Epigenome-wide association studies (EWAS): Past, present, and future

Methods in Molecular Biology

Volumn 1238, Issue , 2015, Pages 51-63

  Flanagan, James M ^a  

^a NONE

Author keywords

Biomarker; Cancer; EWAS; Exposures; Methylation; Peripheral blood; Risk

Indexed keywords

DNA;

ARTICLE; BLOOD SAMPLING; CANCER GENETICS; CANCER RISK; DNA METHYLATION; EPIGENETICS; EPIGENOME WIDE ASSOCIATION STUDIES; GENETIC ASSOCIATION; GENETIC EPIDEMIOLOGY; GENETIC RISK; HUMAN; LEUKOCYTE; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL;

EID: 84921773545     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-1804-1_3     Document Type: Article

References (91)

1. Hindorff LA, MacArthur J, Morales J, Junkins HA, Hall PN, Klemm AK et al. A Catalog of Published Genome-Wide Association Studies. www.genome.gov/gwastudies. Accessed 9 Jan 2014
2. Michailidou K, Hall P, Gonzalez-Neira A, Ghoussaini M, Dennis J, Milne RL et al (2013) Large-scale genotyping identifi es 41 new loci associated with breast cancer risk. Nat Genet 45:353–361, 361 e351–352
3. Pharoah PD, Tsai YY, Ramus SJ, Phelan CM, Goode EL, Lawrenson K et al (2013) GWAS meta-analysis and replication identifies three new susceptibility loci for ovarian cancer. Nat Genet 45:362–370, 370 e361–362
4. Eeles RA, Olama AA, Benlloch S, Saunders EJ, Leongamornlert DA, Tymrakiewicz M et al (2013) Identification of 23 new prostate cancer susceptibility loci using the iCOGS custom genotyping array. Nat Genet 45:385–391, 391 e381–382
5. Issa JP (2000) The epigenetics of colorectal cancer. Ann N Y Acad Sci 910:140–153, discussion 153–155
6. Jablonka E, Lamb MJ (2002) The changing concept of epigenetics. Ann N Y Acad Sci 981:82–96
7. Michels KB (2010) The promises and challenges of epigenetic epidemiology. Exp Gerontol 45:297–301
8. Mill J, Heijmans BT (2013) From promises to practical strategies in epigenetic epidemiology. Nat Rev Genet 14:585–594
9. Relton CL, Davey Smith G (2010) Epigenetic epidemiology of common complex disease: prospects for prediction, prevention, and treatment. PLoS Med 7:e1000356
10. Vaiserman AM, Voitenko VP, Mekhova LV (2011) [Epigenetic epidemiology of agerelated diseases]. Ontogenez 42:30–50
11. Verma M, Rogers S, Divi RL, Schully SD, Nelson S, Joseph Su L, et al (2014) Epigenetic research in cancer epidemiology: trends, opportunities, and challenges. Cancer Epidemiol Biomarkers Prev 23:223–233
12. Waterland RA (2008) Epigenetic epidemiology of obesity: application of epigenomic technology. Nutr Rev 66(Suppl 1):S21–S23
13. Waterland RA, Michels KB (2007) Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr 27:363–388
14. Rakyan VK, Down TA, Balding DJ, Beck S (2011) Epigenome-wide association studies for common human diseases. Nat Rev Genet 12: 529–541
15. Patel CJ, Bhattacharya J, Butte AJ (2010) An Environment-Wide Association Study (EWAS) on type 2 diabetes mellitus. PLoS One 5: e10746
16. Bogdanos DP, Smyk DS, Invernizzi P, Rigopoulou EI, Blank M, Pouria S et al (2013) Infectome: a platform to trace infectious triggers of autoimmunity. Autoimmun Rev 12: 726–740
17. Rappaport SM (2012) Biomarkers intersect with the exposome. Biomarkers 17:483–489
18. Barnett C, Vanicek N, Polman R, Hancock A, Brown B, Smith L et al (2009) Kinematic gait adaptations in unilateral transtibial amputees during rehabilitation. Prosthet Orthot Int 33:135–147
19. Cui H, Cruz-Correa M, Giardiello FM, Hutcheon DF, Kafonek DR, Brandenburg S et al (2003) Loss of IGF2 imprinting: a potential marker of colorectal cancer risk. Science 299:1753–1755
20. Cui H, Onyango P, Brandenburg S, Wu Y, Hsieh CL, Feinberg AP (2002) Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF 2. Cancer Res 62:6442–6446
21. Cruz-Correa M, Cui H, Giardiello FM, Powe NR, Hylind L, Robinson A et al (2004) Loss of imprinting of insulin growth factor II gene: a potential heritable biomarker for colon neoplasia predisposition. Gastroenterology 126:964–970
22. Jirtle RL (2004) IGF2 loss of imprinting: a potential heritable risk factor for colorectal cancer. Gastroenterology 126:1190–1193
23. Ito Y, Koessler T, Ibrahim AE, Rai S, Vowler SL, Abu-Amero S et al (2008) Somatically acquired hypomethylation of IGF2 in breast and colorectal cancer. Hum Mol Genet 17:2633–2643
24. Chan TL, Yuen ST, Kong CK, Chan YW, Chan AS, Ng WF et al (2006) Heritable germline epimutation of MSH2 in a family with hereditary nonpolyposis colorectal cancer. Nat Genet 38:1178–1183
25. Suter CM, Martin DI, Ward RL (2004) Germline epimutation of MLH1 in individuals with multiple cancers. Nat Genet 36:497–501
26. Kwok CT, Vogelaar IP, van Zelst-Stams WA, Mensenkamp AR, Ligtenberg MJ, Rapkins RW, et al (2014) The MLH1 c.-27C>A and c.85G>T variants are linked to dominantly inherited MLH1 epimutation and are borne on a European ancestral haplotype. Eur J Hum Genet 22:617–624
27. Ligtenberg MJ, Kuiper RP, Chan TL, Goossens M, Hebeda KM, Voorendt M et al (2009) Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3' exons of TACSTD 1. Nat Genet 41:112–117
28. Brennan K, Garcia-Closas M, Orr N, Fletcher O, Jones M, Ashworth A et al (2012) Intragenic ATM methylation in peripheral blood DNA as a biomarker of breast cancer risk. Cancer Res 72:2304–2313
29. Widschwendter M, Apostolidou S, Raum E, Rothenbacher D, Fiegl H, Menon U et al (2008) Epigenotyping in peripheral blood cellDNA and breast cancer risk: a proof of principle study. PLoS One 3:e2656
30. Iwamoto T, Yamamoto N, Taguchi T, Tamaki Y, Noguchi S. (2011) BRCA1 promoter methylation in peripheral blood cells is associated with increased risk of breast cancer with BRCA1 promoter methylation. Breast Cancer Res Treat 129:69–77
31. Snell C, Krypuy M, Wong EM, Loughrey MB, Dobrovic A (2008) BRCA1 promoter methylation in peripheral blood DNA of mutation negative familial breast cancer patients with a BRCA1 tumour phenotype. Breast Cancer Res 10:R12
32. Wong EM, Southey MC, Fox SB, Brown MA, Dowty JG, Jenkins MA et al (2011) Constitutional methylation of the BRCA1 promoter is specifically associated with BRCA1 mutation-associated pathology in early-onset breast cancer. Cancer Prev Res (Phila) 4:23–33
33. Heijmans BT, Mill J (2012) Commentary: the seven plagues of epigenetic epidemiology. Int J Epidemiol 41:74–78
34. Michels KB, Binder AM, Dedeurwaerder S, Epstein CB, Greally JM, Gut I et al (2013) Recommendations for the design and analysis of epigenome-wide association studies. Nat Methods 10:949–955
35. Verma M (2012) Epigenome-Wide Association Studies (EWAS) in Cancer. Curr Genomics 13:308–313
36. Wilhelm-Benartzi CS, Koestler DC, Karagas MR, Flanagan JM, Christensen BC, Kelsey KT et al (2013) Review of processing and analysis methods for DNA methylation array data. Br J Cancer 109:1394–1402
37. Bell JT, Saffery R (2012) The value of twins in epigenetic epidemiology. Int J Epidemiol 41:140–150
38. Bock C (2012) Analysing and interpreting DNA methylation data. Nat Rev Genet 13:705–719
39. Jaffe AE, Murakami P, Lee H, Leek JT, Fallin MD, Feinberg AP et al (2012) Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol 41:200–209
40. Ng JW, Barrett LM, Wong A, Kuh D, Smith GD, Relton CL (2012) The role of longitudinal cohort studies in epigenetic epidemiology: challenges and opportunities. Genome Biol 13:246
41. Ong ML, Holbrook JD. (2014) Novel region discovery method for Infinium 450k DNA methylation data reveals changes associated with aging in muscle and neuronal pathways. Aging Cell 13:142–155
42. Ramagopalan SV, Rakyan VK (2013) The promise and challenges of blood spot methylomics. Epigenetics 8:775–777
43. Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G et al (2010) Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB J 24:3135–3144
44. Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D et al (2013) A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infi nium 450k DNA methylation data. Bioinformatics 29:189–196
45. Zhuang J, Widschwendter M, Teschendorff AE (2012) A comparison of feature selection and classifi cation methods in DNA methylation studies using the Illumina Infinium platform. BMC Bioinformatics 13:59
46. Lowe R, Gemma C, Beyan H, Hawa MI, Bazeos A, Leslie RD et al (2013) Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies. Epigenetics 8:445–454
47. Koestler DC, Christensen B, Karagas MR, Marsit CJ, Langevin SM, Kelsey KT et al (2013) Blood-based profiles of DNA methylation predict the underlying distribution of cell types: a validation analysis. Epigenetics 8:816–826
48. Koestler DC, Marsit CJ, Christensen BC, Accomando W, Langevin SM, Houseman EA et al (2012) Peripheral blood immune cell methylation profi les are associated with nonhematopoietic cancers. Cancer Epidemiol Biomarkers Prev 21:1293–1302
49. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlen SE, Greco D et al (2012) Differential DNA methylation in purifi ed human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One 7:e41361
50. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH et al (2012) DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 13:86
51. Liu Y, Aryee MJ, Padyukov L, Fallin MD, Hesselberg E, Runarsson A et al (2013) Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nat Biotechnol 31:142–147
52. Bjornsson HT, Sigurdsson MI, Fallin MD, Irizarry RA, Aspelund T, Cui H et al (2008) Intra-individual change over time in DNA methylation with familial clustering. JAMA 299:2877–2883
53. Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, Aspelund T et al (2010) Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci Transl Med 2:49ra67
54. Florath I, Butterbach K, Müller H, Bewerunge- Hudler M, Brenner H. (2014) Cross-sectional and longitudinal changes in DNA methylation with age: an epigenome-wide analysis revealing over 60 novel age-associated CpG sites. Hum Mol Genet 23:1186–1201
55. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML et al (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102: 10604–10609
56. Bell JT, Tsai PC, Yang TP, Pidsley R, Nisbet J, Glass D et al (2012) Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet 8:e1002629
57. Bell CG, Finer S, Lindgren CM, Wilson GA, Rakyan VK, Teschendorff AE et al (2010) Integrated genetic and epigenetic analysis identifi es haplotype-specific methylation in the FTO type 2 diabetes and obesity susceptibility locus. PLoS One 5:e14040
58. Schalkwyk LC, Meaburn EL, Smith R, Dempster EL, Jeffries AR, Davies MN et al (2010) Allelic skewing of DNA methylation is widespread across the genome. Am J Hum Genet 86:196–212
59. Hitchins MP, Rapkins RW, Kwok CT, Srivastava S, Wong JJ, Khachigian LM et al (2011) Dominantly inherited constitutional epigenetic silencing of MLH1 in a cancer-affected family is linked to a single nucleotide variant within the 5'UTR. Cancer Cell 20:200–213
60. Rakyan VK, Down TA, Maslau S, Andrew T, Yang TP, Beyan H et al (2010) Human agingassociated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res 20:434–439
61. Breitling LP, Yang R, Korn B, Burwinkel B, Brenner H (2011) Tobacco-smoking-related differential DNA methylation: 27k discovery and replication. Am J Hum Genet 88:450–457
62. Shenker NS, Polidoro S, van Veldhoven K, Sacerdote C, Ricceri F, Birrell MA et al (2013) Epigenome-wide association study in the European Prospective Investigation into Cancer and Nutrition (EPIC-Turin) identifi es novel genetic loci associated with smoking. Hum Mol Genet 22:843–851
63. Zhang Y, Yang R, Burwinkel B, Breitling LP, Brenner H. (2014) F2RL3 methylation as a biomarker of current and lifetime smoking exposures. Environ Health Perspect122:131–137
64. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Gayther SA, Apostolidou S et al (2009) An epigenetic signature in peripheral blood predicts active ovarian cancer. PLoS One 4:e8274
65. Marsit CJ, Koestler DC, Christensen BC, Karagas MR, Houseman EA, Kelsey KT (2011) DNA methylation array analysis identifi es profiles of blood-derived DNA methylation associated with bladder cancer. J Clin Oncol 29:1133–1139
66. Langevin SM, Koestler DC, Christensen BC, Butler RA, Wiencke JK, Nelson HH et al (2012) Peripheral blood DNA methylation profiles are indicative of head and neck squamous cell carcinoma: an epigenome-wide association study. Epigenetics 7:291–299
67. Xu Z, Bolick SC, DeRoo LA, Weinberg CR, Sandler DP, Taylor JA (2013) Epigenomewide association study of breast cancer using prospectively collected sister study samples. J Natl Cancer Inst 105:694–700
68. Garcia-Closas M, Gail MH, Kelsey KT, Ziegler RG (2013) Searching for blood DNA methylation markers of breast cancer risk and early detection. J Natl Cancer Inst 105:678–680
69. Brennan K, Flanagan JM (2012) Is there a link between genome-wide hypomethylation in blood and cancer risk? Cancer Prev Res (Phila) 5:1345–1357
70. Rakyan VK, Beyan H, Down TA, Hawa MI, Maslau S, Aden D et al (2011) Identifi cation of type 1 diabetes-associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet 7:e1002300
71. Hidalgo B, Irvin MR, Sha J, Zhi D, Aslibekyan S, Absher D, et al (2014) 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 63:801–807
72. Hosokawa M, Yoshikawa T, Negishi R, Yoshino T, Koh Y, Kenmotsu H et al (2013) Microcavity array system for size-based enrichment of circulating tumor cells from the blood of patients with small-cell lung cancer. Anal Chem 85: 5692–5698
73. Shenker NS, Ueland PM, Polidoro S, van Veldhoven K, Ricceri F, Brown R et al (2013) DNA methylation as a long-term biomarker of exposure to tobacco smoke. Epidemiology 24: 712–716
74. Philibert RA, Beach SR, Brody GH (2012) Demethylation of the aryl hydrocarbon receptor repressor as a biomarker for nascent smokers. Epigenetics 7:1331–1338
75. Joubert BR, Haberg SE, Nilsen RM, Wang X, Vollset SE, Murphy SK et al (2012) 450k epigenome- wide scan identifies differentialDNA methylation in newborns related to maternal smoking during pregnancy. Environ Health Perspect 120:1425–1431
76. Wan ES, Qiu W, Baccarelli A, Carey VJ, Bacherman H, Rennard SI et al (2012) Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome. Hum Mol Genet 21:3073–3082
77. Monick MM, Beach SR, Plume J, Sears R, Gerrard M, Brody GH et al (2012) Coordinated changes in AHRR methylation in lymphoblasts and pulmonary macrophages from smokers. Am J Med Genet B Neuropsychiatr Genet 159B:141–151
78. Philibert RA, Sears RA, Powers LS, Nash E, Bair T, Gerke AK et al (2012) Coordinated DNA methylation and gene expression changes in smoker alveolar macrophages: specifi c effects on VEGF receptor 1 expression. J Leukoc Biol 92:621–631
79. Haworth KE, Farrell WE, Emes RD, Ismail KM, Carroll WD, Borthwick HA et al (2013) Combined infl uence of gene-specifi c cord blood methylation and maternal smoking habit on birth weight. Epigenomics 5:37–49
80. Nishihara R, Morikawa T, Kuchiba A, Lochhead P, Yamauchi M, Liao X et al (2013) A prospective study of duration of smoking cessation and colorectal cancer risk by epigenetics- related tumor classifi cation. Am J Epidemiol 178:84–100
81. Philibert RA, Beach SR, Lei MK, Brody GH (2013) Changes in DNA methylation at the aryl hydrocarbon receptor repressor may be a new biomarker for smoking. Clin Epigenetics 5:19
82. Sun YV, Smith AK, Conneely KN, Chang Q, Li W, Lazarus A et al (2013) Epigenomic association analysis identifi es smoking-related DNA methylation sites in African Americans. Hum Genet 132:1027–1037
83. Zeilinger S, Kuhnel B, Klopp N, Baurecht H, Kleinschmidt A, Gieger C et al (2013) Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PLoS One 8:e63812
84. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H et al (2010) Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res 20:440–446
85. West J, Beck S, Wang X, Teschendorff AE (2013) An integrative network algorithm identifi es age-associated differential methylation interactome hotspots targeting stem-cell differentiation pathways. Sci Rep 3:1630
86. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S et al (2013) Genomewide methylation profi les reveal quantitative views of human aging rates. Mol Cell 49: 359–367
87. Heyn H, Carmona FJ, Gomez A, Ferreira HJ, Bell JT, Sayols S, et al (2013) DNA methylation profi ling in breast cancer discordant identical twins identifi es DOK7 as novel epigenetic biomarker. Carcinogenesis 34:102–108
88. Garagnani P, Bacalini MG, Pirazzini C, Gori D, Giuliani C, Mari D et al (2012) Methylation of ELOVL2 gene as a new epigenetic marker of age. Aging Cell 11:1132–1134
89. Esteller M (2011) Epigenetic changes in cancer. F1000 Biol Rep 3:9
90. Brennan K, Flanagan JM (2012) Epigenetic epidemiology for cancer risk: harnessing germline epigenetic variation. Methods Mol Biol 863:439–465
91. Beck S (2010) Taking the measure of the methylome. Nat Biotechnol 28:1026–1028