Childhood abuse is associated with methylation of multiple loci in adult DNA

BMC Medical Genomics

Volumn 7, Issue 1, 2014, Pages

  Suderman, Matthew ^a,b   Borghol, Nada ^a   Pappas, Jane J ^a   Pinto Pereira, Snehal M ^c   Pembrey, Marcus ^c   Hertzman, Clyde ^d   Power, Chris ^c   Szyf, Moshe ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Biomarker; Childhood abuse; DNA methylation; Early life environment; Epigenetics; Epigenome

Indexed keywords

METALLOPROTEINASE;

ADULT; ARTICLE; BLOOD SAMPLING; CHILD ABUSE; COHORT ANALYSIS; CONTROLLED STUDY; DNA METHYLATION; GENE; GENE REPLICATION; GENETIC ASSOCIATION; GENETIC REGULATION; HUMAN; IMMUNOPRECIPITATION; MALE; NUCLEOTIDE SEQUENCE; PM20D1 GENE; PRIORITY JOURNAL; PYROSEQUENCING; RISK ASSESSMENT; SIGNAL TRANSDUCTION; VALIDATION STUDY;

ADULT; BASE PAIRING; CHILD; CHILD ABUSE; CLUSTER ANALYSIS; CPG ISLANDS; DNA METHYLATION; GENETIC ASSOCIATION STUDIES; GENETIC LOCI; GENOME, HUMAN; HUMANS; MALE; MICRORNAS; PROMOTER REGIONS, GENETIC; REPRODUCIBILITY OF RESULTS; SOCIOECONOMIC FACTORS; WNT SIGNALING PATHWAY;

EID: 84901654790     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/1755-8794-7-13     Document Type: Article

References (65)

1. Burden and consequences of child maltreatment in high-income countries. Gilbert R, Widom CS, Browne K, Fergusson D, Webb E, Janson S, Lancet 2009 373 9657 68 81 10.1016/S0140-6736(08)61706-7 19056114
2. Adverse childhood experiences and smoking during adolescence and adulthood. Anda RF, Croft JB, Felitti VJ, Nordenberg D, Giles WH, Williamson DF, Giovino GA, JAMA 1999 282 17 1652 1658 10.1001/jama.282.17.1652 10553792
3. Adverse childhood experiences, alcoholic parents, and later risk of alcoholism and depression. Anda RF, Whitfield CL, Felitti VJ, Chapman D, Edwards VJ, Dube SR, Williamson DF, Psychiatr Serv 2002 53 8 1001 1009 12161676
4. Adverse childhood experiences and the association with ever using alcohol and initiating alcohol use during adolescence. Dube SR, Miller JW, Brown DW, Giles WH, Felitti VJ, Dong M, Anda RF, J Adolesc Health 2006 38 4 444 e441-410 16549308
5. Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) study. Felitti VJ, Anda RF, Nordenberg D, Williamson DF, Spitz AM, Edwards V, Koss MP, Marks JS, Am J Prev Med 1998 14 4 245 258 10.1016/S0749-3797(98)00017-8 9635069
6. Insights into causal pathways for ischemic heart disease: adverse childhood experiences study. Dong M, Giles WH, Felitti VJ, Dube SR, Williams JE, Chapman DP, Anda RF, Circulation 2004 110 13 1761 1766 10.1161/01.CIR. 0000143074.54995.7F 15381652
7. Relation of childhood socioeconomic status and family environment to adult metabolic functioning in the CARDIA study. Lehman BJ, Taylor SE, Kiefe CI, Seeman TE, Psychosom Med 2005 67 6 846 854 10.1097/01.psy.0000188443.48405.eb 16314588
8. Childhood adversities experienced by working-aged coronary heart disease patients. Sumanen M, Koskenvuo M, Sillanmaki L, Mattila K, J Psychosom Res 2005 59 5 331 335 10.1016/j.jpsychores.2005.04.005 16253624
9. Childhood abuse and early menarche: findings from the black women's health study. Wise LA, Palmer JR, Rothman EF, Rosenberg L, Am J Publ Health 2009 99 Suppl 2 460 S466
10. Childhood sexual abuse and early menarche: the direction of their relationship and its implications. Zabin LS, Emerson MR, Rowland DL, J Adolesc Health 2005 36 5 393 400 10.1016/j.jadohealth.2004.07.013 15837343
11. A life history assessment of early childhood sexual abuse in women. Vigil JM, Geary DC, Byrd-Craven J, Dev Psychol 2005 41 3 553 561 15910162
12. The association between childhood physical abuse and heart disease in adulthood: findings from a representative community sample. Fuller-Thomson E, Brennenstuhl S, Frank J, Child Abuse Negl 2010 34 9 689 698 10.1016/j.chiabu. 2010.02.005 20663556
13. Association between childhood trauma and physical disorders among adults in the United States. Goodwin RD, Stein MB, Psychol Med 2004 34 3 509 520 10.1017/S003329170300134X 15259836
14. Childhood physical abuse and midlife physical health: testing a multi-pathway life course model. Springer KW, Soc Sci Med 2009 69 1 138 146 10.1016/j.socscimed.2009.04.011 19446943
15. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Jaenisch R, Bird A, Nat Genet 2003 33 Suppl 245 254 12610534
16. Epigenetics and microRNAs. Chuang JC, Jones PA, Pediatr Res 2007 61 5 Pt 2 24R 29R 17413852
17. Extensive promoter DNA hypermethylation and hypomethylation is associated with aberrant microRNA expression in chronic lymphocytic leukemia. 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, Canc Res 2012 72 15 3775 3785 10.1158/0008-5472.CAN-12-0803
18. Prenatal famine and genetic variation are independently and additively associated with DNA methylation at regulatory loci within IGF2/H19. Tobi EW, Slagboom PE, van Dongen J, Kremer D, Stein AD, Putter H, Heijmans BT, Lumey LH, PloS One 2012 7 5 37933 10.1371/journal.pone.0037933 22666415
19. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonte B, Szyf M, Turecki G, Meaney MJ, Nat Neurosci 2009 12 3 342 348 10.1038/nn.2270 19234457
20. Lasting epigenetic influence of early-life adversity on the BDNF gene. Roth TL, Lubin FD, Funk AJ, Sweatt JD, Biol Psychiatr 2009 65 9 760 769 10.1016/j.biopsych.2008.11.028
21. Epigenetic programming by maternal behavior. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ, Nat Neurosci 2004 7 8 847 854 10.1038/nn1276 15220929
22. DNA methylation patterns. Formation and function. Razin A, Szyf M, Biochim Biophys Acta 1984 782 4 331 342 10.1016/0167-4781(84)90043-5 6383476
23. How do environments talk to genes? Szyf M, Nat Neurosci 2013 16 1 2 4 23257925
24. Associations with early-life socio-economic position in adult DNA methylation. Borghol N, Suderman M, McArdle W, Racine A, Hallett M, Pembrey M, Hertzman C, Power C, Szyf M, Int J Epidemiol 2012 41 1 62 74 10.1093/ije/dyr147 22422449
25. The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. Provencal N, Suderman MJ, Guillemin C, Massart R, Ruggiero A, Wang D, Bennett AJ, Pierre PJ, Friedman DP, Cote SM, Hallett M, Tremblay RE, Suomi SJ, Szyf M, J Neurosci Offic J Soc Neurosci 2012 32 44 15626 15642 10.1523/JNEUROSCI.1470-12.2012
26. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC, Pariante CM, Pace TW, Mercer KB, Mayberg HS, Bradley B, Nemeroff CB, Holsboer F, Heim CM, Ressler KJ, Rein T, Binder EB, Nat Neurosci 2013 16 1 33 41 23201972
27. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Mehta D, Klengel T, Conneely KN, Smith AK, Altmann A, Pace TW, Rex-Haffner M, Loeschner A, Gonik M, Mercer KB, Bradley B, Muller-Myhsok B, Ressler KJ, Binder EB, Proc Natl Acad Sci U S A 2013 110 20 8302 8307 10.1073/pnas.1217750110 23630272
28. Obesity and type 2 diabetes risk in midadult life: the role of childhood adversity. Thomas C, Hypponen E, Power C, Pediatrics 2008 121 5 1240 e1249 10.1542/peds.2007-2403 18450866
29. Cohort profile: 1958 British birth cohort (National Child Development Study). Power C, Elliott J, Int J Epidemiol 2006 35 1 34 41 16155052
30. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007 447 7145 661 678 10.1038/nature05911 17554300
31. Childhood adversity in an Australian population. Rosenman S, Rodgers B, Soc Psychiatry Psychiatr Epidemiol 2004 39 9 695 702 10.1007/s00127-004-0802-0 15672289
32. Limma: linear models for microarray data. Smyth GK, Bioinformatics and Computational Biology Solutions using R and Bioconductor, Volume 1 New York: Springer, Gentleman VC R, Dudoit S, Irizarry R, Huber W, 2005 397 420
33. Bioconductor: open software development for computational biology and bioinformatics. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J, Genome Biol 2004 5 10 80 10.1186/gb-2004-5-10- r80 15461798
34. Statistical discoveries and effect-size estimation. Soric B, J Am Stat Assoc 1989 84 406 608 610
35. Controlling the false discovery rate-a practical and powerful approach to multiple testing. Benjamini Y, Hochberg Y, J Roy Stat Soc B Met 1995 57 1 289 300
36. Gene ontology: tool for the unification of biology. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G, Nat Genet 2000 25 1 25 29 10.1038/75556 10802651
37. KEGG: kyoto encyclopedia of genes and genomes. Kanehisa M, Goto S, Nucleic Acids Res 2000 28 1 27 30 10.1093/nar/28.1.27 10592173
38. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP, Proc Natl Acad Sci USA 2005 102 43 15545 15550 10.1073/pnas.0506580102 16199517
39. Sensitive and quantitative universal Pyrosequencing methylation analysis of CpG sites. Colella S, Shen L, Baggerly KA, Issa JP, Krahe R, Biotechniques 2003 35 1 146 150 12866414
40. An integrated resource for genome-wide identification and analysis of human tissue-specific differentially methylated regions (tDMRs). Rakyan VK, Down TA, Thorne NP, Flicek P, Kulesha E, Graf S, Tomazou EM, Backdahl L, Johnson N, Herberth M, Howe KL, Jackson DK, Miretti MM, Fiegler H, Marioni JC, Birney E, Hubbard TJ, Carter NP, Tavare S, Beck S, Genome Res 2008 18 9 1518 1529 10.1101/gr.077479.108 18577705
41. A gene atlas of the mouse and human protein-encoding transcriptomes. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB, Proc Natl Acad Sci U S A 2004 101 16 6062 6067 10.1073/pnas.0400782101 15075390
42. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlen SE, Greco D, Soderhall C, Scheynius A, Kere J, PloS One 2012 7 7 41361 10.1371/journal.pone.0041361 22848472
43. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Lewis BP, Burge CB, Bartel DP, Cell 2005 120 1 15 20 10.1016/j.cell.2004.12.035 15652477
44. CpG-rich islands and the function of DNA methylation. Bird AP, Nature 1986 321 6067 209 213 10.1038/321209a0 2423876
45. CpG islands: features and distribution in the genomes of vertebrates. Aissani B, Bernardi G, Gene 1991 106 2 173 183 10.1016/0378-1119(91)90197-J 1937048
46. Comparison of methyl-DNA immunoprecipitation (MeDIP) and methyl-CpG binding domain (MBD) protein capture for genome-wide DNA methylation analysis reveal CpG sequence coverage bias. Nair SS, Coolen MW, Stirzaker C, Song JZ, Statham AL, Strbenac D, Robinson MW, Clark SJ, Epigenetics 2011 6 1 34 44 10.4161/epi.6.1.13313 20818161
47. Broad epigenetic signature of maternal care in the brain of adult rats. McGowan PO, Suderman M, Sasaki A, Huang TC, Hallett M, Meaney MJ, Szyf M, PloS One 2011 6 2 14739 10.1371/journal.pone.0014739 21386994
48. TCF/LEF factor earn their wings. Clevers H, van de Wetering M, Trends Genet 1997 13 12 485 489 10.1016/S0168-9525(97)01305-X 9433138
49. Medicine. Wnt fans the flames in obesity. Oh DY, Olefsky JM, Science 329 5990 397 398
50. Sfrp5 is an anti-inflammatory adipokine that modulates metabolic dysfunction in obesity. Ouchi N, Higuchi A, Ohashi K, Oshima Y, Gokce N, Shibata R, Akasaki Y, Shimono A, Walsh K, Science 2010 329 5990 454 457 10.1126/science.1188280 20558665
51. Wnt/beta-catenin signaling in adipogenesis and metabolism. Prestwich TC, Macdougald OA, Curr Opin Cell Biol 2007 19 6 612 617 10.1016/j.ceb.2007.09.014 17997088
52. Prime suspect: the TCF7L2 gene and type 2 diabetes risk. Hattersley AT, J Clin Invest 2007 117 8 2077 2079 10.1172/JCI33077 17671643
53. TCF7L2 genetic defect and type 2 diabetes. Cauchi S, Froguel P, Curr Diab Rep 2008 8 2 149 155 10.1007/s11892-008-0026-x 18445358
54. The WNT, signalling pathway and diabetes mellitus. Jin T, Diabetologia 2008 51 10 1771 1780 10.1007/s00125-008-1084-y 18696049
55. Wnt-signalling and the metabolic syndrome. Schinner S, Horm Metab Res 2009 41 2 159 163 10.1055/s-0028-1119408 19214925
56. The wnt pathway: a macrophage effector molecule that triggers inflammation. Pereira CP, Bachli EB, Schoedon G, Curr Atheroscler Rep 2009 11 3 236 242 10.1007/s11883-009-0036-4 19361356
57. The role of Wnt proteins in arthritis. Schett G, Zwerina J, David JP, Nat Clin Pract Rheumatol 2008 4 9 473 480 18756273
58. The Wnt/beta-catenin signaling pathway as a target in drug discovery. Takahashi-Yanaga F, Sasaguri T, J Pharmacol Sci 2007 104 4 293 302 10.1254/jphs.CR0070024 17721040
59. The control of beta-catenin and TCF during embryonic development and cancer. Waltzer L, Bienz M, Canc Metastasis Rev 1999 18 2 231 246
60. Personalized epigenomic signatures that are stable over time and covary with body mass index. Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, Aspelund T, Eiriksdottir G, Harris TB, Launer L, Gudnason V, Fallin MD, Sci Transl Med 2010 2 49 49ra67 20844285
61. Comprehensive high-throughput arrays for relative methylation (CHARM). Irizarry RA, Ladd-Acosta C, Carvalho B, Wu H, Brandenburg SA, Jeddeloh JA, Wen B, Feinberg AP, Genome Res 2008 18 5 780 790 10.1101/gr.7301508 18316654
62. Assessing the efficiency and significance of Methylated DNA Immunoprecipitation (MeDIP) assays in using in vitro methylated genomic DNA. Jia J, Pekowska A, Jaeger S, Benoukraf T, Ferrier P, Spicuglia S, BMC Res Notes 2010 3 240 10.1186/1756-0500-3-240 20846371
63. Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Jin SG, Kadam S, Pfeifer GP, Nucleic Acids Res 2010 38 11 125 10.1093/nar/gkq223 20371518
64. Assessment of methylation level prediction accuracy in methyl-DNA immunoprecipitation and sodium bisulfite based microarray platforms. Rajendram R, Ferreira JC, Grafodatskaya D, Choufani S, Chiang T, Pu S, Butcher DT, Wodak SJ, Weksberg R, Epigenetics 2011 6 4 410 415 10.4161/epi.6.4.14763 21343703
65. Evaluation of affinity-based genome-wide DNA methylation data: effects of CpG density, amplification bias, and copy number variation. Robinson MD, Stirzaker C, Statham AL, Coolen MW, Song JZ, Nair SS, Strbenac D, Speed TP, Clark SJ, Genome Res 2010 20 12 1719 1729 10.1101/gr.110601.110 21045081