Personality vulnerability to depression, resilience, and depressive symptoms: epigenetic markers among perinatal women
Keywords:
trauma, resilience, depressive symptoms, pregnancy, epigenetics
Abstract
Background: We examined differences in DNA methylation patterns in the NR3C1 and FKBP5 genes in relation to personality vulnerability to depression, resilience, and perinatal depressive symptoms, whilst also considering possible moderating effects of childhood traumatic events.
Methods: N = 160 perinatal women were assessed at late pregnancy and 1 year postpartum for personality vulnerability to depression, resilience, depressive symptoms, and childhood traumatic events with self-reported questionnaires. NR3C1 and FKBP5 methylation markers were analyzed via sodium bisulfite sequencing. Associations of methylation markers with the above mentioned variables were tested using multivariable regressions.
Results: NR3C1 methylation at CpGs 1, 4 and average methylation sites were negatively associated with resilience; NR3C1 methylation at CpG 2 was positively associated with postpartum depressive symptoms; methylation at CpG 4 was positively associated with prenatal depressive symptoms. The interaction between current distress due to interpersonal traumatic events and NR3C1 CpG sites in relation to personality vulnerability was significant on CpG sites 3 and 4, whereas the interaction between current distress due to total traumatic events and NR3C1 in relation to personality vulnerability was significant on CpG site 2. FKBP5 showed no significant associations with the outcomes.
Conclusions: This study identified associations between NR3C1 methylation and resilience as well as perinatal depressive symptoms. Interestingly, an interaction between early trauma and personality vulnerability was noted. Our findings on these specific DNA methylation markers may, if replicated and integrated into risk prediction models, contribute to early diagnosis of mothers at risk, targeted health promotion, and early interventions.
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References
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2. Teicher MH, Samson JA, Anderson CM, Ohashi K. The effects of childhood maltreatment on brain structure, function and connectivity. Nat Rev Neurosci. 2016;17(10):652–66. doi: 10.1038/nrn.2016.111
3. Teicher MH, Samson JA. Annual research review: enduring neurobiological effects of childhood abuse and neglect. J Child Psychol Psychiatry. 2016;57(3):241–66. doi: 10.1111/jcpp.12507
4. Meltzer‐Brody S, Larsen J, Petersen L, Guintivano J, Florio AD, Miller W, et al. Adverse life events increase risk for postpartum psychiatric episodes: a population‐based epidemiologic study. Depress Anxiety. 2018;35(2):160–7. doi: 10.1002/da.22697
5. Lewis SJ, Arseneault L, Caspi A, Fisher HL, Matthews T, Moffitt TE, et al. The epidemiology of trauma and post-traumatic stress disorder in a representative cohort of young people in England and Wales. Lancet Psychiatry. 2019;6(3):247–56. doi: 10.1016/S2215-0366(19)30031-8
6. Green JG, McLaughlin KA, Berglund PA, Gruber MJ, Sampson NA, Zaslavsky AM, et al. Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Arch Gen Psychiatry. 2010;67(2):113–23. doi: 10.1001/archgenpsychiatry.2009.186
7. Weich S, Patterson J, Shaw R, Stewart-Brown S. Family relationships in childhood and common psychiatric disorders in later life: systematic review of prospective studies. Br J Psychiatry. 2009;194(5):392–8. doi: 10.1192/bjp.bp.107.042515
8. McGloin JM, Widom CS. Resilience among abused and neglected children grown up. Dev Psychopathol. 2001;13(4):1021–38. doi: 10.1017/S095457940100414X
9. Rutter M. The promotion of resilience in the face of adversity. In: Clarke-Stewart A, Dunn J, eds. Families count: Effects on child and adolescent development. Cambridge University Press, 2006; pp. 26–52. doi: 10.1017/CBO9780511616259.003
10. Yehuda R, Flory JD, Southwick S, Charney DS. Developing an agenda for translational studies of resilience and vulnerability following trauma exposure. Ann N Y Acad Sci. 2006;1071(1):379–96. doi: 10.1196/annals.1364.028
11. Collishaw S, Pickles A, Messer J, Rutter M, Shearer C, Maughan B. Resilience to adult psychopathology following childhood maltreatment: evidence from a community sample. Child Abuse Negl. 2007;31(3):211–29. doi: 10.1016/j.chiabu.2007.02.004
12. Smoller JW, Andreassen OA, Edenberg HJ, Faraone SV, Glatt SJ, Kendler KS. Psychiatric genetics and the structure of psychopathology. Mol Psychiatry. 2019;24(3):409–20. doi: 10.1038/s41380-017-0010-4
13. Heim C, Newport DJ, Heit S, Graham YP, Wilcox M, Bonsall R, et al. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA. 2000;284(5):592–7. doi: 10.1001/jama.284.5.592
14. Carpenter LL, Carvalho JP, Tyrka AR, Wier LM, Mello AF, Mello MF, et al. Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol Psychiatry. 2007;62(10):1080–7. doi: 10.1016/j.biopsych.2007.05.002
15. Perroud N, Paoloni-Giacobino A, Prada P, Olié 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(12):e59. doi: 10.1038/tp.2011.60
16. Bradley RG, Binder EB, Epstein MP, Tang Y, Nair HP, Liu W, et al. Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. Arch Gen Psychiatry. 2008;65(2):190–200. doi: 10.1001/archgenpsychiatry.2007.26
17. Russcher H, van Rossum EF, de Jong FH, Brinkmann AO, Lamberts SW, Koper JW. Increased expression of the glucocorticoid receptor – a translational isoform as a result of the ER22/23EK polymorphism. Mol Endocrinol. 2005;19(7):1687–96. doi: 10.1210/me.2004-0467
18. Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC, Pariante CM, et al. Allele-specific FKBP5 DNA demethylation mediates gene–childhood trauma interactions. Nat Neurosci. 2013;16(1):33–41. doi: 10.1038/nn.3275
19. Mehta D, Klengel T, Conneely KN, Smith AK, Altmann A, Pace TW, et al. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proc Natl Acad Sci. 2013;110(20):8302–7. doi: 10.1073/pnas.1217750110
20. Armans M, Addante S, Ciciolla L, Anderson M, Shreffler KM. Resilience during pregnancy: how early life experiences are associated with pregnancy-specific stress. Advers Resil Sci. 2020;1(4):295–305. doi: 10.1007/s42844-020-00017-3
21. Juul SH, Hendrix C, Robinson B, Stowe ZN, Newport DJ, Brennan PA, et al. Maternal early-life trauma and affective parenting style: the mediating role of HPA-axis function. Arch Womens Mental Health. 2016;19(1):17–23. doi: 10.1007/s00737-015-0528-x
22. Muzik M, Bocknek EL, Broderick A, Richardson P, Rosenblum KL, Thelen K, et al. Mother–infant bonding impairment across the first 6 months postpartum: the primacy of psychopathology in women with childhood abuse and neglect histories. Arch Womens Mental Health. 2013;16(1):29–38. doi: 10.1007/s00737-012-0312-0
23. Gee DG. Early adversity and development: parsing heterogeneity and identifying pathways of risk and resilience. Am J Psychiatry. 2021;178(11):998–1013. doi: 10.1176/appi.ajp.2021.21090944
24. Motsan S, Yirmiya K, Feldman R. Chronic early trauma impairs emotion recognition and executive functions in youth; specifying biobehavioral precursors of risk and resilience. Dev Psychopathol. 2022;34(4):1339–52. doi: 10.1017/S0954579421000067
25. Axfors C, Bränn E, Henriksson HE, Hellgren C, Kallak TK, Fransson E, et al. Cohort profile: the Biology, Affect, Stress, Imaging and Cognition (BASIC) study on perinatal depression in a population-based Swedish cohort. BMJ Open. 2019;9(10):e031514. doi: 10.1136/bmjopen-2019-031514
26. Boyce P, Hickey A, Gilchrist J, Talley N. The development of a brief personality scale to measure vulnerability to postnatal depression. Arch Womens Mental Health. 2001;3(4):147–53. doi: 10.1007/s007370170012
27. Lundman B, Strandberg G, Eisemann M, Gustafson Y, Brulin C. Psychometric properties of the Swedish version of the Resilience Scale. Scand J Caring Sci. 2007;21(2):229–37. doi: 10.1111/j.1471-6712.2007.00461.x
28. Wagnild G. A review of the Resilience Scale. J Nurs Meas. 2009;17(2):105–13. doi: 10.1891/1061-3749.17.2.105
29. Cox J, Holden J, Sagovsky R. Edinburgh postnatal depression scale (EPDS). Br J Psychiatry. 1987;150:782–6. doi: 10.1192/bjp.150.6.782
30. Rubertsson C, Börjesson K, Berglund A, Josefsson A, Sydsjö G. The Swedish validation of Edinburgh postnatal depression scale (EPDS) during pregnancy. Nord J Psychiatry. 2011;65(6):414–18. doi: 10.3109/08039488.2011.590606
31. Greenwald R, Rubin A. Assessment of posttraumatic symptoms in children: development and preliminary validation of parent and child scales. Res Soc Work Pract. 1999;9(1):61–75. doi: 10.1177/104973159900900105
32. Larsson I. LITE-P, life incidence of traumatic events. Translation into Swedish, with permission from the author. In: Greenwald R, ed. 2003.
33. Lilly MM, Valdez CE. Interpersonal trauma and PTSD: the roles of gender and a lifespan perspective in predicting risk. Psychol Trauma. 2012;4(1):140. doi: 10.1037/a0022947
34. Marshall C, Semovski V, Stewart SL. Exposure to childhood interpersonal trauma and mental health service urgency. Child Abuse Negl. 2020;106:104464. doi: 10.1016/j.chiabu.2020.104464
35. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170
36. Chen GG, Gross JA, Lutz P-E, Vaillancourt K, Maussion G, Bramoulle A, et al. Medium throughput bisulfite sequencing for accurate detection of 5-methylcytosine and 5-hydroxymethylcytosine. BMC Genomics. 2017;18(1):1–12. doi: 10.1186/s12864-017-3489-9
37. Palma-Gudiel H, Córdova-Palomera A, Leza JC, Fañanás L. Glucocorticoid receptor gene (NR3C1) methylation processes as mediators of early adversity in stress-related disorders causality: a critical review. Neurosci Biobehav Rev. 2015;55:520–35. doi: 10.1016/j.neubiorev.2015.05.016
38. Appleton AA, Kiley KC, Schell LM, Holdsworth EA, Akinsanya A, Beecher C. Prenatal lead and depression exposures jointly influence birth outcomes and NR3C1 DNA methylation. Int J Environ Res Public Health. 2021;18(22):12169.
39. Dos Santos RM. Isolation, social stress, low socioeconomic status and its relationship to immune response in covid-19 pandemic context. Brain Behav Immun Health. 2020;7:100103. doi: 10.1016/j.bbih.2020.100103
40. Turecki G, Meaney MJ. Effects of the social environment and stress on glucocorticoid receptor gene methylation: a systematic review. Biol Psychiatry. 2016;79(2):87–96. doi: 10.1016/j.biopsych.2014.11.022
41. 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(2):97–106. doi: 10.4161/epi.3.2.6034
42. 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(1):e30148. doi: 10.1371/journal.pone.0030148
43. Vukojevic V, Kolassa I-T, Fastenrath M, Gschwind L, Spalek K, Milnik A, et al. Epigenetic modification of the glucocorticoid receptor gene is linked to traumatic memory and post-traumatic stress disorder risk in genocide survivors. J Neurosci. 2014;34(31):10274–84. doi: 10.1523/JNEUROSCI.1526-14.2014
44. Hompes T, Izzi B, Gellens E, Morreels M, Fieuws S, Pexsters A, et al. Investigating the influence of maternal cortisol and emotional state during pregnancy on the DNA methylation status of the glucocorticoid receptor gene (NR3C1) promoter region in cord blood. J Psychiatr Res. 2013;47(7):880–91. doi: 10.1016/j.jpsychires.2013.03.009
45. Van Der Knaap L, Riese H, Hudziak J, Verbiest M, Verhulst F, Oldehinkel A, et al. Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. The TRAILS study. Transl Psychiatry. 2014;4(4):e381. doi: 10.1038/tp.2014.22
46. Miller O, Shakespeare-Finch J, Bruenig D, Mehta D. DNA methylation of NR3C1 and FKBP5 is associated with posttraumatic stress disorder, posttraumatic growth, and resilience. Psychol Trauma. 2020;12(7):750. doi: 10.1037/tra0000574
47. Mehta D, Miller O, Bruenig D, David G, Shakespeare‐Finch J. A systematic review of DNA methylation and gene expression studies in posttraumatic stress disorder, posttraumatic growth, and resilience. J Trauma Stress. 2020;33(2):171–80. doi: 10.1002/jts.22472
48. Bauer JJ, Bonanno GA. I can, I do, I am: the narrative differentiation of self-efficacy and other self-evaluations while adapting to bereavement. J Res Personal. 2001;35(4):424–48. doi: 10.1006/jrpe.2001.2323
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Published
2024-09-04
How to Cite
Amiel Castro R. T., Gardini E., Iliadis S. I., Ehlert U., Kunovac Kallak T., & Skalkidou A. (2024). Personality vulnerability to depression, resilience, and depressive symptoms: epigenetic markers among perinatal women. Upsala Journal of Medical Sciences, 129, e10603. https://doi.org/10.48101/ujms.v129.10603
Section
Original Articles
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