Association of a History of Child Abuse With Impaired Myelination in the Anterior Cingulate Cortex: Convergent Epigenetic, Transcriptional, and Morphological Evidence
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 investiga...
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Published in | The American journal of psychiatry Vol. 174; no. 12; pp. 1185 - 1194 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
American Psychiatric Association
01.12.2017
American Psychiatric Publishing |
Subjects | |
Online Access | Get full text |
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Abstract | 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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AbstractList | 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.
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.
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.
The results suggest that child abuse, in part through epigenetic reprogramming of oligodendrocytes, may lastingly disrupt cortical myelination, a fundamental feature of cerebral connectivity. OBJECTIVEChild 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.METHODPostmortem 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.RESULTSA 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.CONCLUSIONSThe results suggest that child abuse, in part through epigenetic reprogramming of oligodendrocytes, may lastingly disrupt cortical myelination, a fundamental feature of cerebral connectivity. 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. |
Author | Chen, Gang G Chay, Marc-Aurele Yang, Jennie Gasecka, Alicja M’Boutchou, Marie-Noël van Kempen, Léon C Zhang, Tie-Yuan Davoli, Maria Antonietta Bramoullé, Alexandre Prud’homme, Josée Wakid, Marina Vaillancourt, Kathryn Shaw, Meghan Yerko, Volodymyr Côté, Daniel Larivière, Vanessa Barnett-Burns, Sarah Théroux, Jean-François Kim, John J Mechawar, Naguib Lutz, Pierre-Eric Meaney, Michael J Tanti, Arnaud Almeida, Daniel Zhou, Yi Ernst, Carl Turecki, Gustavo |
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References | Maussion, G 2012; 69 Vercelli, A 2014; 24 Liu, J 2012; 15 Rosen, KM 2012; 337 Bredy, TW 2013; 36 Baker-Andresen, D 2013; 36 Ferrand, P 2016; 7 Turecki, G 2005; 30 Fischer, LK 2016; 80 Gutman, DA 2008; 18 Tamayo, P 2005; 102 Spencer, KS 2009; 136 Cohen, P 2002; 59 Bick, J 2015; 169 Lein, ES 2007; 445 Cai, J 2010; 58 Ratnu, VS 2013; 36 Appel, B 2010; 58 Edwards, G 1996; 16 Trabzuni, D 2011; 119 Stroh, T 2015; 118 Gross, JA 2017; 18 Zheng, K 2010; 58 Makinodan, M 2012; 337 Diallo, AB 2014; 15 Milner, R 1996; 16 Zhu, Q 2010; 58 Takada, N 2010; 58 Mi, S 2005; 8 Zhu, T 2015; 169 Suderman, M 2012; 69 Nishiyama, A 2009; 10 Lesage, AD 2005; 162 Dietz, K 2012; 15 Sokolov, BP 2005; 10 Barros, CS 2009; 136 Kendler, KS 2004; 161 Landreth, G 2004; 24 Johnson, JG 2002; 59 Labonté, B 2012; 69 Walker, R 2011; 119 Gasecka, A 2016; 7 Caminiti, R 2012; 22 Pantazatos, SP 2017; 22 Tremblay, RE 2012; 42 Turecki, G 2014; 264 Campbell, JS 2015; 118 Dumais, A 2005; 162 Suzuki, R 2009; 10 Huang, YY 2017; 22 Mugnaini, E 2012; 32 Hawrylycz, MJ 2007; 445 Maciag, D 2015; 65 Le, N 2007; 27 DeLoyht, JM 2012; 15 Jiang, L 2005; 10 Basser, PJ 1995; 8 Purger, D 2014; 344 Poujol, R 2014; 15 Behrens, TE 2008; 18 Samson, JA 2016; 17 Lillie, A 1997; 38 Bélanger, E 2014; 5 Bifulco, A 1997; 38 Wang, JY 2007; 27 Johansen-Berg, H 2008; 18 Komitova, M 2009; 10 Meaney, MJ 2005; 28 Innocenti, GM 2014; 24 Mount, CW 2014; 344 Lutz, PE 2014; 264 Chen, GG 2017; 18 Peter, CJ 2016; 80 Ryu, EJ 2007; 27 Lee, X 2005; 8 Rajkowska, G 2015; 65 Brown, GW 1997; 38 Cleff, C 2016; 7 Wanner, B 2012; 42 Bégin, S 2014; 5 Rosoklija, GB 2017; 22 Nguyen, T 2009; 136 Ao, N 2007; 445 Niven, JE 2012; 32 Caminiti, R 2014; 24 Kuhn, J 2004; 161 Ryten, M 2011; 119 Gibson, EM 2014; 344 Dupont-Therrien, O 2014; 5 Alda, M 2005; 162 Anderson, CM 2016; 17 Chen, GG 2014; 15 Miller, RH 2005; 8 Mahajan, G 2015; 65 Stikov, N 2015; 118 Prescott, CA 2004; 161 Kucenas, S 2010; 58 Aston, C 2005; 10 Mootha, VK 2005; 102 Perge, JA 2012; 32 Streuli, C 1996; 16 Stamoulis, C 2015; 169 Kundakovic, M 2016; 80 Koenigsknecht, J 2004; 24 Ito, S 2012; 337 Gould, MS 2002; 59 Vitaro, F 2012; 42 Teicher, MH 2016; 17 Tomasi, S 2012; 22 Szyf, M 2005; 28 Subramanian, A 2005; 102 Innocenti, GM 2012; 22 Lutz, PE 2017; 18 B20 B21 B22 B25 B26 B27 B28 B29 Cai J (B24) 2010; 58 B30 B31 B10 B32 B11 B33 B12 B34 B13 B35 B14 B36 Turecki G (B3) 2005; 30 B15 B37 B16 B38 B17 B39 B18 B19 Takada N (B23) 2010; 58 B1 B2 B4 B5 B6 B7 B8 B9 B40 |
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Snippet | Objective:Child abuse has devastating and long-lasting consequences, considerably increasing the lifetime risk of negative mental health outcomes such as... Child abuse has devastating and long-lasting consequences, considerably increasing the lifetime risk of negative mental health outcomes such as depression and... Objective: Child abuse has devastating and long-lasting consequences, considerably increasing the lifetime risk of negative mental health outcomes such as... OBJECTIVEChild abuse has devastating and long-lasting consequences, considerably increasing the lifetime risk of negative mental health outcomes such as... |
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SubjectTerms | Adult Survivors of Child Abuse Animals Axons - pathology Brain Case-Control Studies Cell Count Child abuse & neglect Children Deoxyribonucleic acid DNA DNA Methylation Epigenesis, Genetic Epigenetics Gene Expression Genetics Genomics Gyrus Cinguli - metabolism History Humans Life Life Sciences Mental health Morphology Myelin Sheath - metabolism Myelin Sheath - ultrastructure Neurons - metabolism Oligodendroglia - metabolism Rats Research subjects Suicide Technology Transcription factors Transcription, Genetic |
Title | Association of a History of Child Abuse With Impaired Myelination in the Anterior Cingulate Cortex: Convergent Epigenetic, Transcriptional, and Morphological Evidence |
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