1932

Abstract

The field of social and behavioral epigenetics examines the role of epigenetic modifications to mediate the effect of psychosocial stressors on an individual's health and well-being. Epigenetic modifications influence gene expression, which can lead to changes in an individual's phenotype. DNA methylation is an important epigenetic modification that varies throughout the lifespan and appears to respond to a wide range of psychosocial and biological stressors. The effects of early-life adversity impact future health and may be passed on to future generations. The underlying model proposes that stress influences health via an epigenetic mechanism involving altered DNA methylation and gene expression. This review summarizes a range of studies that have identified DNA methylation at specific genes and throughout the genome in association with multiple psychosocial stressors, including psychiatric disorders, sexual and physical abuse, and war trauma. Future studies should test a comprehensive list of epigenetic modifications in association with psychosocial stressors and multiple health outcomes.

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2016-10-21
2024-06-22
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Literature Cited

  1. Andreano JM, Cahill L. 2006. Glucocorticoid release and memory consolidation in men and women. Psychol. Sci. 17:466–70 [Google Scholar]
  2. Barker DJ. 1990. The fetal and infant origins of adult disease. BMJ 301:1111 [Google Scholar]
  3. Barker DJP, Lampl M, Roseboom T, Winder N. 2012. Resource allocation in utero and health in later life. Placenta 33:Suppl. 2e30–34 [Google Scholar]
  4. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B. et al. 2004. Developmental plasticity and human health. Nature 430:419–21 [Google Scholar]
  5. Benyshek DC. 2013. The “early life” origins of obesity-related health disorders: new discoveries regarding the intergenerational transmission of developmentally programmed traits in the global cardiometabolic health crisis. Am. J. Phys. Anthropol. 152:79–93 [Google Scholar]
  6. Black MC, Basile KC, Breiding MJ, Smith SG, Walters ML. et al. 2010. The National Intimate Partner and Sexual Violence Survey (NISVS): 2010 Summary Report Atlanta, GA: Natl. Cent. Injury Prev. Control, Cent. Dis. Control Prev. [Google Scholar]
  7. Boas F. 1912. Changes in Bodily Form of Descendants of Immigrants New York: Columbia Univ. Press573 [Google Scholar]
  8. Borghol N, Suderman M, McArdle W, Racine A, Hallett M. et al. 2012. Associations with early-life socio-economic position in adult DNA methylation. Int. J. Epidemiol. 41:62–74 [Google Scholar]
  9. Boulter AC, Quinlan JA, Miró-Herrans AT, Pearson LN, Todd NL. et al. 2015. Interaction of Alu polymorphisms and novel measures of discrimination in association with blood pressure in African Americans living in Tallahassee. Hum. Biol. 87:4291–301 [Google Scholar]
  10. Braithwaite EC, Kundakovic M, Ramchandani PG, Murphy SE, Champagne FA. 2015. Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation. Epigenetics 10:408–17 [Google Scholar]
  11. Brix J, Zhou Y, Luo Y. 2015. The epigenetic reprogramming roadmap in generation of iPSCs from somatic cells. J. Genet. Genom. 42:661–70 [Google Scholar]
  12. Cao-Lei L, Massart R, Suderman MJ, Machnes Z, Elgbeili G. et al. 2014. DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: Project Ice Storm. PLOS ONE 9:e107653 [Google Scholar]
  13. Chang L, Wang Y, Ji H, Dai D, Xu X. et al. 2014. Elevation of peripheral BDNF Promoter Methylation Links to the Risk of Alzheimer's Disease. PLOS ONE 9:e110773 [Google Scholar]
  14. Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H. 2012. Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 39:112–19 [Google Scholar]
  15. Choi JD, Lee J-S. 2013. Interplay between epigenetics and genetics in cancer. Genom. Inf. 11:164–73 [Google Scholar]
  16. Clukay CJ, Hughes DA, Rodney NC, Kertes DA, Mulligan CJ. 2016. An epigenetic investigation of methylation complex genes in relation to stress in mother-newborn dyads. Am. J. Phys. Anthropol. Suppl 62:118 [Google Scholar]
  17. Cottrell EC, Seckl JR. 2009. Prenatal stress, glucocorticoids and the programming of adult disease. Front. Behav. Neurosci. 3:19 [Google Scholar]
  18. Davis EP, Sandman CA. 2010. The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev. 81:131–48 [Google Scholar]
  19. Drake AJ, Liu L. 2010. Intergenerational transmission of programmed effects: public health consequences. Trends Endocrinol. Metab. 21:206–13 [Google Scholar]
  20. Essex MJ, Boyce WT, Hertzman C, Lam LL, Armstrong JM. et al. 2011. Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence. Child Dev. 84:58–75 [Google Scholar]
  21. Esteller M. 2007. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8:286–98 [Google Scholar]
  22. Fisher HL, Murphy TM, Arseneault L, Caspi A, Moffitt TE. et al. 2015. Methylomic analysis of monozygotic twins discordant for childhood psychotic symptoms. Epigenetics 10:1014–23 [Google Scholar]
  23. Freel EM, Ingram M, Wallace AM, White A, Fraser R. et al. 2008. Effect of variation in CYP11B1 and CYP11B2 on corticosteroid phenotype and hypothalamic–pituitary–adrenal axis activity in hypertensive and normotensive subjects. Clin. Endocrinol. 68:700–6 [Google Scholar]
  24. Frisancho AR. 1993. Human Adaptation and Accommodation Ann Arbor: Univ. Mich. Press [Google Scholar]
  25. Fuchikami M, Morinobu S, Segawa M, Okamoto Y, Yamawaki S. et al. 2011. DNA methylation profiles of the brain-derived neurotrophic factor (BDNF) gene as a potent diagnostic biomarker in major depression. PLOS ONE 6:e23881 [Google Scholar]
  26. Gassen NC, Fries GR, Zannas AS, Hartmann J, Zschocke J. et al. 2015. Chaperoning epigenetics: FKBP51 decreases the activity of DNMT1 and mediates epigenetic effects of the antidepressant paroxetine. Sci. Signal. 8:ra119 [Google Scholar]
  27. Geronimus AT, Hicken M, Keene D, Bound J. 2006. “Weathering” and age patterns of allostatic load scores among blacks and whites in the United States. Am. J. Public Health 96:826–33 [Google Scholar]
  28. Gluckman PD, Hanson MA. 2006. The developmental origins of health and disease: the breadth and importance of the concept. Early Life Origins of Health and Disease EM Wintour, JA Owens 1–17 New York: Springer [Google Scholar]
  29. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. 2008. Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359:61–73 [Google Scholar]
  30. Gunnar M, Quevedo K. 2007. The neurobiology of stress and development. Annu. Rev. Psychol. 58:145–73 [Google Scholar]
  31. Handel AE, Ebers GC, Ramagopalan SV. 2009. Epigenetics: molecular mechanisms and implications for disease. Trends Mol. Med. 16:7–16 [Google Scholar]
  32. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ. et al. 2008. Persistent epigenetic differences associated with prenatal exposure to famine in humans. PNAS 105:17046–49 [Google Scholar]
  33. Herman JG, Baylin SB. 2003. Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349:2042–54 [Google Scholar]
  34. Jasienska G. 2009. Low birth weight of contemporary African Americans: an intergenerational effect of slavery?. Am. J. Hum. Biol. 21:16–24 [Google Scholar]
  35. Jawahar M, Murgatroyd C, Harrison E, Baune B. 2015. Epigenetic alterations following early postnatal stress: a review on novel aetiological mechanisms of common psychiatric disorders. Clin. Epigenet. 7:122 [Google Scholar]
  36. Johansson Å, Enroth S, Gyllensten U. 2013. Continuous aging of the human DNA methylome throughout the human lifespan. PLOS ONE 8:e67378 [Google Scholar]
  37. Jones PA. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13:484–92 [Google Scholar]
  38. Kang H-J, Kim J-M, Bae K-Y, Kim S-W, Shin I-S. et al. 2015. Longitudinal associations between BDNF promoter methylation and late-life depression. Neurobiol. Aging 36:1764e1–7 [Google Scholar]
  39. Keller S, Sarchiapone M, Zarrilli F, Videtic A, Ferraro A. et al. 2010. Increased BDNF promoter methylation in the Wernicke area of suicide subjects. Arch. Gen. Psychiatry 67:258–67 [Google Scholar]
  40. Kertes DA, Kamin H, Hughes DA, Rodney N, Bhatt SS, Mulligan CJ. 2015. Maternal stress predicts methylation of genes regulating the HPA axis in mothers and newborns in the Democratic Republic of Congo. Psychoneuroendocrinology 61:5 [Google Scholar]
  41. Kim J-M, Kang H-J, Kim S-Y, Kim S-W, Shin I-S. et al. 2015. BDNF promoter methylation associated with suicidal ideation in patients with breast cancer. Int. J. Psychiatry Med. 49:75–94 [Google Scholar]
  42. Kinnally EL, Feinberg C, Kim D, Ferguson K, Leibel R. et al. 2011. DNA methylation as a risk factor in the effects of early life stress. Brain Behav. Immun. 25:1548–53 [Google Scholar]
  43. Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC. et al. 2013. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat. Neurosci. 16:33–41 [Google Scholar]
  44. Koss MP, Gidycz CA, Wisniewski N. 1987. The scope of rape: incidence and prevalence of sexual aggression and victimization in a national sample of higher education students. J. Consult. Clin. Psychol. 55:162–70 [Google Scholar]
  45. Krebs CP, Lindquist CH, Warner TD, Fisher BS, Martin SL. 2009. College women's experiences with physically forced, alcohol- or other drug-enabled, and drug-facilitated sexual assault before and since entering college. J. Am. Coll. Health 57:639–49 [Google Scholar]
  46. Kuzawa C, Quinn EA. 2009. Developmental Origins of Adult Function and Health: Evolutionary Hypotheses. Annu. Rev. Anthropol. 38:131–47 [Google Scholar]
  47. Kuzawa CW. 2005. Fetal origins of developmental plasticity: Are fetal cues reliable predictors of future nutritional environments?. Am. J. Hum. Biol. 17:5–21 [Google Scholar]
  48. Kuzawa CW, Pike IL. 2005. Introduction. Fetal origins of developmental plasticity. Am. J. Hum. Biol. 17:1–4 [Google Scholar]
  49. Kuzawa CW, Thayer ZM. 2011. Timescales of human adaptation: the role of epigenetic processes. Epigenomics 3:221–34 [Google Scholar]
  50. Laget S, Miotto B, Chin HG, Estève P-O, Roberts RJ. et al. 2014. MBD4 cooperates with DNMT1 to mediate methyl-DNA repression and protects mammalian cells from oxidative stress. Epigenetics 9:546–56 [Google Scholar]
  51. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E. et al. 2012. Factors underlying variable DNA methylation in a human community cohort. PNAS 109:17253–60 [Google Scholar]
  52. Lasker GW. 1969. Human biological adaptability. The ecological approach in physical anthropology. Science 166:1480–86 [Google Scholar]
  53. Lenkov K, Lee MH, Lenkov OD, Swafford A, Fernald RD. 2015. Epigenetic DNA Methylation Linked to Social Dominance. PLOS ONE 10:e0144750 [Google Scholar]
  54. McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonté B. et al. 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12:342–48 [Google Scholar]
  55. Mulligan CJ. 2015. Social and behavioral epigenetics. Am. Anthropol. 117:738–39 [Google Scholar]
  56. Mulligan CJ, D'Errico NC, Stees J, Hughes DA. 2012. Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics 7:853–57 [Google Scholar]
  57. Needham BL, Smith JA, Zhao W, Wang X, Mukherjee B. et al. 2015. Life course socioeconomic status and DNA methylation in genes related to stress reactivity and inflammation: The Multi-Ethnic Study of Atherosclerosis. Epigenetics 10:958–69 [Google Scholar]
  58. Nguyen K-DH, Pihur V, Ganesh SK, Rakha A, Cooper RS. et al. 2013. Effects of rare and common blood pressure gene variants on essential hypertension: results from the Family Blood Pressure Program, CLUE, and Atherosclerosis Risk in Communities studies. Circ. Res. 112318–26 [Google Scholar]
  59. Non AL, Binder AM, Kubzansky LD, Michels KB. 2014. Genome-wide DNA methylation in neonates exposed to maternal depression, anxiety, or SSRI medication during pregnancy. Epigenetics 9:964–72 [Google Scholar]
  60. Non AL, Thayer ZM. 2015. Epigenetics for anthropologists: an introduction to methods. Am. J. Hum. Biol. 27:295–303 [Google Scholar]
  61. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. 2008. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3:97–106 [Google Scholar]
  62. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ. 2008. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. Br. J. Obstet. Gynaecol. 115:1243–49 [Google Scholar]
  63. Palma-Gudiel H, Córdova-Palomera A, Eixarch E, Deuschle M, Fañanás L. 2015a. Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: a meta-analysis. Epigenetics 10:893–902 [Google Scholar]
  64. Palma-Gudiel H, Córdova-Palomera A, Leza JC, Fañanás L. 2015b. Glucocorticoid receptor gene (NR3C1) methylation processes as mediators of early adversity in stress-related disorders causality: a critical review. Neurosci. Biobehav. Rev. 55:520–35 [Google Scholar]
  65. Panter-Brick C. 2010. Conflict, violence, and health: setting a new interdisciplinary agenda. Soc. Sci. Med. 70:1–6 [Google Scholar]
  66. Panter-Brick C, Grimon M-P, Kalin M, Eggerman M. 2015. Trauma memories, mental health, and resilience: a prospective study of Afghan youth. J. Child Psychol. Psychiatry 56:814–25 [Google Scholar]
  67. Pastor WA, Aravind L, Rao A. 2013. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell. Biol. 14:341–56 [Google Scholar]
  68. Perroud N, Salzmann A, Prada P, Nicastro R, Hoeppli ME. et al. 2013. Response to psychotherapy in borderline personality disorder and methylation status of the BDNF gene. Transl. Psychiatry 3:e207 [Google Scholar]
  69. Pike IL, Straight B, Oesterle M, Hilton C, Lanyasunya A. 2010. Documenting the health consequences of endemic warfare in three pastoralist communities of northern Kenya: a conceptual framework. Soc. Sci. Med. 70:45–52 [Google Scholar]
  70. Pike IL, Williams SR. 2006. Incorporating psychosocial health into biocultural models: preliminary findings from Turkana women of Kenya. Am. J. Hum. Biol. 18:729–40 [Google Scholar]
  71. Plongthongkum N, Diep DH, Zhang K. 2014. Advances in the profiling of DNA modifications: cytosine methylation and beyond. Nat. Rev. Genet. 15:647–61 [Google Scholar]
  72. Pluess M, Belsky J. 2011. Prenatal programming of postnatal plasticity?. Dev. Psychopathol. 23:29–38 [Google Scholar]
  73. Popp C, Dean W, Feng S, Cokus SJ, Andrews S. et al. 2010. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463:1101–5 [Google Scholar]
  74. Radtke KM, Ruf M, Gunter HM, Dohrmann K, Schauer M. et al. 2011. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl. Psychiatry 1:e21 [Google Scholar]
  75. Reed RV, Fazel M, Jones L, Panter-Brick C, Stein A. 2012. Mental health of displaced and refugee children resettled in low-income and middle-income countries: risk and protective factors. Lancet 379:250–65 [Google Scholar]
  76. Reynolds LM, Taylor JR, Ding J, Lohman K, Johnson C. et al. 2014. Age-related variations in the methylome associated with gene expression in human monocytes and T cells. Nat. Commun. 5:5366 [Google Scholar]
  77. Rodney NC, Mulligan CJ. 2014. A biocultural study of the effects of maternal stress on mother and newborn health in the Democratic Republic of Congo. Am. J. Phys. Anthropol. 155:200–9 [Google Scholar]
  78. Roseboom TJ, Painter RC, van Abeelen AFM, Veenendaal MVE, de Rooij SR. 2011. Hungry in the womb: What are the consequences? Lessons from the Dutch famine. Maturitas 70:141–45 [Google Scholar]
  79. Saban KL, Mathews HL, DeVon HA, Janusek LW. 2014. Epigenetics and social context: implications for disparity in cardiovascular disease. Aging Dis. 5:346–55 [Google Scholar]
  80. Seckl JR, Meaney MJ. 2006. Glucocorticoid “programming” and PTSD risk. Ann. N. Y. Acad. Sci. 1071:351–78 [Google Scholar]
  81. Siklenka K, Erkek S, Godmann M, Lambrot R, McGraw S. et al. 2015. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350: doi: 10.1126/science.aab2006 [Google Scholar]
  82. Smallwood SA, Kelsey G. 2012. De novo DNA methylation: a germ cell perspective. Trends Genet. 28:33–42 [Google Scholar]
  83. Straight B, Pike I, Hilton C, Oesterle M. 2014. Suicide in three East African pastoralist communities and the role of researcher outsiders for positive transformation: a case study. Cult. Med. Psychiatry 39:557–78 [Google Scholar]
  84. Thaler L, Gauvin L, Joober R, Groleau P, de Guzman R. et al. 2014. Methylation of BDNF in women with bulimic eating syndromes: associations with childhood abuse and borderline personality disorder. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 54:43–49 [Google Scholar]
  85. Thayer Z, Non A. 2015. Anthropology meets epigenetics: current and future directions. Am. Anthropol. 117:722–35 [Google Scholar]
  86. Tung J, Barreiro LB, Johnson ZP, Hansen KD, Michopoulos V. et al. 2012. Social environment is associated with gene regulatory variation in the rhesus macaque immune system. PNAS 109:6490–95 [Google Scholar]
  87. Turecki G, Meaney MJ. 2016. Effects of the social environment and stress on glucocorticoid receptor gene methylation: a systematic review. Biol. Psychiatry 79:87–96 [Google Scholar]
  88. Vukojevic V, Kolassa I-T, Fastenrath M, Gschwind L, Spalek K. et al. 2014. Epigenetic modification of the glucocorticoid receptor gene is linked to traumatic memory and post-traumatic stress disorder risk in genocide survivors. J. Neurosci. 34:10274–84 [Google Scholar]
  89. Waddington CH. 2012 (1942). The epigenotype. Int. J. Epidemiol. 41:10–13 [Google Scholar]
  90. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S. et al. 2004. Epigenetic programming by maternal behavior. Nat. Neurosci. 7:847–54 [Google Scholar]
  91. Yehuda R, Daskalakis NP, Bierer LM, Bader HN, Klengel T. et al. 2015. Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biol. Psychiatry. doi: 10.1016/j.biopsych.2015.08.005 [Google Scholar]
  92. Yehuda R, Flory JD, Bierer LM, Henn-Haase C, Lehrner A. et al. 2014. Lower methylation of glucocorticoid receptor gene promoter 1F in peripheral blood of veterans with posttraumatic stress disorder. Biol. Psychiatry 77:356–64 [Google Scholar]
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