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Volume 40 Issue 7
Jul.  2013
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Article Contents

DNA Methylation, Behavior and Early Life Adversity

doi: 10.1016/j.jgg.2013.06.004
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  • Corresponding author: E-mail address: Moshe.szyf@mcgill.ca (Moshe Szyf)
  • Received Date: 2013-04-18
  • Accepted Date: 2013-06-19
  • Rev Recd Date: 2013-06-16
  • Available Online: 2013-06-25
  • Publish Date: 2013-07-20
  • The impact of early physical and social environments on life-long phenotypes is well known. Moreover, we have documented evidence for gene–environment interactions where identical gene variants are associated with different phenotypes that are dependent on early life adversity. What are the mechanisms that embed these early life experiences in the genome? DNA methylation is an enzymatically-catalyzed modification of DNA that serves as a mechanism by which similar sequences acquire cell type identity during cellular differentiation and embryogenesis in the same individual. The hypothesis that will be discussed here proposes that the same mechanism confers environmental-exposure specific identity upon DNA providing a mechanism for embedding environmental experiences in the genome, thus affecting long-term phenotypes. Particularly important is the environment early in life including both the prenatal and postnatal social environments.
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  • [1]
    Adams, R.L., Burdon, R.H., Gibb, S. et al. Biochim. Biophys. Acta, 655 (1981),pp. 329-334
    [2]
    Adams, R.L., McKay, E.L., Craig, L.M. et al. Mouse DNA methylase: methylation of native DNA Biochim. Biophys. Acta, 561 (1979),pp. 345-357
    [3]
    Angst, J., Gamma, A., Rossler, W. et al. Childhood adversity and chronicity of mood disorders Eur. Arch. Psychiatry Clin. Neurosci., 261 (2011),pp. 21-27
    [4]
    Bhattacharya, S.K., Ramchandani, S., Cervoni, N. et al. A mammalian protein with specific demethylase activity for mCpG DNA Nature, 397 (1999),pp. 579-583
    [5]
    Borghol, N., Suderman, M., McArdle, W. et al. Associations with early-life socio-economic position in adult DNA methylation Int. J. Epidemiol., 41 (2012),pp. 62-74
    [6]
    Caspi, A., Sugden, K., Moffitt, T.E. et al. Science, 301 (2003),pp. 386-389
    [7]
    Cervoni, N., Szyf, M. Demethylase activity is directed by histone acetylation J. Biol. Chem., 276 (2001),pp. 40778-40787
    [8]
    Chen, C.C., Wang, K.Y., Shen, C.K. DNA 5-methylcytosine demethylation activities of the mammalian DNA methyltransferases J. Biol. Chem., 288 (2013),pp. 9084-9091
    [9]
    Comb, M., Goodman, H.M. CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2 Nucleic Acids Res., 18 (1990),pp. 3975-3982
    [10]
    Corcoran, C.A., Pierre, P.J., Haddad, T. et al. Long-term effects of differential early rearing in rhesus macaques: behavioral reactivity in adulthood Dev. Psychobiol., 54 (2012),pp. 546-555
    [11]
    Crudo, A., Petropoulos, S., Moisiadis, V.G. et al. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects Endocrinology, 153 (2012),pp. 3269-3283
    [12]
    Crudo, A., Suderman, M., Moisiadis, V.G. et al. Glucocorticoid programming of the fetal male hippocampal epigenome Endocrinology, 154 (2013),pp. 1168-1180
    [13]
    Dolinoy, D.C., Huang, D., Jirtle, R.L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 13056-13061
    [14]
    Eden, S., Hashimshony, T., Keshet, I. et al. DNA methylation models histone acetylation Nature, 394 (1998),p. 842
    [15]
    Francis, D., Diorio, J., Liu, D. et al. Nongenomic transmission across generations of maternal behavior and stress responses in the rat Science, 286 (1999),pp. 1155-1158
    [16]
    Fuks, F., Hurd, P.J., Deplus, R. et al. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase Nucleic Acids Res., 31 (2003),pp. 2305-2312
    [17]
    Garrett, A.M., Weiner, J.A. Control of CNS synapse development by {gamma}-protocadherin-mediated astrocyte-neuron contact J. Neurosci., 29 (2009),pp. 11723-11731
    [18]
    Gruenbaum, Y., Cedar, H., Razin, A. Substrate and sequence specificity of a eukaryotic DNA methylase Nature, 295 (1982),pp. 620-622
    [19]
    Hazel, N.A., Hammen, C., Brennan, P.A. et al. Early childhood adversity and adolescent depression: the mediating role of continued stress Psychol. Med., 38 (2008),pp. 581-589
    [20]
    Hendrich, B., Guy, J., Ramsahoye, B. et al. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development Genes Dev., 15 (2001),pp. 710-723
    [21]
    Hertzman, C., Power, C., Matthews, S. et al. Using an interactive framework of society and lifecourse to explain self-rated health in early adulthood Soc. Sci. Med., 53 (2001),pp. 1575-1585
    [22]
    Hompes, T., Izzi, B., Gellens, E. et al. J. Psychiatr. Res., 47 (2013),pp. 880-891
    [23]
    Jost, J.P. Nuclear extracts of chicken embryos promote an active demethylation of DNA by excision repair of 5-methyldeoxycytidine Proc. Natl. Acad. Sci. USA, 90 (1993),pp. 4684-4688
    [24]
    Kangaspeska, S., Stride, B., Metivier, R. et al. Transient cyclical methylation of promoter DNA Nature, 452 (2008),pp. 112-115
    [25]
    Klengel, T., Mehta, D., Anacker, C. et al. Nat. Neurosci., 16 (2013),pp. 33-41
    [26]
    Kriaucionis, S., Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain Science, 324 (2009),pp. 929-930
    [27]
    Liberman, S.A., Mashoodh, R., Thompson, R.C. et al. Concordance in hippocampal and fecal Nr3c1 methylation is moderated by maternal behavior in the mouse Ecol. Evol., 2 (2012),pp. 3123-3131
    [28]
    Lister, R., Pelizzola, M., Dowen, R.H. et al. Human DNA methylomes at base resolution show widespread epigenomic differences Nature, 462 (2009),pp. 315-322
    [29]
    Maughan, B., McCarthy, G. Childhood adversities and psychosocial disorders Br. Med. Bull., 53 (1997),pp. 156-169
    [30]
    McGowan, P.O., Sasaki, A., D'Alessio, A.C. et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse Nat. Neurosci., 12 (2009),pp. 342-348
    [31]
    McGowan, P.O., Sasaki, A., Huang, T.C. et al. Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain PLoS ONE, 3 (2008),p. e2085
    [32]
    McGowan, P.O., Suderman, M., Sasaki, A. et al. Broad epigenetic signature of maternal care in the brain of adult rats PLoS ONE, 6 (2011),p. e14739
    [33]
    McLaughlin, K.A., Kubzansky, L.D., Dunn, E.C. et al. Childhood social environment, emotional reactivity to stress, and mood and anxiety disorders across the life course Depress Anxiety, 27 (2010),pp. 1087-1094
    [34]
    Meaney, M.J., Szyf, M. Maternal care as a model for experience-dependent chromatin plasticity? Trends Neurosci., 28 (2005),pp. 456-463
    [35]
    Miller, G.E., Chen, E., Fok, A.K. et al. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 14716-14721
    [36]
    Miller, K.E., Laszlo, K., Suomi, S.J. Am. J. Primatol., 70 (2008),pp. 119-126
    [37]
    Murgatroyd, C., Patchev, A.V., Wu, Y. et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress Nat. Neurosci., 12 (2009),pp. 1559-1566
    [38]
    Nan, X., Ng, H.H., Johnson, C.A. et al.
    [39]
    Ng, H.H., Zhang, Y., Hendrich, B. et al. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex Nat. Genet., 23 (1999),pp. 58-61
    [40]
    Oberlander, T.F., Weinberg, J., Papsdorf, M. et al. Epigenetics, 3 (2008),pp. 97-106
    [41]
    Power, C., Hertzman, C., Matthews, S. et al. Social differences in health: life-cycle effects between ages 23 and 33 in the 1958 British birth cohort Am. J. Public Health, 87 (1997),pp. 1499-1503
    [42]
    Power, C., Li, L., Hertzman, C. Associations of early growth and adult adiposity with patterns of salivary cortisol in adulthood J. Clin. Endocrinol. Metab., 91 (2006),pp. 4264-4270
    [43]
    Provencal, N., Suderman, M.J., Guillemin, C. et al. The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells J. Neurosci., 32 (2012),pp. 15626-15642
    [44]
    Raber, J., Sorg, O., Horn, T.F. et al. Inflammatory cytokines: putative regulators of neuronal and neuro-endocrine function Brain Res. Brain Res. Rev., 26 (1998),pp. 320-326
    [45]
    Ramchandani, S., Bhattacharya, S.K., Cervoni, N. et al. DNA methylation is a reversible biological signal Proc. Natl. Acad. Sci. USA, 96 (1999),pp. 6107-6112
    [46]
    Razin, A., Riggs, A.D. DNA methylation and gene function Science, 210 (1980),pp. 604-610
    [47]
    Razin, A., Szyf, M. DNA methylation patterns. Formation and function Biochim. Biophys. Acta, 782 (1984),pp. 331-342
    [48]
    Razin, A., Szyf, M., Kafri, T. et al. Replacement of 5-methylcytosine by cytosine: a possible mechanism for transient DNA demethylation during differentiation Proc. Natl. Acad. Sci. USA, 83 (1986),pp. 2827-2831
    [49]
    Ressler, K.J., Mercer, K.B., Bradley, B. et al. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor Nature, 470 (2011),pp. 492-497
    [50]
    Roth, T.L., Lubin, F.D., Funk, A.J. et al. Biol. Psychiatry, 65 (2009),pp. 760-769
    [51]
    Ruppenthal, G.C., Arling, G.L., Harlow, H.F. et al. A 10-year perspective of motherless-mother monkey behavior J. Abnorm. Psychol, 85 (1976),pp. 341-349
    [52]
    Stein, D.J., Scott, K., Haro Abad, J.M. et al. Early childhood adversity and later hypertension: data from the World Mental Health Survey Ann. Clin. Psychiatry, 22 (2010),pp. 19-28
    [53]
    Suderman, M., McGowan, P.O., Sasaki, A. et al. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 17266-17272
    [54]
    Suomi, S.J., Collins, M.L., Harlow, H.F. et al. Effects of maternal and peer separations on young monkeys J. Child. Psychol. Psychiatry, 17 (1976),pp. 101-112
    [55]
    Szyf, M. The early-life social environment and DNA methylation Clin. Genet., 81 (2012),pp. 341-349
    [56]
    Szyf, M. How do environments talk to genes? Nat. Neurosci., 16 (2013),pp. 2-4
    [57]
    Thomassin, H., Flavin, M., Espinas, M.L. et al. Glucocorticoid-induced DNA demethylation and gene memory during development EMBO J., 20 (2001),pp. 1974-1983
    [58]
    Tyrka, A.R., Price, L.H., Marsit, C. et al. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults PLoS ONE, 7 (2012),p. e30148
    [59]
    Uchida, S., Hara, K., Kobayashi, A. et al. Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents J. Neurosci., 30 (2010),pp. 15007-15018
    [60]
    Wang, D., Szyf, M., Benkelfat, C. et al. PLoS ONE, 7 (2012),p. e39501
    [61]
    Waterland, R.A., Jirtle, R.L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation Mol. Cell. Biol., 23 (2003),pp. 5293-5300
    [62]
    Weaver, I.C., Cervoni, N., Champagne, F.A. et al. Epigenetic programming by maternal behavior Nat. Neurosci., 7 (2004),pp. 847-854
    [63]
    Weaver, I.C., Champagne, F.A., Brown, S.E. et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life J. Neurosci., 25 (2005),pp. 11045-11054
    [64]
    Weaver, I.C., D'Alessio, A.C., Brown, S.E. et al. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes J. Neurosci., 27 (2007),pp. 1756-1768
    [65]
    Yirmiya, R., Goshen, I. Immune modulation of learning, memory, neural plasticity and neurogenesis Brain Behav. Immun., 25 (2011),pp. 181-213
    [66]
    Zalcman, S., Murray, L., Dyck, D.G. et al. Interleukin-2 and -6 induce behavioral-activating effects in mice Brain Res., 811 (1998),pp. 111-121
    [67]
    Zhou, Z., Hong, E.J., Cohen, S. et al. Neuron, 52 (2006),pp. 255-269
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