     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.114.000804     Document Type: Article

References (44)

1. Andrawes WF, Bussy C, Belmin J. Prevention of cardiovascular events in elderly people. Drugs Aging. 2005;22:859-876.
2. Elder SJ, Lichtenstein AH, Pittas AG, Roberts SB, Fuss PJ, Greenberg AS, et al. Genetic and environmental influences on factors associated with cardiovascular disease and the metabolic syndrome. J Lipid Res. 2009;50:1917-1926. doi: 10.1194/jlr.P900033-JLR200.
3. Lichtenstein AH, Appel LJ, Brands M, Carnethon M, Daniels S, Franch HA, et al; American Heart Association Nutrition Committee. Diet and lifestyle recommendations revision 2006: a scientific statement from the American Heart Association Nutrition Committee. Circulation. 2006;114:82-96. doi: 10.1161/CIRCULATIONAHA.106.176158.
4. Willer CJ, Schmidt EM, Sengupta S, Peloso GM, Gustafsson S, Kanoni S, et al; Global Lipids Genetics Consortium. Discovery and refinement of loci associated with lipid levels. Nat Genet. 2013;45:1274-1283. doi: 10.1038/ng.2797.
5. Guay SP, Voisin G, Brisson D, Munger J, Lamarche B, Gaudet D, et al. Epigenome-wide analysis in familial hypercholesterolemia identified new loci associated with high-density lipoprotein cholesterol concentration. Epigenomics. 2012;4:623-639. doi: 10.2217/epi.12.62.
6. Irvin MR, Zhi D, Joehanes R, Mendelson M, Aslibekyan S, Claas SA, et al. Epigenome-wide association study of fasting blood lipids in the Genetics of Lipid-lowering Drugs and Diet Network study. Circulation. 2014;130:565-572. doi: 10.1161/CIRCULATIONAHA.114.009158.
7. Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics. 2013;29:189-196. doi: 10.1093/bioinformatics/bts680.
8. Pidsley R, Wong CCY, Volta M, Lunnon K, Mill J, Schalkwyk LC. A datadriven approach to preprocessing Illumina 450K methylation array data. BMC Genomics. 2013;14:293. doi: 10.1186/1471-2164-14-293.
9. Chen LS, Storey JD. Eigen-R2 for dissecting variation in high-dimensional studies. Bioinformatics. 2008;24:2260-2262. doi: 10.1093/bioinformatics/btn411.
10. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86. doi: 10.1186/1471-2105-13-86.
11. Edwards LJ, Muller KE, Wolfinger RD, Qaqish BF, Schabenberger O. An R2 statistic for fixed effects in the linear mixed model. Stat Med. 2008;27:6137-6157. doi: 10.1002/sim.3429.
12. Grundberg E, Meduri E, Sandling JK, Hedman AK, Keildson S, Buil A, et al; Multiple Tissue Human Expression Resource Consortium. Global analysis of DNA methylation variation in adipose tissue from twins reveals links to disease-associated variants in distal regulatory elements. Am J Hum Genet. 2013;93:876-890. doi: 10.1016/j.ajhg.2013.10.004.
13. Schurmann C, Heim K, Schillert A, Blankenberg S, Carstensen M, Dörr M, et al. Analyzing illumina gene expression microarray data from different tissues: methodological aspects of data analysis in the metaxpress consortium. PLoS One. 2012;7:e50938. doi: 10.1371/journal.pone.0050938.
14. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlén SE, Greco D, et al. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One. 2012;7:e41361. doi: 10.1371/journal.pone.0041361.
15. Moen EL, Zhang X, Mu W, Delaney SM, Wing C, McQuade J, et al. Genome-wide variation of cytosine modifications between European and African populations and the implications for complex traits. Genetics. 2013;194:987-996. doi: 10.1534/genetics.113.151381.
16. Edwards PA, Tabor D, Kast HR, Venkateswaran A. Regulation of gene expression by SREBP and SCAP. Biochim Biophys Acta. 2000;1529:103-113.
17. Horton JD. Sterol regulatory element-binding proteins: transcriptional activators of lipid synthesis. Biochem Soc Trans. 2002;30(Part 6):1091-1095.
18. Marquart TJ, Allen RM, Ory DS, Baldán A. miR-33 links SREBP-2 induction to repression of sterol transporters. Proc Natl Acad Sci USA. 2010;107:12228-12232. doi: 10.1073/pnas.1005191107.
19. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, et al. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science. 2010;328:1566-1569. doi: 10.1126/science.1189123.
20. Rayner KJ, Suárez Y, Dávalos A, Parathath S, Fitzgerald ML, Tamehiro N, et al. MiR-33 contributes to the regulation of cholesterol homeostasis. Science. 2010;328:1570-1573. doi: 10.1126/science.1189862.
21. Dávalos A, Goedeke L, Smibert P, Ramírez CM, Warrier NP, Andreo U, et al. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci USA. 2011;108:9232-9237. doi: 10.1073/pnas.1102281108.
22. Gerin I, Clerbaux LA, Haumont O, Lanthier N, Das AK, Burant CF, et al. Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J Biol Chem. 2010;285:33652-33661. doi: 10.1074/jbc.M110.152090.
23. Horie T, Ono K, Horiguchi M, Nishi H, Nakamura T, Nagao K, et al. MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo. Proc Natl Acad Sci USA. 2010;107:17321-17326. doi: 10.1073/pnas.1008499107.
24. McGarry JD, Brown NF. The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem. 1997;244:1-14.
25. Rotllan N, Fernández-Hernando C. MicroRNA regulation of cholesterol metabolism. Cholesterol. 2012;2012:847849. doi: 10.1155/2012/847849.
26. Gelissen IC, Harris M, Rye KA, Quinn C, Brown AJ, Kockx M, et al. ABCA1 and ABCG1 synergize to mediate cholesterol export to apoAI. Arterioscler Thromb Vasc Biol. 2006;26:534-540. doi: 10.1161/01. ATV.0000200082.58536.e1.
27. Wang N, Lan D, Chen W, Matsuura F, Tall AR. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc Natl Acad Sci USA. 2004;101:9774-9779. doi: 10.1073/pnas.0403506101.
28. Kennedy MA, Barrera GC, Nakamura K, Baldán A, Tarr P, Fishbein MC, et al. ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell Metab. 2005;1:121-131. doi: 10.1016/j.cmet.2005.01.002.
29. Tarling EJ, Edwards PA. ATP binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter. Proc Natl Acad Sci USA. 2011;108:19719-19724. doi: 10.1073/pnas.1113021108.
30. Tarling EJ, Edwards PA. Dancing with the sterols: critical roles for ABCG1, ABCA1, miRNAs, and nuclear and cell surface receptors in controlling cellular sterol homeostasis. Biochim Biophys Acta. 2012;1821:386-395. doi: 10.1016/j.bbalip.2011.07.011.
31. Ramasamy I. Recent advances in physiological lipoprotein metabolism. Clin Chem Lab Med. 2014;52:1695-1727.
32. Olivier M, Tanck MW, Out R, Villard EF, Lammers B, Bouchareychas L, et al. Human ATP-binding cassette G1 controls macrophage lipoprotein lipase bioavailability and promotes foam cell formation. Arterioscler Thromb Vasc Biol. 2012;32:2223-2231. doi: 10.1161/ATVBAHA.111.243519.
33. Flores AM, Gurevich I, Zhang C, Ramirez VP, Devens TR, Aneskievich BJ. TNIP1 is a corepressor of agonist-bound PPARs. Arch Biochem Biophys. 2011;516:58-66. doi: 10.1016/j.abb.2011.08.014.
34. Gurevich I, Aneskievich BJ. Liganded RARalpha and RARgamma interact with but are repressed by TNIP1. Biochem Biophys Res Commun. 2009;389:409-414. doi: 10.1016/j.bbrc.2009.08.159.
35. Ayaori M, Yakushiji E, Ogura M, Nakaya K, Hisada T, Uto-Kondo H, et al. Retinoic acid receptor agonists regulate expression of ATPbinding cassette transporter G1 in macrophages. Biochim Biophys Acta. 2012;1821:561-572. doi: 10.1016/j.bbalip.2012.02.004.
36. Chinetti G, Lestavel S, Bocher V, Remaley AT, Neve B, Torra IP, et al. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat Med. 2001;7:53-58. doi: 10.1038/83348.
37. Li AC, Binder CJ, Gutierrez A, Brown KK, Plotkin CR, Pattison JW, et al. Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPARalpha, beta/delta, and gamma. J Clin Invest. 2004;114:1564-1576. doi: 10.1172/JCI18730.
38. Mauldin JP, Nagelin MH, Wojcik AJ, Srinivasan S, Skaflen MD, Ayers CR, et al. Reduced expression of ATP-binding cassette transporter G1 increases cholesterol accumulation in macrophages of patients with type 2 diabetes mellitus. Circulation. 2008;117:2785-2792. doi: 10.1161/CIRCULATIONAHA.107.741314.
39. Hidalgo B, Irvin MR, Sha J, Zhi D, Aslibekyan S, Absher D, et al. Epigenome-wide association study of fasting measures of glucose, insulin, and HOMA-IR in the Genetics of Lipid Lowering Drugs and Diet Network study. Diabetes. 2014;63:801-807. doi: 10.2337/db13-1100.
40. Wierda RJ, Geutskens SB, Jukema JW, Quax PH, van den Elsen PJ. Epigenetics in atherosclerosis and inflammation. J Cell Mol Med. 2010;14:1225-1240. doi: 10.1111/j.1582-4934.2010.01022.x.
41. 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;7:464-472. doi: 10.4161/epi.19633.
42. Xu Y, Wang W, Zhang L, Qi LP, Li LY, Chen LF, et al. A polymorphism in the ABCG1 promoter is functionally associated with coronary artery disease in a Chinese Han population. Atherosclerosis. 2011;219:648-654. doi: 10.1016/j.atherosclerosis.2011.05.043.
43. Schou J, Frikke-Schmidt R, Kardassis D, Thymiakou E, Nordestgaard BG, Jensen G, et al. Genetic variation in ABCG1 and risk of myocardial infarction and ischemic heart disease. Arterioscler Thromb Vasc Biol. 2012;32:506-515. doi: 10.1161/ATVBAHA.111.234872.
44. Wong BX, Kyle RA, Croft KD, Quinn CM, Jessup W, Yeap BB. Modulation of macrophage fatty acid content and composition by exposure to dyslipidemic serum in vitro. Lipids. 2011;46:371-380. doi: 10.1007/s11745-011-3528-2.