Investigating epigenetic consequences of early-life adversity: some methodological considerations

References

• Aberg K.A. , Xie L.Y. , McClay J.L. , Nerella S. , Vunck S. , Snider S. , Van den Oord E.J . Testing two models describing how methylome-wide studies in blood are informative for psychiatric conditions. Epigenomics. 2013; 5(4): 367–377.
   Google Scholar
• Beach S.R. , Brody G.H. , Todorov A.A. , Gunter T.D. , Philibert R.A . Methylation at SLC6A4 is linked to family history of child abuse: An examination of the Iowa Adoptee sample. American Journal of Medical Genetics Part B Neuropsychiatric Genetics. 2010; 153B(2): 710–713.
   Google Scholar
• Bernstein D.P. , Fink L. , Handelsman L. , Foote J. , Lovejoy M. , Wenzel K. , Ruggiero J . Initial reliability and validity of a new retrospective measure of child abuse and neglect. American Journal of Psychiatry. 1994; 151(8): 1132–1136.
   Google Scholar
• Bifulco A. , Brown G.W. , Harris T.O . Childhood experience of care and abuse (CECA): A retrospective interview measure. Journal of Child Psychology and Psychiatry. 1994; 35(8): 1419–1435.
   Google Scholar
• Brent D.A., Melhem N.M., Oquendo M., Burke A., Birmaher B., Stanley B., Mann J.J. Familial pathways to early-onset suicide attempt: A 5.6-year prospective study. JAMA Psychiatry. 2015; 72(2): 160–168. doi: http://dx.doi.org/10.1001/jamapsychiatry.2014.2141.
   Google Scholar
• Brezo J., Paris J., Barker E.D., Tremblay R., Vitaro F., Zoccolillo M., Turecki G. Natural history of suicidal behaviors in a population-based sample of young adults. Psychological Medicine. 2007; 37(11): 1563–1574. doi: http://dx.doi.org/10.1017/S003329170700058X.
   Google Scholar
• Caspi A., Moffitt T.E. Gene-environment interactions in psychiatry: Joining forces with neuroscience. Nature Reviews Neuroscience. 2006; 7(7): 583–590. doi: http://dx.doi.org/10.1038/nrn1925.
   Google Scholar
• Davies M.N. , Volta M. , Pidsley R. , Lunnon K. , Dixit A. , Lovestone S. , Mill J . Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biology. 2012; 13(6): R43.
   Google Scholar
• Davis E.P., Pfaff D. Sexually dimorphic responses to early adversity: Implications for affective problems and autism spectrum disorder. Psychoneuroendocrinology. 2014; 49: 11–25. doi: http://dx.doi.org/10.1016/j.psyneuen.2014.06.014.
   Google Scholar
• Fergusson D.M. , Woodward L.J. , Horwood L.J . Risk factors and life processes associated with the onset of suicidal behaviour during adolescence and early adulthood. Psychological Medicine. 2000; 30(1): 23–39.
   Google Scholar
• Gaunt T.R., Shihab H.A., Hemani G., Min J.L., Woodward G., Lyttleton O., Relton C.L. Systematic identification of genetic influences on methylation across the human life course. Genome Biology. 2016; 17(1): 61. doi: http://dx.doi.org/10.1186/s13059-016-0926-z.
   Google Scholar
• Gilbert R., Widom C.S., Browne K., Fergusson D., Webb E., Janson S. Burden and consequences of child maltreatment in high-income countries. The Lancet. 2009; 373(9657): 68–81. doi: http://dx.doi.org/10.1016/S0140-6736(08)61706-7.
   Google Scholar
• Guintivano J., Aryee M.J., Kaminsky Z.A. A cell epigenotype specific model for the correction of brain cellular heterogeneity bias and its application to age, brain region and major depression. Epigenetics. 2013; 8(3): 290–302. doi: http://dx.doi.org/10.4161/epi.23924.
   Google Scholar
• Guintivano J., Kaminsky Z.A. Role of epigenetic factors in the development of mental illness throughout life. Neuroscience Research. 2016; 102: 56–66. doi: http://dx.doi.org/10.1016/j.neures.2014.08.003.
   Google Scholar
• Guo J.U., Su Y., Shin J.H., Shin J., Li H., Xie B., Song H. Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nature Neuroscience. 2014; 17(2): 215–222. doi: http://dx.doi.org/10.1038/nn.3607.
   Google Scholar
• Hannon E., Lunnon K., Schalkwyk L., Mill J. Interindividual methylomic variation across blood, cortex, and cerebellum: Implications for epigenetic studies of neurological and neuropsychiatric phenotypes. Epigenetics. 2015; 10(11): 1024–1032. doi: http://dx.doi.org/10.1080/15592294.2015.1100786.
   Google Scholar
• Hardt J. , Rutter M . Validity of adult retrospective reports of adverse childhood experiences: Review of the evidence. Journal of Child Psychology and Psychiatry. 2004; 45(2): 260–273.
   Google Scholar
• Heim C.M., Binder E.B. Current research trends in early life stress and depression: Review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Experimental Neurology. 2012; 233(1): 102–111. doi: http://dx.doi.org/10.1016/j.expneurol.2011.10.032.
   Google Scholar
• Heim C.M., Mayberg H.S., Mletzko T., Nemeroff C.B., Pruessner J.C. Decreased cortical representation of genital somatosensory field after childhood sexual abuse. The American Journal of Psychiatry. 2013; 170(6): 616–623. doi: http://dx.doi.org/10.1176/appi.ajp.2013.12070950.
   Google Scholar
• Heim C.M., Shugart M., Craighead W.E., Nemeroff C.B. Neurobiological and psychiatric consequences of child abuse and neglect. Developmental Psychobiology. 2010; 52(7): 671–690. doi: http://dx.doi.org/10.1002/dev.20494.
   Google Scholar
• Houseman E.A., Accomando W.P., Koestler D.C., Christensen B.C., Marsit C.J., Nelson H.H., Kelsey K.T. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012; 13: 86. doi: http://dx.doi.org/10.1186/1471-2105-13-86.
   Google Scholar
• Jawahar M.C., Murgatroyd C., Harrison E.L., Baune B.T. Epigenetic alterations following early postnatal stress: A review on novel aetiological mechanisms of common psychiatric disorders. Clinical Epigenetics. 2015; 7: 122. doi: http://dx.doi.org/10.1186/s13148-015-0156-3.
   Google Scholar
• Khulan B., Manning J.R., Dunbar D.R., Seckl J.R., Raikkonen K., Eriksson J.G., Drake A.J. Epigenomic profiling of men exposed to early-life stress reveals DNA methylation differences in association with current mental state. Translational Psychiatry. 2014; 4: e448. doi: http://dx.doi.org/10.1038/tp.2014.94.
   Google Scholar
• Klengel T., Mehta D., Anacker C., Rex-Haffner M., Pruessner J.C., Pariante C.M., Binder E.B. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nature Neuroscience. 2013; 16(1): 33–41. doi: http://dx.doi.org/10.1038/nn.3275.
   Google Scholar
• Klose R.J. , Bird A.P . Genomic DNA methylation: The mark and its mediators. Trends in Biochemical Sciences. 2006; 31(2): 89–97.
   Google Scholar
• Kozlenkov A., Roussos P., Timashpolsky A., Barbu M., Rudchenko S., Bibikova M., Dracheva S. Differences in DNA methylation between human neuronal and glial cells are concentrated in enhancers and non-CpG sites. Nucleic Acids Research. 2014; 42(1): 109–127. doi: http://dx.doi.org/10.1093/nar/gkt838.
   Google Scholar
• Kundakovic M., Lim S., Gudsnuk K., Champagne F.A. Sex-specific and strain-dependent effects of early life adversity on behavioral and epigenetic outcomes. Frontiers in Psychiatry. 2013; 4: 78. doi: http://dx.doi.org/10.3389/fpsyt.2013.00078.
   Google Scholar
• Labonte B., Suderman M., Maussion G., Navaro L., Yerko V., Mahar I., Turecki G. Genome-wide epigenetic regulation by early-life trauma. Archives of General Psychiatry. 2012; 69(7): 722–731. doi: http://dx.doi.org/10.1001/archgenpsychiatry.2011.2287.
   Google Scholar
• Labonte B., Yerko V., Gross J., Mechawar N., Meaney M.J., Szyf M., Turecki G. Differential glucocorticoid receptor exon 1(B), 1(C), and 1(H) expression and methylation in suicide completers with a history of childhood abuse. Biological Psychiatry. 2012; 72(1): 41–8. doi: http://dx.doi.org/10.1016/j.biopsych.2012.01.034.
   Google Scholar
• Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., Ecker J.R. Global epigenomic reconfiguration during mammalian brain development. Science. 2013; 341(6146): 1237905. doi: http://dx.doi.org/10.1126/science.1237905.
   Google Scholar
• Lopez-Castroman J., Jaussent I., Beziat S., Genty C., Olie E., De Leon-Martinez V., Guillaume S. Suicidal phenotypes associated with family history of suicidal behavior and early traumatic experiences. Journal of Affective Disorders. 2012; 142(1–3): 193–199. doi: http://dx.doi.org/10.1016/j.jad.2012.04.025.
   Google Scholar
• Lopez-Castroman J., Melhem N., Birmaher B., Greenhill L., Kolko D., Stanley B., Oquendo M.A. Early childhood sexual abuse increases suicidal intent. World Psychiatry. 2013; 12(2): 149–154. doi: http://dx.doi.org/10.1002/wps.20039.
   Google Scholar
• Lunnon K., Hannon E., Smith R.G., Dempster E., Wong C., Burrage J., Mill J. Variation in 5-hydroxymethylcytosine across human cortex and cerebellum. Genome Biology. 2016; 17(1): 27. doi: http://dx.doi.org/10.1186/s13059-016-0871-x.
   Google Scholar
• Lutz P.E. , Almeida D. , Fiori L.M. , Turecki G . Childhood maltreatment and stress-related psychopathology: The epigenetic memory hypothesis. Current Pharmaceutical Design. 2015; 21(11): 1413–1417.
   Google Scholar
• Massart R., Suderman M., Provencal N., Yi C., Bennett A.J., Suomi S., Szyf M. Hydroxymethylation and DNA methylation profiles in the prefrontal cortex of the non-human primate rhesus macaque and the impact of maternal deprivation on hydroxymethylation. Neuroscience. 2014; 268: 139–148. doi: http://dx.doi.org/10.1016/j.neuroscience.2014.03.021.
   Google Scholar
• McGirr A., Alda M., Seguin M., Cabot S., Lesage A., Turecki G. Familial aggregation of suicide explained by cluster B traits: A three-group family study of suicide controlling for major depressive disorder. American Journal of Psychiatry. 2009; 166(10): 1124–1134. doi: http://dx.doi.org/10.1176/appi.ajp.2009.08111744.
   Google Scholar
• McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience. 2009; 12(3): 342–348. doi: http://dx.doi.org/10.1038/nn.2270.
   Google Scholar
• McLaughlin K.A. , Green J.G. , Gruber M.J. , Sampson N.A. , Zaslavsky A.M. , Kessler R.C . Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: Associations with persistence of DSM-IV disorders. Archives of General Psychiatry. 2010; 67(2): 124–132.
   Google Scholar
• Melas P.A., Wei Y., Wong C.C., Sjoholm L.K., Aberg E., Mill J., Lavebratt C. Genetic and epigenetic associations of MAOA and NR3C1 with depression and childhood adversities. International Journal of Neuropsychopharmacology. 2013; 16(7): 1513–1528. doi: http://dx.doi.org/10.1017/S1461145713000102.
   Google Scholar
• Mellen M., Ayata P., Dewell S., Kriaucionis S., Heintz N. MeCP2 Binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell. 2012; 151(7): 1417–1430. doi: http://dx.doi.org/10.1016/j.cell.2012.11.022.
   Google Scholar
• Mill J., Heijmans B.T. From promises to practical strategies in epigenetic epidemiology. Nature Reviews Genetics. 2013; 14(8): 585–594. doi: http://dx.doi.org/10.1038/nrg3405.
   Google Scholar
• Monk C., Spicer J., Champagne F.A. Linking prenatal maternal adversity to developmental outcomes in infants: The role of epigenetic pathways. Development and Psychopathology. 2012; 24(4): 1361–1376. doi: http://dx.doi.org/10.1017/S0954579412000764.
   Google Scholar
• Moussavi S. , Chatterji S. , Verdes E. , Tandon A. , Patel V. , Ustun B . Depression, chronic diseases, and decrements in health: Results from the world health surveys. The Lancet. 2007; 370(9590): 851–858.
   Google Scholar
• Perroud N., Paoloni-Giacobino A., Prada P., Olie E., Salzmann A., Nicastro R., Malafosse A. Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: A link with the severity and type of trauma. Translational Psychiatry. 2011; 1: e59. doi: http://dx.doi.org/10.1038/tp.2011.60.
   Google Scholar
• Perroud N., Salzmann A., Prada P., Nicastro R., Hoeppli M.E., Furrer S., Malafosse A. Response to psychotherapy in borderline personality disorder and methylation status of the BDNF gene. Translational Psychiatry. 2013; 3: e207. doi: http://dx.doi.org/10.1038/tp.2012.140.
   Google Scholar
• Plongthongkum N., Diep D.H., Zhang K. Advances in the profiling of DNA modifications: Cytosine methylation and beyond. Nature Reviews Genetics. 2014; 15(10): 647–661. doi: http://dx.doi.org/10.1038/nrg3772.
   Google Scholar
• Prados J., Stenz L., Courtet P., Prada P., Nicastro R., Adouan W., Perroud N. Borderline personality disorder and childhood maltreatment: A genome-wide methylation analysis. Genes Brain and Behavior. 2015; 14(2): 177–188. doi: http://dx.doi.org/10.1111/gbb.12197.
   Google Scholar
• Rhein M., Hagemeier L., Klintschar M., Muschler M., Bleich S., Frieling H. DNA methylation results depend on DNA integrity-role of post mortem interval. Frontiers in Genetics. 2015; 6: 182. doi: http://dx.doi.org/10.3389/fgene.2015.00182.
   Google Scholar
• Roadmap Epigenomics Consortium, Kundaje A., Meuleman W., Ernst J., Bilenky M., Yen A., Kellis M. Integrative analysis of 111 reference human epigenomes. Nature. 2015; 518(7539): 317–330. doi: http://dx.doi.org/10.1038/nature14248.
   Google Scholar
• Schultz M.D., He Y., Whitaker J.W., Hariharan M., Mukamel E.A., Leung D., Ecker J.R. Human body epigenome maps reveal noncanonical DNA methylation variation. Nature. 2015; 523(7559): 212–216. doi: http://dx.doi.org/10.1038/nature14465.
   Google Scholar
• Suderman M. , Borghol N. , Pappas J.J. , Pinto Pereira S.M. , Pembrey M. , Hertzman C. , Szyf M . Childhood abuse is associated with methylation of multiple loci in adult DNA. BMC Medical Genomics. 2014; 7: 13.
   Google Scholar
• Suderman M., McGowan P.O., Sasaki A., Huang T.C., Hallett M.T., Meaney M.J., Szyf M. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(Suppl. 2): 17266–17272. doi: http://dx.doi.org/10.1073/pnas.1121260109.
   Google Scholar
• Suderman M., Pappas J.J., Borghol N., Buxton J.L., McArdle W.L., Ring S.M., Pembrey M. Lymphoblastoid cell lines reveal associations of adult DNA methylation with childhood and current adversity that are distinct from whole blood associations. International Journal of Epidemiology. 2015; 44(4): 1331–1340. doi: http://dx.doi.org/10.1093/ije/dyv168.
   Google Scholar
• Thaler L. , Gauvin L. , Joober R. , Groleau P. , De Guzman R. , Ambalavanan A. , Steiger H . Methylation of BDNF in women with bulimic eating syndromes: Associations with childhood abuse and borderline personality disorder. Progress in Neuropsychopharmacology Biological Psychiatry. 2014; 54: 43–59.
   Google Scholar
• Tsankova N. , Renthal W. , Kumar A. , Nestler E.J . Epigenetic regulation in psychiatric disorders. Nature Reviews Neuroscience. 2007; 8(5): 355–367.
   Google Scholar
• Turecki G. The molecular bases of the suicidal brain. Nature Reviews Neuroscience. 2014; 15(12): 802–816. doi: http://dx.doi.org/10.1038/nrn3839.
   Google Scholar
• Turecki G., Brent D.A. Suicide and suicidal behaviour. The Lancet. 2015; 387(10024): 1227–1239. doi: http://dx.doi.org/10.1016/S0140-6736(15)00234-2.
   Google Scholar
• Turecki G., Meaney M.J. Effects of the social environment and stress on glucocorticoid receptor gene methylation: A systematic review. Biological Psychiatry. 2014; 79(2): 87–96. doi: http://dx.doi.org/10.1016/j.biopsych.2014.11.022.
   Google Scholar
• Turecki G., Ota V.K., Belangero S.I., Jackowski A., Kaufman J. Early life adversity, genomic plasticity, and psychopathology. Lancet Psychiatry. 2014; 1(6): 461–466. doi: http://dx.doi.org/10.1016/S2215-0366(14)00022-4.
   Google Scholar
• Tylee D.S., Kawaguchi D.M., Glatt S.J. On the outside, looking in: A review and evaluation of the comparability of blood and brain “-omes”. American Journal of Medical Genetics Part B Neuropsychiatric Genetics. 2013; 162B(7): 595–603. doi: http://dx.doi.org/10.1002/ajmg.b.32150.
   Google Scholar
• Tyrka A.R., Ridout K.K., Parade S.H., Paquette A., Marsit C.J., Seifer R. Childhood maltreatment and methylation of FK506 binding protein 5 gene (FKBP5). Development and Psychopathology. 2015; 27 (4 Pt 2): 1637–1645. doi: http://dx.doi.org/10.1017/S0954579415000991.
   Google Scholar
• Van Der Knaap L.J., Riese H., Hudziak J.J., Verbiest M.M., Verhulst F.C., Oldehinkel A.J., Van Oort F.V. Adverse life events and allele-specific methylation of the serotonin transporter gene (SLC6A4) in adolescents: The TRAILS study. Psychosomatic Medicine. 2015; 77(3): 246–255. doi: http://dx.doi.org/10.1097/PSY.0000000000000159.
   Google Scholar
• Walton E., Hass J., Liu J., Roffman J.L., Bernardoni F., Roessner V., Ehrlich S. Correspondence of DNA methylation between blood and brain tissue and its application to schizophrenia research. Schizophrenia Bulletin. 2015; 42(2): 406–414. doi: http://dx.doi.org/10.1093/schbul/sbv074.
   Google Scholar
• Wang D. , Szyf M. , Benkelfat C. , Provencal N. , Turecki G. , Caramaschi D. , Booij L . Peripheral SLC6A4 DNA methylation is associated with in vivo measures of human brain serotonin synthesis and childhood physical aggression. PLoS One. 2012; 7(6): e39501.
   Google Scholar
• Wankerl M., Miller R., Kirschbaum C., Hennig J., Stalder T., Alexander N. Effects of genetic and early environmental risk factors for depression on serotonin transporter expression and methylation profiles. Translational Psychiatry. 2014; 4: e402. doi: http://dx.doi.org/10.1038/tp.2014.37.
   Google Scholar
• Wanner B., Vitaro F., Tremblay R.E., Turecki G. Childhood trajectories of anxiousness and disruptiveness explain the association between early-life adversity and attempted suicide. Psychological Medicine. 2012; 42(11): 2373–2382. doi: http://dx.doi.org/10.1017/S0033291712000438.
   Google Scholar
• Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Meaney M.J. Epigenetic programming by maternal behavior. Nature Neuroscience. 2004; 7(8): 847–854. doi: http://dx.doi.org/10.1038/nn1276.
   Google Scholar
• Weber M., Davies J.J., Wittig D., Oakeley E.J., Haase M., Lam W.L., Schubeler D. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nature Genetics. 2005; 37(8): 853–862. doi: http://dx.doi.org/10.1038/ng1598.
   Google Scholar
• Xin Y., Chanrion B., Liu M.M., Galfalvy H., Costa R., Ilievski B., Haghighi F. Genome-wide divergence of DNA methylation marks in cerebral and cerebellar cortices. PLoS One. 2010; 5(6): e11357. doi: http://dx.doi.org/10.1371/journal.pone.0011357.
   Google Scholar
• Yehuda R., Daskalakis N.P., Bierer L.M., Bader H.N., Klengel T., Holsboer F., Binder E.B. Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biological Psychiatry. 2015; 80(5): 372–380. doi: http://dx.doi.org/10.1016/j.biopsych.2015.08.005.
   Google Scholar
• Zhang H. , Wang F. , Kranzler H.R. , Zhao H. , Gelernter J . Profiling of childhood adversity-associated DNA methylation changes in alcoholic patients and healthy controls. PLoS One. 2013; 8(6): e65648.
   Google Scholar
• Ziller M.J., Gu H., Muller F., Donaghey J., Tsai L.T., Kohlbacher O., Meissner A. Charting a dynamic DNA methylation landscape of the human genome. Nature. 2013; 500(7463): 477–481. doi: http://dx.doi.org/10.1038/nature12433.
   Google Scholar