Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. the TRAILS study

Translational Psychiatry

Volumn 4, Issue , 2014, Pages

  Van Der Knaap, L J ^a   Riese, H ^b,c   Hudziak, J J ^a,d   Verbiest, M M P J ^e   Verhulst, F C ^e   Oldehinkel, A J ^b   Van Oort, F V A ^a  

^a SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^e ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID RECEPTOR; NR3C1 PROTEIN; UNCLASSIFIED DRUG; NR3C1 PROTEIN, HUMAN;

ADOLESCENCE; ADOLESCENT; ADULT; AGE DISTRIBUTION; ARTICLE; BIRTH; CHILD; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA METHYLATION; EARLY LIFE STRESS; EPIGENETICS; FEMALE; GENE; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GLUCOCORTICOID RECEPTOR GENE; GROUPS BY AGE; HIGH RISK POPULATION; HUMAN; INFANT; LIFE EVENT; MALE; NEWBORN; NORMAL HUMAN; PERINATAL STRESS; PERSONAL EXPERIENCE; POPULATION RESEARCH; POSTTRAUMATIC STRESS DISORDER; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; RISK ASSESSMENT; RISK FACTOR; STRESS; STRESSFUL LIFE EVENT; CHILD ABUSE; EPIDEMIOLOGY; GENETIC EPIGENESIS; GENETICS; MENTAL STRESS; METABOLISM; NETHERLANDS; AMPLICON; CPG ISLAND; LIFE STRESS; MAJOR CLINICAL STUDY; PROTEIN METHYLATION; SEXUAL ABUSE;

ADOLESCENT; CHILD ABUSE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HUMANS; LIFE CHANGE EVENTS; MALE; NETHERLANDS; RECEPTORS, GLUCOCORTICOID; STRESS, PSYCHOLOGICAL;

EID: 84927760119     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2014.22     Document Type: Article

References (50)

1. Heim C, Newport DJ, Mletzko T, Miller AH, Nemeroff CB. The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 2008; 33: 693-710.
2. Heim C, Newport DJ, Wagner D, Wilcox MM, Miller AH, Nemeroff CB. The role of early adverse experience and adulthood stress in the prediction of neuroendocrine stress reactivity in women: a multiple regression analysis. Depress Anxiety 2002; 15: 117-125. (Pubitemid 34522472)
3. Holsboer F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 2000; 23: 477-501.
4. Bosch NM, Riese H, Reijneveld SA, Bakker MP, Verhulst FC, Ormel J et al. Timing matters: long term effects of adversities from prenatal period up to adolescence on adolescents' cortisol stress response. The TRAILS study. Psychoneuroendocrinology 2012; 37: 1439-1447.
5. Xiong F, Zhang L. Role of the hypothalamic-pituitary-adrenal axis in developmental programming of health and disease. Front Neuroendocrinol 2013; 34: 27-46.
6. Hunter RG, McEwen BS. Stress and anxiety across the lifespan: structural plasticity and epigenetic regulation. Epigenomics 2013; 5: 177-194.
7. Razin A, Cedar H. DNA methylation and gene expression. Microbiol Rev 1991; 55: 451-458. (Pubitemid 21895162)
8. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 1998; 17: 4905-4908. (Pubitemid 28408457)
9. Watt F, Molloy PL. Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 1988; 2: 1136-1143.
10. Bird AP, Wolffe AP. Methylation-induced repression-belts, braces, and chromatin. Cell 1999; 99: 451-454. (Pubitemid 129746827)
11. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006; 31: 89-97. (Pubitemid 43221841)
12. Szyf M. The dynamic epigenome and its implications in toxicology. Toxicol Sci 2007; 100: 7-23. (Pubitemid 47617798)
13. Faulk C, Dolinoy DC. Timing is everything: the when and how of environmentally induced changes in the epigenome of animals. Epigenetics 2011; 6: 791-797.
14. Szyf M. The early life environment and the epigenome. Biochim Biophys Acta 2009; 1790: 878-885.
15. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7: 847-854. (Pubitemid 38989508)
16. McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonte B, Szyf M et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 2009; 12: 342-348.
17. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008; 3: 97-106.
18. Radtke KM, Ruf M, Gunter HM, Dohrmann K, Schauer M, Meyer A et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl Psychiatry 2011; 1: e21.
19. Mulligan CJ, D'Errico NC, Stees J, Hughes DA. Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics 2012; 7: 853-857.
20. Perroud N, Paoloni-Giacobino A, Prada P, Olie E, Salzmann A, Nicastro R et al. Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma. Transl Psychiatry 2011; 1: e59.
21. Tyrka AR, Price LH, Marsit C, Walters OC, Carpenter LL. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS One 2012; 7: e30148.
22. Perroud N, Dayer A, Piguet C, Nallet A, Favre S, Malafosse A et al. Childhood maltreatment and methylation of the glucocorticoid receptor gene NR3C1 in bipolar disorder. Br J Psychiatry 2013; 204: 30-35.
23. de Rooij SR, Costello PM, Veenendaal MV, Lillycrop KA, Gluckman PD, Hanson MA et al. Associations between DNA methylation of a glucocorticoid receptor promoter and acute stress responses in a large healthy adult population are largely explained by lifestyle and educational differences. Psychoneuroendocrinology 2012; 37: 782-788.
24. Essex MJ, Boyce WT, Hertzman C, Lam LL, Armstrong JM, Neumann SM et al. Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence. Child Dev 2013; 84: 58-75.
25. Murgatroyd C, Spengler D. Epigenetics of early child development. Front Psychiatry 2011; 2: 16.
26. Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009; 10: 434-445.
27. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 2005; 102: 10604-10609. (Pubitemid 41061601)
28. Talens RP, Christensen K, Putter H, Willemsen G, Christiansen L, Kremer D et al. Epigenetic variation during the adult lifespan: cross-sectional and longitudinal data on monozygotic twin pairs. Aging Cell 2012; 11: 694-703.
29. Wong CC, Caspi A, Williams B, Craig IW, Houts R, Ambler A et al. A longitudinal study of epigenetic variation in twins. Epigenetics 2010; 5: 516-526.
30. Veenema AH. Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front Neuroendocrinol 2009; 30: 497-518.
31. McGorry PD, Purcell R, Goldstone S, Amminger GP. Age of onset and timing of treatment for mental and substance use disorders: implications for preventive intervention strategies and models of care. Curr Opin Psychiatry 2011; 24: 301-306.
32. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 2009; 12: 1559-1566.
33. Huisman M, Oldehinkel AJ, de Winter A, Minderaa RB, de Bildt A, Huizink AC et al. Cohort profile: the Dutch 'TRacking Adolescents' Individual Lives' Survey'; TRAILS. Int J Epidemiol 2008; 37: 1227-1235.
34. Ormel J, Oldehinkel AJ, Sijtsema J, van Oort F, Raven D, Veenstra R et al. The TRacking Adolescents' Individual Lives Survey (TRAILS): design, current status, and selected findings. J Am Acad Child Adolesc Psychiatry 2012; 51: 1020-1036.
35. Reijneveld SA, Brugman E, Verhulst FC, Verloove-Vanhorick SP. Identification and management of psychosocial problems among toddlers in Dutch preventive child health care. Arch Pediatr Adolesc Med 2004; 158: 811-817. (Pubitemid 39025082)
36. Caspi A, Moffitt TE, Thornton A, Freedman D, Amell JW, Harrington Het al. The life history calendar: A research and clinical assessment method for collecting retrospective event-history data. Int J Methods Psychiatr Res 1996; 6, 101-114. (Pubitemid 126812777)
37. Labonte B, Yerko V, Gross J, Mechawar N, Meaney MJ, Szyf M et al. Differential glucocorticoid receptor exon 1(B), 1(C), and 1(H) expression and methylation in suicide completers with a history of childhood abuse. Biol Psychiatry 2012; 72: 41-48.
38. Turner JD, Alt SR, Cao L, Vernocchi S, Trifonova S, Battello N et al. Transcriptional control of the glucocorticoid receptor: CpG islands, epigenetics and more. Biochem Pharmacol 2010; 80: 1860-1868.
39. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988; 16: 1215.
40. Warnecke PM, Stirzaker C, Melki JR, Millar DS, Paul CL, Clark SJ. Detection and measurement of PCR bias in quantitative methylation analysis of bisulphitetreated DNA. Nucleic Acids Res 1997; 25: 4422-4426. (Pubitemid 27485227)
41. Murgatroyd C, Wu Y, Bockmuhl Y, Spengler D. Genes learn from stress: how infantile trauma programs us for depression. Epigenetics 2010; 5: 194-199.
42. Daniels WM, Fairbairn LR, van Tilburg G, McEvoy CR, Zigmond MJ, Russell VA et al. Maternal separation alters nerve growth factor and corticosterone levels but not the DNA methylation status of the exon 1(7) glucocorticoid receptor promoter region. Metab Brain Dis 2009; 24: 615-627.
43. Witzmann SR, Turner JD, Meriaux SB, Meijer OC, Muller CP. Epigenetic regulation of the glucocorticoid receptor promoter 1(7) in adult rats. Epigenetics 2012; 7: 1290-1301.
44. Branco MR, Ficz G, Reik W. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 2012; 13: 7-13.
45. Bhutani N, Burns DM, Blau HM. DNA demethylation dynamics. Cell 2011; 146: 866-872.
46. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 2005; 25: 11045-11054. (Pubitemid 41692634)
47. Turner JD, Schote AB, Macedo JA, Pelascini LP, Muller CP. Tissue specific glucocorticoid receptor expression, a role for alternative first exon usage? Biochem Pharmacol 2006; 72: 1529-1537.
48. Weaver IC, D'Alessio AC, Brown SE, Hellstrom IC, Dymov S, Sharma S et al. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J Neurosci 2007; 27: 1756-1768. (Pubitemid 46280071)
49. Turner JD, Pelascini LP, Macedo JA, Muller CP. Highly individual methylation patterns of alternative glucocorticoid receptor promoters suggest individualized epigenetic regulatory mechanisms. Nucleic Acids Res 2008; 36: 7207-7218.
50. Oldehinkel AJ, Ormel J, Bosch NM, Bouma EM, Van Roon AM, Rosmalen JG et al. Stressed out? Associations between perceived and physiological stress responses in adolescents: the TRAILS study. Psychophysiology 2011; 48: 441-452.