Association of a history of child abuse with impaired myelination in the anterior cingulate cortex: convergent epigenetic, transcriptional, and morphological evidence
Open accessAbstract
OBJECTIVE: Child abuse has devastating and long-lasting consequences, considerably increasing the lifetime risk of negative mental health outcomes such as depression and suicide. Yet the neurobiological processes underlying this heightened vulnerability remain poorly understood. The authors investigated the hypothesis that epigenetic, transcriptomic, and cellular adaptations may occur in the anterior cingulate cortex as a function of child abuse. METHOD: Postmortem brain samples from human subjects (N=78) and from a rodent model of the impact of early-life environment (N=24) were analyzed. The human samples were from depressed individuals who died by suicide, with (N=27) or without (N=25) a history of severe child abuse, as well as from psychiatrically healthy control subjects (N=26). Genome-wide DNA methylation and gene expression were investigated using reduced representation bisulfite sequencing and RNA sequencing, respectively. Cell type-specific validation of differentially methylated loci was performed after fluorescence-activated cell sorting of oligodendrocyte and neuronal nuclei. Differential gene expression was validated using NanoString technology. Finally, oligodendrocytes and myelinated axons were analyzed using stereology and coherent anti-Stokes Raman scattering microscopy. RESULTS: A history of child abuse was associated with cell type-specific changes in DNA methylation of oligodendrocyte genes and a global impairment of the myelin-related transcriptional program. These effects were absent in the depressed suicide completers with no history of child abuse, and they were strongly correlated with myelin gene expression changes observed in the animal model. Furthermore, a selective and significant reduction in the thickness of myelin sheaths around small-diameter axons was observed in individuals with history of child abuse. CONCLUSIONS: The results suggest that child abuse, in part through epigenetic reprogramming of oligodendrocytes, may lastingly disrupt cortical myelination, a fundamental feature of cerebral connectivity.
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There was a bidirectional regulation of methylation in the cingulate cortex of those with/without childhood trauma who had depression and died by suicide, with the highest differential methylation occurring in genes related to myelin.
“Similarly, there was a bidirectional regulation of methylation in the cingulate cortex of those with/without childhood trauma who has had depression and died by suicide, with the highest differential methylation occurring in genes that related to myelin (103).”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [103]
The Epigenetic Effects of Child Abuse section reports both increased and decreased methylation, with the three most significant differentially methylated regions in myelin- or oligodendrocyte-related genes. However, that genome-wide comparison was between depressed suicide decedents with a history of child abuse and psychiatrically healthy controls—not between depressed suicide decedents with and without childhood abuse. The latter group was included in targeted follow-up tests of selected genes. (LLM, conf=0.88)
Experimental — accuracy not yet measuredFluorescence-activated cell sorting detected oligodendrocyte-specific DNA methylation changes in MDD postmortem.
“Fluorescence-activated cell sorting detected oligodendrocyte-specific DNA methylation changes in MDD postmortem.79”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [79]
The ‘Epigenetic Effects of Child Abuse’ section reports that FACS-sorted oligodendrocyte nuclei from postmortem samples showed decreased methylation at LINGO3 and POU3F1 in depressed suicide completers with a history of child abuse. The changes were absent in the depressed group without that history, so the claim is too broad if it attributes them to MDD generally. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThree EWAS studies in BD, Borderline PD and MDD have consistently shown changes in DNAm in genes from the POU family that are associated with childhood adversity (POU6F2, POU5F1 and POU3F1 respectively), which are genes involved in myelinisation and neurogenesis.
“For instance, three EWAS studies in BD (Comes et al., 2019), Borderline PD (Arranz et al., 2021) and MDD (Lutz et al., 2017) have consistently shown changes in DNAm in genes from the POU family that are associated with CA (POU6F2, POU5F1 and POU3F1 respectively), which are genes involved in myelinisation and neurogenesis (Online Supplementary Table S1 (SM) – EWAS section).”
From Can epigenetics shine a light on the biological pathways underlying major mental disorders? (2022) · cites this paper as Lutz et al., 2017
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredCell type-specific alterations in methylation of oligodendrocyte genes along with a general disruption of the transcriptional program related to myelin were reported in depressed suicide decedents with childhood maltreatment.
“Cell type-specific alterations in the methylation of DNA in oligodendrocyte genes along with a general disruption of the transcriptional program related to myelin, were reported in depressed suicide decedents with childhood maltreatment.79”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [79]
Impaired myelination in the anterior cingulate cortex in those with childhood abuse was observed.
“Impaired myelination in the anterior cingulate cortex in those with childhood abuse was also observed.”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [79]
Isolated oligodendrocytes from the anterior cingulate cortex of human suicide completers with a history of childhood abuse exhibit decreased CpG methylation of LINGO3 and POU3F1 compared to controls.
“Isolated oligodendrocytes from the anterior cingulate cortex of human suicide completers with a history of childhood abuse exhibited decreased CpG methylation of myelination-regulating genes, specifically, leucine-rich repeat and immunoglobulin-like domain-containing nogo receptor- interacting protein 3 (LINGO3) and POU class 3 homeobox 1 (POU3F1), compared to controls who died of non-suicide caus”
From Cell-type-specific epigenetic effects of early life stress on the brain (2022) · cites this paper as [139]
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“Similarly, there was a bidirectional regulation of methylation in the cingulate cortex of those with/without childhood trauma who has had depression and died by suicide, with the highest differential methylation occurring in genes that related to myelin (103).”
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“79 Consistent with the consideration Fig.”
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“…children Differently methylated between CA + and CA- POU6F2 Comes et al. (2020) EWAS Blood BD ↑CA-> ↓POU6F2 POU5F1 Arranz et al. (2021) EWAS Blood Borderline PD ↑CA-> ↓POU5F1 POU3F1 Lutz et al. (2017) EWAS PMB Depression ↑CA-> ↓POU3F1 CUX1* Osborne et al. (2020) EWAS Blood General population…”
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- Authors
- Lutz, P.-E., Tanti, A., Gasecka, A., Barnett-Burns, S., Kim, J. J., Zhou, Y., Chen, G. G., Wakid, M., Shaw, M., Almeida, D., Chay, M.-A., Yang, J., Larivière, V., M’Boutchou, M.-N., van Kempen, L. C., Yerko, V., Prud’homme, J., Davoli, M. A., Vaillancourt, K., Théroux, J.-F., Bramoullé, A., Zhang, T.-Y., Meaney, M. J., Ernst, C., Côté, D., Mechawar, N., & Turecki, G.
- Affiliations
- From the McGill Group for Suicide Studies, Douglas Mental Health University Institute, McGill University, Montreal; Institut Universitaire en Santé Mentale de Québec, Quebec; Centre d’Optique, Photonique, et Laser, Université Laval, Quebec; Segal Cancer Centre, Lady Davis Institute, Jewish General Hospital, McGill University, Montreal; the Department of Psychiatry, McGill University, Montreal; the Sackler Program for Epigenetics and Psychobiology at McGill University and the Ludmer Centre for...
- Douglas Mental Health University Institute (CA)
- Unilever (United Kingdom) (GB)
- ORCID
- Venue
- American Journal of Psychiatry
- Published
- 2017-12-01
- Volume
- 174
- Issue
- 12
- Pages
- 1185-1194
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- OpenAlex
- W2740366507
- Cited by
- 203
- References
- 39
- Citations by year
- 2026: 13 · 2025: 25 · 2024: 16 · 2023: 17 · 2022: 25 · 2021: 34 · 2020: 17 · 2019: 15 · 2018: 34 · 2017: 5 · 2015: 1
- FWCI
- 24.02
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- American Foundation for Suicide Prevention
- Pfizer
- National Alliance for Research on Schizophrenia and Depression
- Fondation pour la Recherche Médicale
- Fondation Fyssen
- National Institutes of Health
- Canadian Institutes of Health Research (MOP119430, MOP11260, MOP93775, MOP119429, 111022_1, MOP93775, MOP11260, MOP119429, and MOP119430, FDN148374)
- Fonds de Recherche du Québec - Santé
- National Institute on Drug Abuse (R01DA033684)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- child abuse, anterior cingulate cortex, myelination, oligodendrocytes, DNA methylation, epigenetic reprogramming, depression, suicide, myelin gene expression, myelin thickness, early life environment
- MeSH terms
- Animals, Axons, Cell Count, Gyrus Cinguli, Humans, Myelin Sheath, Neurons, Oligodendroglia, Transcription, Genetic, Gene Expression, Case-Control Studies, DNA Methylation, Epigenesis, Genetic, Rats, Adult Survivors of Child Abuse
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