Identification of methylation quantitative trait loci (mQTLs) influencing promoter DNA methylation of alcohol dependence risk genes

Human Genetics

Volumn 133, Issue 9, 2014, Pages 1093-1104

  Zhang, Huiping ^a   Wang, Fan ^a   Kranzler, Henry R ^c   Yang, Can ^a,b   Xu, Hongqin ^a   Wang, Zuoheng ^b   Zhao, Hongyu ^a,b   Gelernter, Joel ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ALCOHOL DEHYDROGENASE 4; CAMP RESPONSIVE ELEMENT BINDING PROTEIN 1; COILED COIL DOMAIN CONTAINING 69; GANGLIOSIDE GM2 ACTIVATOR PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ALCOHOLISM; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC RISK; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; QUANTITATIVE TRAIT LOCUS; RACE; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

AFRICAN AMERICANS; ALCOHOLISM; CASE-CONTROL STUDIES; COMPUTATIONAL BIOLOGY; CPG ISLANDS; DNA METHYLATION; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC ASSOCIATION STUDIES; GENOTYPE; HUMANS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; QUANTITATIVE TRAIT LOCI; RISK FACTORS;

EID: 84907424835     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-014-1452-2     Document Type: Article

References (51)

1. Abdolmaleky HM, Cheng KH, Faraone SV, Wilcox M, Glatt SJ, Gao F, Smith CL, Shafa R, Aeali B, Carnevale J, Pan H, Papageorgis P, Ponte JF, Sivaraman V, Tsuang MT, Thiagalingam S (2006) Hypomethylation of MB-COMT promoter is a major risk factor for schizophrenia and bipolar disorder. Hum Mol Genet 15:3132–3145
2. American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders, 4th edn. Washington, DC
3. Baer C, Claus R, Frenzel LP, Zucknick M, Park YJ, Gu L, Weichenhan D, Fischer M, Pallasch CP, Herpel E, Rehli M, Byrd JC, Wendtner CM, Plass C (2012) Extensive promoter DNA hypermethylation and hypomethylation is associated with aberrant microRNA expression in chronic lymphocytic leukemia. Cancer Res 72:3775–3785
4. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF, Gilad Y, Pritchard JK (2011) DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol 12:R10
5. Boks MP, Derks EM, Weisenberger DJ, Strengman E, Janson E, Sommer IE, Kahn RS, Ophoff RA (2009) The relationship of DNA methylation with age, gender and genotype in twins and healthy controls. PLoS One 4:e6767
6. Chen Y, Ozturk NC, Zhou FC (2013) DNA methylation program in developing hippocampus and its alteration by alcohol. PLoS One 8:e60503
7. Dayem Ullah AZ, Lemoine NR, Chelala C (2012) SNPnexus: a web server for functional annotation of novel and publicly known genetic variants (2012 update). Nucleic Acids Res 40:W65–W70
8. de Rooij SR, Costello PM, Veenendaal MV, Lillycrop KA, Gluckman PD, Hanson MA, Painter RC, Roseboom TJ (2012) Associations between DNA methylation of a glucocorticoid receptor promoter and acute stress responses in a large healthy adult population are largely explained by lifestyle and educational differences. Psychoneuroendocrinology 37:782–788
9. Edenberg HJ, Xuei X, Chen HJ, Tian H, Wetherill LF, Dick DM, Almasy L, Bierut L, Bucholz KK, Goate A, Hesselbrock V, Kuperman S, Nurnberger J, Porjesz B, Rice J, Schuckit M, Tischfield J, Begleiter H, Foroud T (2006) Association of alcohol dehydrogenase genes with alcohol dependence: a comprehensive analysis. Hum Mol Genet 15:1539–1549
10. Egger G, Liang G, Aparicio A, Jones PA (2004) Epigenetics in human disease and prospects for epigenetic therapy. Nature 429:457–463
11. Etcheverry A, Aubry M, de Tayrac M, Vauleon E, Boniface R, Guenot F, Saikali S, Hamlat A, Riffaud L, Menei P, Quillien V, Mosser J (2010) DNA methylation in glioblastoma: impact on gene expression and clinical outcome. BMC Genome 11:701
12. Fraser HB, Lam LL, Neumann SM, Kobor MS (2012) Population-specificity of human DNA methylation. Genome Biol 13:R8
13. Gelernter J, Kranzler HR, Sherva R, Almasy L, Koesterer R, Smith AH, Anton R, Preuss UW, Ridinger M, Rujescu D, Wodarz N, Zill P, Zhao H, Farrer LA (2014) Genome-wide association study of alcohol dependence: significant findings in African- and European-Americans including novel risk loci. Mol Psychiatry 19:41–49
14. Gibbs JR, van der Brug MP, Hernandez DG, Traynor BJ, Nalls MA, Lai SL, Arepalli S, Dillman A, Rafferty IP, Troncoso J, Johnson R, Zielke HR, Ferrucci L, Longo DL, Cookson MR, Singleton AB (2010) Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet 6:e1000952
15. GTExConsortium (2013) The Genotype-Tissue Expression (GTEx) project. Nat Genet 45:580–585
16. Guo AY, Webb BT, Miles MF, Zimmerman MP, Kendler KS, Zhao Z (2009) ERGR: an ethanol-related gene resource. Nucleic Acids Res 37:D840–D845
17. Hodgkinson CA, Yuan Q, Xu K, Shen PH, Heinz E, Lobos EA, Binder EB, Cubells J, Ehlers CL, Gelernter J, Mann J, Riley B, Roy A, Tabakoff B, Todd RD, Zhou Z, Goldman D (2008) Addictions biology: haplotype-based analysis for 130 candidate genes on a single array. Alcohol Alcohol 43:505–515
18. Huang H, Chen Z, Huang X (2013) Age-adjusted nonparametric detection of differential DNA methylation with case-control designs. BMC Bioinform 14:86
19. Johnson WE, Li C, Rabinovic A (2007) Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8:118–127
20. Kerkel K, Spadola A, Yuan E, Kosek J, Jiang L, Hod E, Li K, Murty VV, Schupf N, Vilain E, Morris M, Haghighi F, Tycko B (2008) Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation. Nat Genet 40:904–908
21. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, Kobor MS (2012) Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci USA 109(Suppl 2):17253–17260
22. Lan X, Cretney EC, Kropp J, Khateeb K, Berg MA, Penagaricano F, Magness R, Radunz AE, Khatib H (2013) Maternal diet during pregnancy induces gene expression and DNA methylation changes in fetal tissues in sheep. Front Genet 4:49
23. Liu J, Morgan M, Hutchison K, Calhoun VD (2010) A study of the influence of sex on genome wide methylation. PLoS One 5:e10028
24. Luo X, Kranzler HR, Zuo L, Yang BZ, Lappalainen J, Gelernter J (2005) ADH4 gene variation is associated with alcohol and drug dependence: results from family controlled and population-structured association studies. Pharmacogenet Genomics 15:755–768
25. Moen EL, Zhang X, Mu W, Delaney SM, Wing C, McQuade J, Myers J, Godley LA, Dolan ME, Zhang W (2013) Genome-wide variation of cytosine modifications between European and African populations and the implications for complex traits. Genetics 194:987–996
26. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D, Holsboer F, Wotjak CT, Almeida OF, Spengler D (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12:1559–1566
27. Nicolae DL, Gamazon E, Zhang W, Duan S, Dolan ME, Cox NJ (2010) Trait-associated SNPs are more likely to be eQTLs: annotation to enhance discovery from GWAS. PLoS Genet 6:e1000888
28. Nielsen DA, Hamon S, Yuferov V, Jackson C, Ho A, Ott J, Kreek MJ (2010) Ethnic diversity of DNA methylation in the OPRM1 promoter region in lymphocytes of heroin addicts. Hum Genet 127:639–649
29. Numata S, Ye T, Hyde TM, Guitart-Navarro X, Tao R, Wininger M, Colantuoni C, Weinberger DR, Kleinman JE, Lipska BK (2012) DNA methylation signatures in development and aging of the human prefrontal cortex. Am J Hum Genet 90:260–272
30. Philibert RA, Plume JM, Gibbons FX, Brody GH, Beach SR (2012) The impact of recent alcohol use on genome wide DNA methylation signatures. Front Genet 3:54
31. Pierucci-Lagha A, Gelernter J, Feinn R, Cubells JF, Pearson D, Pollastri A, Farrer L, Kranzler HR (2005) Diagnostic reliability of the semi-structured assessment for drug dependence and alcoholism (SSADDA). Drug Alcohol Depend 80:303–312
32. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
33. Pruim RJ, Welch RP, Sanna S, Teslovich TM, Chines PS, Gliedt TP, Boehnke M, Abecasis GR, Willer CJ (2010) LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26:2336–2337
34. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575
35. Quon G, Lippert C, Heckerman D, Listgarten J (2013) Patterns of methylation heritability in a genome-wide analysis of four brain regions. Nucleic Acids Res 41:2095–2104
36. Schalkwyk LC, Meaburn EL, Smith R, Dempster EL, Jeffries AR, Davies MN, Plomin R, Mill J (2010) Allelic skewing of DNA methylation is widespread across the genome. Am J Hum Genet 86:196–212
37. Soubry A, Schildkraut JM, Murtha A, Wang F, Huang Z, Bernal A, Kurtzberg J, Jirtle RL, Murphy SK, Hoyo C (2013) Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort. BMC Med 11:29
38. Storey JD (2002) A direct approach to false discovery rates. J Royal Stat Soc Ser B (Statistical Methodology) 64:479–498
39. Supic G, Jagodic M, Magic Z (2013) Epigenetics: a new link between nutrition and cancer. Nutr Cancer 65:781–792
40. Tekpli X, Landvik NE, Anmarkud KH, Skaug V, Haugen A, Zienolddiny S (2013) DNA methylation at promoter regions of interleukin 1B, interleukin 6, and interleukin 8 in non-small cell lung cancer. Cancer Immunol Immunother 62:337–345
41. Tyrka AR, Price LH, Marsit C, Walters OC, Carpenter LL (2012) Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS One 7:e30148
42. Unternaehrer E, Luers P, Mill J, Dempster E, Meyer AH, Staehli S, Lieb R, Hellhammer DH, Meinlschmidt G (2012) Dynamic changes in DNA methylation of stress-associated genes (OXTR, BDNF) after acute psychosocial stress. Transl Psychiatry 2:e150
43. Woloszynska-Read A, James SR, Link PA, Yu J, Odunsi K, Karpf AR (2007) DNA methylation-dependent regulation of BORIS/CTCFL expression in ovarian cancer. Cancer Immun 7:21
44. Xie P, Kranzler HR, Poling J, Stein MB, Anton RF, Brady K, Weiss RD, Farrer L, Gelernter J (2009) Interactive effect of stressful life events and the serotonin transporter 5-HTTLPR genotype on posttraumatic stress disorder diagnosis in 2 independent populations. Arch Gen Psychiatry 66:1201–1209
45. Xu H, Wang F, Liu Y, Yu Y, Gelernter J, Zhang H (2014) Sex-biased methylome and transcriptome in human prefrontal cortex. Hum Mol Genet 23:1260–1270
46. Yang BZ, Zhang H, Ge W, Weder N, Douglas-Palumberi H, Perepletchikova F, Gelernter J, Kaufman J (2013) Child abuse and epigenetic mechanisms of disease risk. Am J Prev Med 44:101–107
47. Zhang D, Cheng L, Badner JA, Chen C, Chen Q, Luo W, Craig DW, Redman M, Gershon ES, Liu C (2010) Genetic control of individual differences in gene-specific methylation in human brain. Am J Hum Genet 86:411–419
48. Zhang FF, Cardarelli R, Carroll J, Fulda KG, Kaur M, Gonzalez K, Vishwanatha JK, Santella RM, Morabia A (2011) Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood. Epigenetics 6:623–629
49. Zhang H, Herman AI, Kranzler HR, Anton RF, Zhao H, Zheng W, Gelernter J (2013a) Array-based profiling of DNA methylation changes associated with alcohol dependence. Alcohol Clin Exp Res 37(Suppl 1):E108–E115
50. Zhang H, Wang F, Kranzler HR, Zhao H, Gelernter J (2013b) Profiling of childhood adversity-associated DNA methylation changes in alcoholic patients and healthy controls. PLoS One 8:e65648
51. Zhao Z, Webb BT, Jia P, Bigdeli TB, Maher BS, van den Oord E, Bergen SE, Amdur RL, O’Neill FA, Walsh D, Thiselton DL, Chen X, Pato CN, International Schizophrenia C, Riley BP, Kendler KS, Fanous AH (2013) Association study of 167 candidate genes for schizophrenia selected by a multi-domain evidence-based prioritization algorithm and neurodevelopmental hypothesis. PLoS One 8:e67776