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Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection

The hippocampus participates in spatial navigation and behavioral processes, displays molecular plasticity in response to environmental challenges, and can play a role in neuropsychiatric diseases. The combined effects of inflammatory prenatal and postnatal challenges can disrupt the hippocampal gen...

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Autores principales: Rodriguez-Zas, Sandra L., Southey, Bruce R., Rymut, Haley E., Rund, Laurie A., Johnson, Rodney W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9859158/
https://www.ncbi.nlm.nih.gov/pubmed/36672818
http://dx.doi.org/10.3390/genes14010077
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author Rodriguez-Zas, Sandra L.
Southey, Bruce R.
Rymut, Haley E.
Rund, Laurie A.
Johnson, Rodney W.
author_facet Rodriguez-Zas, Sandra L.
Southey, Bruce R.
Rymut, Haley E.
Rund, Laurie A.
Johnson, Rodney W.
author_sort Rodriguez-Zas, Sandra L.
collection PubMed
description The hippocampus participates in spatial navigation and behavioral processes, displays molecular plasticity in response to environmental challenges, and can play a role in neuropsychiatric diseases. The combined effects of inflammatory prenatal and postnatal challenges can disrupt the hippocampal gene networks and regulatory mechanisms. Using a proven pig model of viral maternal immune activation (MIA) matched to controls and an RNA-sequencing approach, the hippocampal transcriptome was profiled on two-month-old female and male offspring assigned to fasting, mimetic viral, or saline treatments. More than 2600 genes presented single or combined effects (FDR-adjusted p-value < 0.05) of MIA, postnatal stress, or sex. Biological processes and pathways encompassing messenger cyclic adenosine 3′,5′-monophosphate (cAMP) signaling were enriched with genes including gastric inhibitory polypeptide receptor (GIPR) predominantly over-expressed in the MIA-exposed fasting males relative to groups that differed in sex, prenatal or postnatal challenge. While this pattern was amplified in fasting offspring, the postnatal inflammatory challenge appeared to cancel out the effects of the prenatal challenge. The transcription factors C-terminal binding protein 2 (CTBP2), RE1 silencing transcription factor (REST), signal transducer and activator of transcription 1 (STAT1), and SUZ12 polycomb repressive complex 2 subunit were over-represented among the genes impacted by the prenatal and postnatal factors studied. Our results indicate that one environmental challenge can influence the effect of another challenge on the hippocampal transcriptome. These findings can assist in the identification of molecular targets to ameliorate the effects of pre-and post-natal stressors on hippocampal-associated physiology and behavior.
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spelling pubmed-98591582023-01-21 Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection Rodriguez-Zas, Sandra L. Southey, Bruce R. Rymut, Haley E. Rund, Laurie A. Johnson, Rodney W. Genes (Basel) Article The hippocampus participates in spatial navigation and behavioral processes, displays molecular plasticity in response to environmental challenges, and can play a role in neuropsychiatric diseases. The combined effects of inflammatory prenatal and postnatal challenges can disrupt the hippocampal gene networks and regulatory mechanisms. Using a proven pig model of viral maternal immune activation (MIA) matched to controls and an RNA-sequencing approach, the hippocampal transcriptome was profiled on two-month-old female and male offspring assigned to fasting, mimetic viral, or saline treatments. More than 2600 genes presented single or combined effects (FDR-adjusted p-value < 0.05) of MIA, postnatal stress, or sex. Biological processes and pathways encompassing messenger cyclic adenosine 3′,5′-monophosphate (cAMP) signaling were enriched with genes including gastric inhibitory polypeptide receptor (GIPR) predominantly over-expressed in the MIA-exposed fasting males relative to groups that differed in sex, prenatal or postnatal challenge. While this pattern was amplified in fasting offspring, the postnatal inflammatory challenge appeared to cancel out the effects of the prenatal challenge. The transcription factors C-terminal binding protein 2 (CTBP2), RE1 silencing transcription factor (REST), signal transducer and activator of transcription 1 (STAT1), and SUZ12 polycomb repressive complex 2 subunit were over-represented among the genes impacted by the prenatal and postnatal factors studied. Our results indicate that one environmental challenge can influence the effect of another challenge on the hippocampal transcriptome. These findings can assist in the identification of molecular targets to ameliorate the effects of pre-and post-natal stressors on hippocampal-associated physiology and behavior. MDPI 2022-12-26 /pmc/articles/PMC9859158/ /pubmed/36672818 http://dx.doi.org/10.3390/genes14010077 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Rodriguez-Zas, Sandra L.
Southey, Bruce R.
Rymut, Haley E.
Rund, Laurie A.
Johnson, Rodney W.
Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection
title Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection
title_full Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection
title_fullStr Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection
title_full_unstemmed Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection
title_short Hippocampal Changes Elicited by Metabolic and Inflammatory Stressors following Prenatal Maternal Infection
title_sort hippocampal changes elicited by metabolic and inflammatory stressors following prenatal maternal infection
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9859158/
https://www.ncbi.nlm.nih.gov/pubmed/36672818
http://dx.doi.org/10.3390/genes14010077
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