Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches

Augmented maternal care during the first postnatal week promotes life-long stress resilience and improved memory compared with the outcome of routine rearing conditions. Recent evidence suggests that this programming commences with altered synaptic connectivity of stress sensitive hypothalamic neuro...

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Main Authors: Annie Vogel Ciernia, Benjamin I . Laufer, Keith W. Dunaway, Charles E. Mordaunt, Rochelle L. Coulson, Theresa S. Totah, Danielle S. Stolzenberg, Jaime C. Frahm, Akanksha Singh-Taylor, Tallie Z. Baram, Janine M. LaSalle, Dag H. Yasui
Format: Article
Language:English
Published: Taylor & Francis Group 2018-03-01
Series:Epigenetics
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Online Access:http://dx.doi.org/10.1080/15592294.2018.1451720
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author Annie Vogel Ciernia
Benjamin I . Laufer
Keith W. Dunaway
Charles E. Mordaunt
Rochelle L. Coulson
Theresa S. Totah
Danielle S. Stolzenberg
Jaime C. Frahm
Akanksha Singh-Taylor
Tallie Z. Baram
Janine M. LaSalle
Dag H. Yasui
author_facet Annie Vogel Ciernia
Benjamin I . Laufer
Keith W. Dunaway
Charles E. Mordaunt
Rochelle L. Coulson
Theresa S. Totah
Danielle S. Stolzenberg
Jaime C. Frahm
Akanksha Singh-Taylor
Tallie Z. Baram
Janine M. LaSalle
Dag H. Yasui
author_sort Annie Vogel Ciernia
collection DOAJ
description Augmented maternal care during the first postnatal week promotes life-long stress resilience and improved memory compared with the outcome of routine rearing conditions. Recent evidence suggests that this programming commences with altered synaptic connectivity of stress sensitive hypothalamic neurons. However, the epigenomic basis of the long-lived consequences is not well understood. Here, we employed whole-genome bisulfite sequencing (WGBS), RNA-sequencing (RNA-seq), and a multiplex microRNA (miRNA) assay to examine the effects of augmented maternal care on DNA cytosine methylation, gene expression, and miRNA expression. A total of 9,439 differentially methylated regions (DMRs) associated with augmented maternal care were identified in male offspring hypothalamus, as well as a modest but significant decrease in global DNA methylation. Differentially methylated and expressed genes were enriched for functions in neurotransmission, neurodevelopment, protein synthesis, and oxidative phosphorylation, as well as known stress response genes. Twenty prioritized genes were identified as highly relevant to the stress resiliency phenotype. This combined unbiased approach enabled the discovery of novel genes and gene pathways that advance our understanding of the epigenomic mechanisms underlying the effects of maternal care on the developing brain.
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spelling doaj.art-227c1ee5f52246338f871058fd4407332023-09-21T13:09:20ZengTaylor & Francis GroupEpigenetics1559-22941559-23082018-03-0113331833010.1080/15592294.2018.14517201451720Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approachesAnnie Vogel Ciernia0Benjamin I . Laufer1Keith W. Dunaway2Charles E. Mordaunt3Rochelle L. Coulson4Theresa S. Totah5Danielle S. Stolzenberg6Jaime C. Frahm7Akanksha Singh-Taylor8Tallie Z. Baram9Janine M. LaSalle10Dag H. Yasui11University of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaUniversity of CaliforniaAugmented maternal care during the first postnatal week promotes life-long stress resilience and improved memory compared with the outcome of routine rearing conditions. Recent evidence suggests that this programming commences with altered synaptic connectivity of stress sensitive hypothalamic neurons. However, the epigenomic basis of the long-lived consequences is not well understood. Here, we employed whole-genome bisulfite sequencing (WGBS), RNA-sequencing (RNA-seq), and a multiplex microRNA (miRNA) assay to examine the effects of augmented maternal care on DNA cytosine methylation, gene expression, and miRNA expression. A total of 9,439 differentially methylated regions (DMRs) associated with augmented maternal care were identified in male offspring hypothalamus, as well as a modest but significant decrease in global DNA methylation. Differentially methylated and expressed genes were enriched for functions in neurotransmission, neurodevelopment, protein synthesis, and oxidative phosphorylation, as well as known stress response genes. Twenty prioritized genes were identified as highly relevant to the stress resiliency phenotype. This combined unbiased approach enabled the discovery of novel genes and gene pathways that advance our understanding of the epigenomic mechanisms underlying the effects of maternal care on the developing brain.http://dx.doi.org/10.1080/15592294.2018.1451720augmented maternal careepigenomicsdna methylationearly-life stresshypothalamusresilience
spellingShingle Annie Vogel Ciernia
Benjamin I . Laufer
Keith W. Dunaway
Charles E. Mordaunt
Rochelle L. Coulson
Theresa S. Totah
Danielle S. Stolzenberg
Jaime C. Frahm
Akanksha Singh-Taylor
Tallie Z. Baram
Janine M. LaSalle
Dag H. Yasui
Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches
Epigenetics
augmented maternal care
epigenomics
dna methylation
early-life stress
hypothalamus
resilience
title Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches
title_full Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches
title_fullStr Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches
title_full_unstemmed Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches
title_short Experience-dependent neuroplasticity of the developing hypothalamus: integrative epigenomic approaches
title_sort experience dependent neuroplasticity of the developing hypothalamus integrative epigenomic approaches
topic augmented maternal care
epigenomics
dna methylation
early-life stress
hypothalamus
resilience
url http://dx.doi.org/10.1080/15592294.2018.1451720
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