Methylation of NR3C1 is related to maternal PTSD, parenting stress and maternal medial prefrontal cortical activity in response to child separation among mothers with histories of violence exposure

Frontiers in Psychology

Volumn 6, Issue , 2015, Pages

  Schechter, Daniel S ^a,b   Moser, Dominik A ^a   Paoloni Giacobino, Ariane ^c   Stenz, Ludwig ^c   Gex Fabry, Marianne ^a   Aue, Tatjana ^d,e   Adouan, Wafae ^c   Cordero, María I ^a,e,f   Suardi, Francesca ^a   Manini, Aurelia ^a   Sancho Rossignol, Ana ^a   Merminod, Gaëlle ^a   Ansermet, Francois ^a   Dayer, Alexandre G ^a   Rusconi Serpa, Sandra ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b Columbia University College of Physicians and Surgeons New York ^*  (United States)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e UNIVERSITY OF BERN   (Switzerland)

^f MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

Author keywords

early life stress; epigenetics; fMRI; glucocorticoid receptor (NR3c1); interpersonal violence; methylation; parenting; PTSD

Indexed keywords

EID: 84953747843     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2015.00690     Document Type: Article

References (46)

1. Abidin R. (1995). Parenting Stress Index 3rd Edn. Lutz, FL: Psychological Assessment Resources Inc.
2. Blake D. D. Weathers F. W. Nagy L. M. Kaloupek D. G. Gusman F. D. Charney D. S. et al. (1995). The development of a Clinician-Administered PTSD Scale. J. Trauma Stress 8 75–90. 10.1002/jts.2490080106
3. Blanchard E. B. Jones-Alexander J. Buckley T. C. Forneris C. A. (1996). Psychometric properties of the PTSD checklist (PCL). Behav. Res. Ther. 34 669–673. 10.1016/0005-7967(96)00033-2
4. Bogdan R. Hyde L. W. Hariri A. R. (2013). A neurogenetics approach to understanding individual differences in brain, behavior, and risk for psychopathology. Mol. Psychiatry 18 288–299. 10.1038/mp.2012.35
5. Breslau N. Koenen K. C. Luo Z. Agnew-Blais J. Swanson S. Houts R. M. et al. (2014). Childhood maltreatment, juvenile disorders and adult post-traumatic stress disorder: a prospective investigation. Psychol. Med. 44 1937–1945. 10.1017/S0033291713002651
6. Cao-Lei L. Massart R. Suderman M. J. Machnes Z. Elgbeili G. Laplante D. P. et al. (2014). DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: project ice storm. PLoS ONE 9:e107653. 10.1371/journal.pone.0107653
7. Cohen L. R. Hien D. A. Batchelder S. (2008). The impact of cumulative maternal trauma and diagnosis on parenting behavior. Child Maltreat. 13 27–38. 10.1177/107755950731004513/1/27
8. Cote S. M. Vaillancourt T. Leblanc J. C. Nagin D. S. Tremblay R. E. (2006). The development of physical aggression from toddlerhood to pre-adolescence: a nation wide longitudinal study of Canadian children. J. Abnorm. Child Psychol. 34 71–85. 10.1007/s10802-005-9001-z
9. Crockett E. E. Holmes B. M. Granger D. A. Lyons-Ruth K. (2013). Maternal disrupted communication during face-to-face interaction at 4 months: relation to maternal and Infant cortisol among at-risk families. Infancy 18 1111–1134. 10.1111/infa.12015
10. Daskalakis N. P. Lehrner A. Yehuda R. (2013). Endocrine aspects of post-traumatic stress disorder and implications for diagnosis and treatment. Endocrinol. Metab. Clin. North Am. 42 503–513. 10.1016/j.ecl.2013.05.004
11. Dumais A. Lesage A. D. Alda M. Rouleau G. Dumont M. Chawky N. et al. (2005). Risk factors for suicide completion in major depression: a case-control study of impulsive and aggressive behaviors in men. Am. J. Psychiatry 162 2116–2124. 10.1176/appi.ajp.162.11.2116
12. Elzinga B. M. Roelofs K. Tollenaar M. S. Bakvis P. Van Pelt J. Spinhoven P. (2008). Diminished cortisol responses to psychosocial stress associated with lifetime adverse events a study among healthy young subjects. Psychoneuroendocrinology 33 227–237. 10.1016/j.psyneuen.2007.11.004
13. Engel S. M. Berkowitz G. S. Wolff M. S. Yehuda R. (2005). Psychological trauma associated with the World Trade Center attacks and its effect on pregnancy outcome. Paediatr. Perinat. Epidemiol. 19 334–341. 10.1111/j.1365-3016.2005.00676.x
14. Farnfield S. Hautamaki A. Norbech P. Sahhar N. (2010). DMM assessments of attachment and adaptation: procedures, validity and utility. Clin. Child Psychol. Psychiatry 15 313–328. 10.1177/1359104510364315
15. First M. B. Spitzer R. L. Gibbon M. Williams J. B. (1995). Structured Clinical Interview for DSM-IV Axis I Disorders. Washington, DC: American Psychiatric Press.
16. Huang Y. Pastor W. A. Shen Y. Tahiliani M. Liu D. R. Rao A. (2010). The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS ONE 5:e8888. 10.1371/journal.pone.0008888
17. Kubany E. S. Haynes S. N. Leisen M. B. Owens J. A. Kaplan A. S. Watson S. B. et al. (2000). Development and preliminary validation of a brief broad-spectrum measure of trauma exposure: the Traumatic Life Events Questionnaire. Psychol. Assess. 12 210–224. 10.1037/1040-3590.12.2.210
18. Kunster A. K. Fegert J. M. Ziegenhain U. (2010). Assessing parent–child interaction in the preschool years: a pilot study on the psychometric properties of the toddler CARE-Index. Clin. Child Psychol. Psychiatry 15 379–389. 10.1177/1359104510367585
19. Largo R. H. Pfister D. Molinari L. Kundu S. Lipp A. Duc G. (1989). Significance of prenatal, perinatal and postnatal factors in the development of AGA preterm infants at five to seven years. Dev. Med. Child Neurol. 31 440–456. 10.1111/j.1469-8749.1989.tb04022.x
20. Lowe R. Gemma C. Beyan H. Hawa M. I. Bazeos A. Leslie R. D. et al. (2013). Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies. Epigenetics 8 445–454. 10.4161/epi.24362
21. Marshall R. D. Schneier F. R. Fallon B. A. Knight C. B. Abbate L. A. Goetz D. et al. (1998). An open trial of paroxetine in patients with noncombat-related, chronic posttraumatic stress disorder. J. Clin. Psychopharmacol. 18 10–18. 10.1097/00004714-199802000-00003
22. McGowan P. O. Sasaki A. D’alessio A. C. Dymov S. Labonte B. Szyf M. et al. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12 342–348. 10.1038/nn.2270
23. Oberlander T. F. Weinberg J. Papsdorf M. Grunau R. Misri S. Devlin A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3 97–106. 10.4161/epi.3.2.6034
24. Perroud N. Paoloni-Giacobino A. Prada P. Olie E. Salzmann A. Nicastro R. et al. (2011). 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 1:e59. 10.1038/tp.2011.60
25. Pervanidou P. Kolaitis G. Charitaki S. Lazaropoulou C. Papassotiriou I. Hindmarsh P. et al. (2007). The natural history of neuroendocrine changes in pediatric posttraumatic stress disorder (PTSD) after motor vehicle accidents: progressive divergence of noradrenaline and cortisol concentrations over time. Biol. Psychiatry 62 1095–1102. 10.1016/j.biopsych.2007.02.008
26. Romens S. E. Mcdonald J. Svaren J. Pollak S. D. (2014). Associations between early life stress and gene methylation in children. Child Dev. 86 303–309. 10.1111/cdev.12270
27. Sancho Rossignol A. S. Cordero M. I. Azbar R. Bonnet J. Epiney M. Rusconi Serpa S. et al. (2014). “Maternal psychosocial and neurobiological stress during pregnancy,” in Proceedings of the 14th Congress of the World Association of Infant Mental Health. Edinburgh, Scotland: Infant Mental Health.
28. Schechter D. S. Coates S. Kaminer T. Coots T. Zeanah C. Davies M. et al. (2008). Distorded maternal mental representations and atypical behavior in a clinical sample of violence-exposed mothers and their toddlers. J. Trauma Dissociation 9 123–147. 10.1080/15299730802045666
29. Schechter D. S. Coots T. Zeanah C. H. Davies M. Coates S. W. Trabka K. A. et al. (2005). Maternal mental representations of the child in an inner-city clinical sample: violence-related posttraumatic stress and reflective functioning. Attach. Hum. Dev. 7 313–331. 10.1080/14616730500246011
30. Schechter D. S. Moser D. A. Wang Z. Marsh R. Hao X. Duan Y. et al. (2012). An fMRI study of the brain responses of traumatized mothers to viewing their toddlers during separation and play. Soc. Cogn. Affect. Neurosci. 7 969–979. 10.1093/scan/nsr069
31. Schechter D. S. Willheim E. Hinojosa C. Scholfield-Kleinman K. Turner J. B. Mccaw J. et al. (2010). Subjective and objective measures of parent-child relationship dysfunction, child separation distress, and joint attention. Psychiatry 73 130–144. 10.1521/psyc.2010.73.2.130
32. Schechter D. S. Zeanah C. H. Jr. Myers M. M. Brunelli S. A. Liebowitz M. R. Marshall R. D. et al. (2004). Psychobiological dysregulation in violence-exposed mothers: salivary cortisol of mothers with very young children pre- and post-separation stress. Bull. Menninger Clin. 68 319–336. 10.1521/bumc.68.4.319.56642
33. Schechter D. S. Zygmunt A. Coates S. W. Davies M. Trabka K. Mccaw J. et al. (2007). Caregiver traumatization adversely impacts young children’s mental representations on the MacArthur Story Stem Battery. Attach. Hum. Dev. 9 187–205. 10.1080/14616730701453762
34. Slotnick S. D. Moo L. R. Segal J. B. Hart J. Jr. (2003). Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain Res. Cogn. Brain Res. 17 75–82. 10.1016/S0926-6410(03)00082-X
35. Sorrells S. F. Sapolsky R. M. (2007). An inflammatory review of glucocorticoid actions in the CNS. Brain Behav. Immun. 21 259–272. 10.1016/j.bbi.2006.11.006
36. Straus M. A. Douglas E. M. (2004). A short form of the Revised Conflict Tactics Scales, and typologies for severity and mutuality. Violence Vict. 19 507–520. 10.1891/vivi.19.5.507.63686
37. Tyrka A. R. Price L. H. Marsit C. Walters O. C. Carpenter L. L. (2012). Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS ONE 7:e30148. 10.1371/journal.pone.0030148
38. Weathers F. W. Keane T. M. Davidson J. R. (2001). Clinician-administered PTSD scale: a review of the first ten years of research. Depress. Anxiety 13 132–156. 10.1002/da.1029
39. Weder N. Zhang H. Jensen K. Yang B. Z. Simen A. Jackowski A. et al. (2014). Child abuse, depression, and methylation in genes involved with stress, neural plasticity, and brain circuitry. J. Am. Acad. Child Adolesc. Psychiatry 53 417–424 e415. 10.1016/j.jaac.2013.12.025
40. World Medical Association. (1999). Proposed revision of the Declaration of Helsinki. Bull. Med. Ethics 147 18–22.
41. Yehuda R. Bierer L. M. Schmeidler J. Aferiat D. H. Breslau I. Dolan S. (2000). Low cortisol and risk for PTSD in adult offspring of holocaust survivors. Am. J. Psychiatry 157 1252–1259. 10.1176/appi.ajp.157.8.1252
42. Yehuda R. Daskalakis N. P. Desarnaud F. Makotkine I. Lehrner A. L. Koch E. et al. (2013). Epigenetic biomarkers as predictors and correlates of symptom improvement following psychotherapy in combat veterans with PTSD. Front. Psychiatry 4:118. 10.3389/fpsyt.2013.00118
43. Yehuda R. Daskalakis N. P. Lehrner A. Desarnaud F. Bader H. N. Makotkine I. et al. (2014a). Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring. Am. J. Psychiatry 171 872–880. 10.1176/appi.ajp.2014.13121571
44. Yehuda R. Flory J. D. Bierer L. M. Henn-Haase C. Lehrner A. Desarnaud F. et al. (2014b). Lower methylation of glucocorticoid receptor gene promoter 1 in peripheral blood of veterans with posttraumatic stress disorder. Biol. Psychiatry 77 356–364. 10.1016/j.biopsych.2014.02.006
45. Yehuda R. Teicher M. H. Seckl J. R. Grossman R. A. Morris A. Bierer L. M. (2007). Parental posttraumatic stress disorder as a vulnerability factor for low cortisol trait in offspring of holocaust survivors. Arch. Gen. Psychiatry 64 1040–1048. 10.1001/archpsyc.64.9.1040
46. Zeanah C. Larrieu J. A. Heller S. S. Vallier J. (2000). “Infant-parent relationship assessment,” in Handbook of Infant Mental Health ed. Zeanah C. H. (New York, NY: Guilford Press) 222–235.