DNA methylation at stress-related genes is associated with exposure to early life institutionalization

American Journal of Physical Anthropology

Volumn 161, Issue 1, 2016, Pages 84-93

  Non, Amy L ^a   Hollister, Brittany M ^b   Humphreys, Kathryn L ^c   Childebayeva, Ainash ^b   Esteves, Kyle ^d   Zeanah, Charles H ^d   Fox, Nathan A ^e   Nelson, Charles A ^f,g   Drury, Stacy S ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c STANFORD UNIVERSITY   (United States)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MARYLAND   (United States)

^f BOSTON CHILDREN S HOSPITAL   (United States)

^g HARVARD GRADUATE SCHOOL OF EDUCATION   (United States)

Author keywords

early life adversity; epigenetics; stress

Indexed keywords

GENOMIC DNA; SEROTONIN TRANSPORTER;

ARTICLE; CHEEK MUCOSA; CHILD; CPG ISLAND; DNA METHYLATION; EPITHELIUM CELL; FEMALE; FKBP5 GENE; FOLLOW UP; FOSTER CARE; GENE; GENETIC ASSOCIATION; HUMAN; INFANT; INSTITUTIONALIZATION; MALE; PROSPECTIVE STUDY; QUANTITATIVE ANALYSIS; SLC6A4 GENE; SOCIAL ISOLATION;

EID: 84982193774     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.23010     Document Type: Article

References (52)

1. BethesdaMDDatabase of Single Nucleotide Polymorphisms (dbSNP). : National Center for Biotechnology Information, National Library of Medicine. dbSNP accession: rs1360785. Available from: http://www.ncbi/nlm.nih.gov/SNP.
2. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, Foley RA, Gluckman P, Godfrey K, Kirkwood T, Lahr MM, McNamara J, Metcalfe NB, Monaghan P, Spencer HG, Sultan SE. 2004. Developmental plasticity and human health. Nature 430:419–421.
3. Beach SR, Brody GH, Todorov AA, Gunter TD, Philibert RA. 2010. Methylation at SLC6A4 is linked to family history of child abuse: an examination of the Iowa Adoptee sample. Am J Med Genet B Neuropsychiatr Genet 153B:710–713.
4. Beach SR, Brody GH, Todorov AA, Gunter TD, Philibert RA. 2011. Methylation at 5HTT mediates the impact of child sex abuse on women's antisocial behavior: an examination of the Iowa adoptee sample. Psychosom Med 73:83–87.
5. Binder EB. 2009. The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology 34(uppl1):S186–195.
6. Bogdan R, Agrawal A, Gaffrey MS, Tillman R, Luby JL. 2014. Serotonin transporter-linked polymorphic region (5-HTTLPR) genotype and stressful life events interact to predict preschool-onset depression: a replication and developmental extension. J Child Psychol Psychiatry 55:448–457.
7. Buchmann AF, Holz N, Boecker R, Blomeyer D, Rietschel M, Witt SH, Schmidt MH, Esser G, Banaschewski T, Brandeis D, Zimmermann US, Laucht M. 2014. Moderating role of FKBP5 genotype in the impact of childhood adversity on cortisol stress response during adulthood. Eur Neuropsychopharmacol 24:837–845.
8. Dayer A. 2014. Serotonin-related pathways and developmental plasticity: relevance for psychiatric disorders. Dialogues Clin Neurosci 16:29–41.
9. Devlin AM, Brain U, Austin J, Oberlander TF. 2010. Prenatal exposure to maternal depressed mood and the MTHFR C677T variant affect SLC6A4 methylation in infants at birth. PloS One 5:e12201.
10. Drury SS, Gleason MM, Theall KP, Smyke AT, Nelson CA, Fox NA, Zeanah CH. 2012a. Genetic sensitivity to the caregiving context: the influence of 5httlpr and BDNF val66met on indiscriminate social behavior. Physiol Behav 106:728–735.
11. Drury SS, Theall K, Gleason MM, Smyke AT, De Vivo I, Wong JY, Fox NA, Zeanah CH, Nelson CA. 2012b. Telomere length and early severe social deprivation: linking early adversity and cellular aging. Mol Psychiatry 17:719–727.
12. Duman EA, Canli T. 2015. Influence of life stress, 5-HTTLPR genotype, and SLC6A4 methylation on gene expression and stress response in healthy Caucasian males. Biol Mood Anxiety Disord 5:2
13. Foley DL, Craig JM, Morley R, Olsson CA, Dwyer T, Smith K, Saffery R. 2009. Prospects for epigenetic epidemiology. Am J Epidemiol 169:389–400.
14. Fox NA, Almas AN, Degnan KA, Nelson CA, Zeanah CH. 2011. The effects of severe psychosocial deprivation and foster care intervention on cognitive development at 8 years of age: findings from the Bucharest Early Intervention Project. J Child Psychol Psychiatry 52:919–928.
15. Galobardes B, Smith GD, Lynch JW. 2006. Systematic review of the influence of childhood socioeconomic circumstances on risk for cardiovascular disease in adulthood. Ann Epidemiol 16:91–104.
16. Hertzman C. 1999. The biological embedding of early experience and its effects on health in adulthood. Ann N Y Acad Sci 896:85–95.
17. Humphreys KL, Gleason MM, Drury SS, Miron D, Nelson CA, 3rd, Fox NA, Zeanah CH. 2015. Effects of institutional rearing and foster care on psychopathology at age 12 years in Romania: follow-up of an open, randomised controlled trial. Lancet Psychiatry 2:625–634.
18. Jans LA, Riedel WJ, Markus CR, Blokland A. 2007. Serotonergic vulnerability and depression: assumptions, experimental evidence and implications. Mol Psychiatry 12:522–543.
19. Jawahar MC, Murgatroyd C, Harrison EL, Baune BT. 2015. Epigenetic alterations following early postnatal stress: a review on novel aetiological mechanisms of common psychiatric disorders. Clin Epigenetics 7:122
20. Karg K, Burmeister M, Shedden K, Sen S. 2011. The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch Gen Psychiatry 68:444–454.
21. Kertes DA, Kamin HS, Hughes DA, Rodney NC, Bhatt S, Mulligan CJ. 2016. Prenatal maternal stress predicts methylation of genes regulating the hypothalamic-pituitary-adrenocortical system in mothers and newborns in the Democratic Republic of Congo. Child Dev 87:61–72.
22. Kinnally EL, Capitanio JP, Leibel R, Deng L, LeDuc C, Haghighi F, Mann JJ. 2010. Epigenetic regulation of serotonin transporter expression and behavior in infant rhesus macaques. Genes Brain Behav 9:575–582.
23. 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. 2013. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat Neurosci 16:33–41.
24. Koss KJ, Hostinar CE, Donzella B, Gunnar MR. 2014. Social deprivation and the HPA axis in early development. Psychoneuroendocrinology 50:1–13.
25. Kuzawa CW, Sweet E. 2009. Epigenetics and the embodiment of race: developmental origins of US racial disparities in cardiovascular health. Am J Hum Biol 21:2–15.
26. Lowe R, Gemma C, Beyan H, Hawa MI, Bazeos A, Leslie RD, Montpetit A, Rakyan VK, Ramagopalan SV. 2013. Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies. Epigenetics 8:445–454.
27. Lupien SJ, McEwen BS, Gunnar MR, Heim C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445.
28. Marshall WA, Tanner JM. 1969. Variations in pattern of pubertal changes in girls. Arch Dis Child 44:291–303.
29. Marshall WA, Tanner JM. 1970. Variations in the pattern of pubertal changes in boys. Arch Dis Child 45:13–23.
30. McLaughlin KA, Fox NA, Zeanah CH, Nelson CA. 2011. Adverse rearing environments and neural development in children: the development of frontal electroencephalogram asymmetry. Biol Psychiatry 70:1008–1015.
31. McLaughlin KA, Sheridan MA, Tibu F, Fox NA, Zeanah CH, Nelson CA. 3rd. 2015. Causal effects of the early caregiving environment on development of stress response systems in children. Proc Natl Acad Sci U S A 112:5637–5642.
32. Naumova OY, Lee M, Koposov R, Szyf M, Dozier M, Grigorenko EL. 2012. Differential patterns of whole-genome DNA methylation in institutionalized children and children raised by their biological parents. Dev Psychopathol 24:143–155.
33. Nelson CA, 3rd, Zeanah CH, Fox NA, Marshall PJ, Smyke AT, Guthrie D. 2007. Cognitive recovery in socially deprived young children: the Bucharest early intervention project. Science 318:1937–1940.
34. Nelson CA, Fox NA, and Zeanah CH. 2014. Romania's abandoned children: deprivation, brain development, and the struggle for recovery. Cambridge, Massachusetts: Harvard University Press. 402 p.
35. Ouellet-Morin I, Wong CC, Danese A, Pariante CM, Papadopoulos AS, Mill J, Arseneault L. 2013. Increased serotonin transporter gene (SERT) DNA methylation is associated with bullying victimization and blunted cortisol response to stress in childhood: a longitudinal study of discordant monozygotic twins. Psychol Med 43:1813–1823.
36. Palma-Gudiel H, Córdova-Palomera A, Leza JC, Fañanás L. 2015. Glucocorticoid receptor gene (NR3C1) methylation processes as mediators of early adversity in stress-related disorders causality: A critical review. Neurosci Biobehav Rev 55:520–535.
37. Phillips NK, Hammen CL, Brennan PA, Najman JM, Bor W. 2005. Early adversity and the prospective prediction of depressive and anxiety disorders in adolescents. J Abnorm Child Psychol 33:13–24.
38. Pollak SD, Nelson CA, Schlaak MF, Roeber BJ, Wewerka SS, Wiik KL, Frenn KA, Loman MM, Gunnar MR. 2010. Neurodevelopmental effects of early deprivation in postinstitutionalized children. Child Dev 81:224–236.
39. 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. 2012. The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. J Neurosci 32:15626–15642.
40. Slopen N, Koenen KC, Kubzansky LD. 2012. Childhood adversity and immune and inflammatory biomarkers associated with cardiovascular risk in youth: a systematic review. Brain Behav Immun 26:239–250.
41. Smyke AT, Zeanah CH, Fox NA, Nelson CA, Guthrie D. 2010. Placement in foster care enhances quality of attachment among young institutionalized children. Child Dev 81:212–223.
42. Struber N, Struber D, Roth G. 2014. Impact of early adversity on glucocorticoid regulation and later mental disorders. Neurosci Biobehav Rev 38:17–37.
43. Todkar A, Granholm L, Aljumah M, Nilsson KW, Comasco E, Nylander I. 2015. HPA axis gene expression and DNA methylation profiles in rats exposed to early life stress, adult voluntary ethanol drinking and single housing. Front Mol Neurosci 8:90.
44. Turecki G, Meaney MJ. 2014. Effects of the social environment and stress on glucocorticoid receptor gene methylation: a systematic review. Biol Psychiatry 79:87–96.
45. Tyrka AR, Ridout KK, Parade SH, Paquette A, Marsit CJ, Seifer R. 2015. Childhood maltreatment and methylation of FK506 binding protein 5 gene (FKBP5). Dev Psychopathol 27:1637–1645.
46. van der Knaap LJ, Riese H, Hudziak JJ, Verbiest MM, Verhulst FC, Oldehinkel AJ, van Oort FV. 2015. Adverse life events and allele-specific methylation of the serotonin transporter gene (SLC6A4) in adolescents: the TRAILS study. Psychosom Med 77:246–255.
47. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854.
48. Weickert CS, Webster MJ, Boerrigter D, Sinclair D. 2016. FKBP5 messenger RNA increases after adolescence in human dorsolateral prefrontal cortex. Biol Psychiatry e1–e3.
49. Yehuda R, Daskalakis NP, Bierer LM, Bader HN, Klengel T, Holsboer F, Binder EB. 2015. Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation. Biol Psychiatry
50. Zeanah CH, Fox NA, Nelson CA. 2012. The Bucharest early intervention project: case study in the ethics of mental health research. J Nerv Ment Dis 200:243–247.
51. Zeanah CH, Nelson CA, Fox NA, Smyke AT, Marshall P, Parker SW, Koga S. 2003. Designing research to study the effects of institutionalization on brain and behavioral development: the Bucharest Early Intervention Project. Dev Psychopathol 15:885–907.
52. Zhang TY, Hellstrom IC, Bagot RC, Wen X, Diorio J, Meaney MJ. 2010. Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. J Neurosci 30:13130–13137.