Behavioral and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice
Abstract Epidemiological evidence implies a role for chronic stress and stress-related disorders in the etiopathogenesis of sporadic Alzheimer's disease (AD). Although chronic stress exposure during various stages of life has been shown to exacerbate AD-related cognitive deficits and neuropatho...
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creator | Sierksma, Annerieke S.R Prickaerts, Jos Chouliaras, Leonidas Rostamian, Somayeh Delbroek, Lore Rutten, Bart P.F Steinbusch, Harry W.M van den Hove, Daniel L.A |
description | Abstract Epidemiological evidence implies a role for chronic stress and stress-related disorders in the etiopathogenesis of sporadic Alzheimer's disease (AD). Although chronic stress exposure during various stages of life has been shown to exacerbate AD-related cognitive deficits and neuropathology in AD mouse models, the role of stress exposure during the prenatal period on AD development and progression remained to be investigated. The present study therefore explored the effects of prenatal maternal stress (PMS) in both male and female APPswe/PS1dE9 mouse offspring in terms of cognition, affect, and AD-related neuropathology. As prenatal perturbations are likely to mediate their effects via alterations in epigenetic regulation, changes in hippocampal DNA methyltransferase 3a, 5-methylcytosine and 5-hydroxymethylcytosine levels were assessed as underlying mechanisms. Repetitive restraint stress during the first week of gestation exerted a sex-dependent effect, with male PMS mice showing spatial memory deficits and a blunted hypothalamus-pituitary-adrenal axis response, while female PMS mice showed improved spatial memory performance, increased depressive-like behavior, as well as a decrease in hippocampal plaque load. In addition, sex differences were observed among APPswe/PS1dE9 mice, independent of PMS (i.e., female mice showed impaired spatial memory performance, higher hippocampal plaque load, altered amyloid precursor protein processing in the CA3 and lower DNA methyltransferase 3a immunoreactivity in the dentate gyrus when compared with male mice of the same age). In conclusion, PMS exposure impacts on the behavioral phenotype and neuropathology of APPswe/PS1dE9 mice. Moreover, given the remarkable sex differences observed, one should not overlook the impact of sex-specific responses to environmental exposures when investigating gene-environment interactions in AD. |
doi_str_mv | 10.1016/j.neurobiolaging.2012.05.012 |
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Although chronic stress exposure during various stages of life has been shown to exacerbate AD-related cognitive deficits and neuropathology in AD mouse models, the role of stress exposure during the prenatal period on AD development and progression remained to be investigated. The present study therefore explored the effects of prenatal maternal stress (PMS) in both male and female APPswe/PS1dE9 mouse offspring in terms of cognition, affect, and AD-related neuropathology. As prenatal perturbations are likely to mediate their effects via alterations in epigenetic regulation, changes in hippocampal DNA methyltransferase 3a, 5-methylcytosine and 5-hydroxymethylcytosine levels were assessed as underlying mechanisms. Repetitive restraint stress during the first week of gestation exerted a sex-dependent effect, with male PMS mice showing spatial memory deficits and a blunted hypothalamus-pituitary-adrenal axis response, while female PMS mice showed improved spatial memory performance, increased depressive-like behavior, as well as a decrease in hippocampal plaque load. In addition, sex differences were observed among APPswe/PS1dE9 mice, independent of PMS (i.e., female mice showed impaired spatial memory performance, higher hippocampal plaque load, altered amyloid precursor protein processing in the CA3 and lower DNA methyltransferase 3a immunoreactivity in the dentate gyrus when compared with male mice of the same age). In conclusion, PMS exposure impacts on the behavioral phenotype and neuropathology of APPswe/PS1dE9 mice. Moreover, given the remarkable sex differences observed, one should not overlook the impact of sex-specific responses to environmental exposures when investigating gene-environment interactions in AD.</description><identifier>ISSN: 0197-4580</identifier><identifier>EISSN: 1558-1497</identifier><identifier>DOI: 10.1016/j.neurobiolaging.2012.05.012</identifier><identifier>PMID: 22738723</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>5-hydroxymethylcytidine (5hmc) ; 5-methylcytidine (5mC) ; 5-Methylcytosine - metabolism ; Aging ; Alzheimer Disease - complications ; Alzheimer Disease - genetics ; Alzheimer's disease ; Amyloid beta-Protein Precursor - genetics ; Amyloid precursor protein ; Animal models ; Animals ; APPswe ; Behavioral Symptoms - etiology ; Benzofurans ; Cognition Disorders - etiology ; Cognitive ability ; Cytosine - analogs & derivatives ; Cytosine - metabolism ; Dentate gyrus ; Disease Models, Animal ; DNA (Cytosine-5-)-Methyltransferases - metabolism ; DNA hydroxymethylation ; DNA methylation ; DNA methyltransferase ; Epigenetics ; Female ; Gestation ; Hippocampus ; Hippocampus - enzymology ; Humans ; Immunoreactivity ; Internal Medicine ; Male ; Memory Disorders - etiology ; Mice ; Mice, Transgenic ; Nervous system ; Neurodegenerative diseases ; Neurology ; Neuropathology ; Plaques ; Pregnancy ; Prenatal experience ; Prenatal Exposure Delayed Effects - physiopathology ; Prenatal stress ; Presenilin-1 - genetics ; PS1dE9 ; Quinolines ; Sex differences ; Sexual dimorphism ; Space Perception - physiology ; spatial memory ; Stress ; Stress, Psychological - complications ; Stress, Psychological - pathology</subject><ispartof>Neurobiology of aging, 2013, Vol.34 (1), p.319-337</ispartof><rights>Elsevier Inc.</rights><rights>2013 Elsevier Inc.</rights><rights>Copyright © 2013 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-3b61990263c74b7ecace2ad64bc871d266aa6b003cb528c23f65b1ea371430fc3</citedby><cites>FETCH-LOGICAL-c474t-3b61990263c74b7ecace2ad64bc871d266aa6b003cb528c23f65b1ea371430fc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0197458012002990$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,4010,27900,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22738723$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sierksma, Annerieke S.R</creatorcontrib><creatorcontrib>Prickaerts, Jos</creatorcontrib><creatorcontrib>Chouliaras, Leonidas</creatorcontrib><creatorcontrib>Rostamian, Somayeh</creatorcontrib><creatorcontrib>Delbroek, Lore</creatorcontrib><creatorcontrib>Rutten, Bart P.F</creatorcontrib><creatorcontrib>Steinbusch, Harry W.M</creatorcontrib><creatorcontrib>van den Hove, Daniel L.A</creatorcontrib><title>Behavioral and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice</title><title>Neurobiology of aging</title><addtitle>Neurobiol Aging</addtitle><description>Abstract Epidemiological evidence implies a role for chronic stress and stress-related disorders in the etiopathogenesis of sporadic Alzheimer's disease (AD). Although chronic stress exposure during various stages of life has been shown to exacerbate AD-related cognitive deficits and neuropathology in AD mouse models, the role of stress exposure during the prenatal period on AD development and progression remained to be investigated. The present study therefore explored the effects of prenatal maternal stress (PMS) in both male and female APPswe/PS1dE9 mouse offspring in terms of cognition, affect, and AD-related neuropathology. As prenatal perturbations are likely to mediate their effects via alterations in epigenetic regulation, changes in hippocampal DNA methyltransferase 3a, 5-methylcytosine and 5-hydroxymethylcytosine levels were assessed as underlying mechanisms. Repetitive restraint stress during the first week of gestation exerted a sex-dependent effect, with male PMS mice showing spatial memory deficits and a blunted hypothalamus-pituitary-adrenal axis response, while female PMS mice showed improved spatial memory performance, increased depressive-like behavior, as well as a decrease in hippocampal plaque load. In addition, sex differences were observed among APPswe/PS1dE9 mice, independent of PMS (i.e., female mice showed impaired spatial memory performance, higher hippocampal plaque load, altered amyloid precursor protein processing in the CA3 and lower DNA methyltransferase 3a immunoreactivity in the dentate gyrus when compared with male mice of the same age). In conclusion, PMS exposure impacts on the behavioral phenotype and neuropathology of APPswe/PS1dE9 mice. Moreover, given the remarkable sex differences observed, one should not overlook the impact of sex-specific responses to environmental exposures when investigating gene-environment interactions in AD.</description><subject>5-hydroxymethylcytidine (5hmc)</subject><subject>5-methylcytidine (5mC)</subject><subject>5-Methylcytosine - metabolism</subject><subject>Aging</subject><subject>Alzheimer Disease - complications</subject><subject>Alzheimer Disease - genetics</subject><subject>Alzheimer's disease</subject><subject>Amyloid beta-Protein Precursor - genetics</subject><subject>Amyloid precursor protein</subject><subject>Animal models</subject><subject>Animals</subject><subject>APPswe</subject><subject>Behavioral Symptoms - etiology</subject><subject>Benzofurans</subject><subject>Cognition Disorders - etiology</subject><subject>Cognitive ability</subject><subject>Cytosine - analogs & derivatives</subject><subject>Cytosine - metabolism</subject><subject>Dentate gyrus</subject><subject>Disease Models, Animal</subject><subject>DNA (Cytosine-5-)-Methyltransferases - metabolism</subject><subject>DNA hydroxymethylation</subject><subject>DNA methylation</subject><subject>DNA methyltransferase</subject><subject>Epigenetics</subject><subject>Female</subject><subject>Gestation</subject><subject>Hippocampus</subject><subject>Hippocampus - enzymology</subject><subject>Humans</subject><subject>Immunoreactivity</subject><subject>Internal Medicine</subject><subject>Male</subject><subject>Memory Disorders - etiology</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Nervous system</subject><subject>Neurodegenerative diseases</subject><subject>Neurology</subject><subject>Neuropathology</subject><subject>Plaques</subject><subject>Pregnancy</subject><subject>Prenatal experience</subject><subject>Prenatal Exposure Delayed Effects - physiopathology</subject><subject>Prenatal stress</subject><subject>Presenilin-1 - genetics</subject><subject>PS1dE9</subject><subject>Quinolines</subject><subject>Sex differences</subject><subject>Sexual dimorphism</subject><subject>Space Perception - physiology</subject><subject>spatial memory</subject><subject>Stress</subject><subject>Stress, Psychological - complications</subject><subject>Stress, Psychological - pathology</subject><issn>0197-4580</issn><issn>1558-1497</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNUk1v1DAUtBCILqV_AeXAgUvS54_YiYSQ2qoFpEpdqfRsOc7L1ksSL3ZS6L_H6ZZKcKGneXqamSfNPELeUygoUHm8LUacg2-c783GjZuCAWUFlEWCF2RFy7LKqajVS7ICWqtclBUckDcxbgFACSVfkwPGFK8U4ytye4q35s75YPrMjG325O03zqYddh3aKWa-y3YBRzOlXZwCxpjhr52Pc8DMjdlgenzQd_gwnqzX8Scer69pe15ng7P4lrzqTB_x6BEPyc3F-bezL_nl1eevZyeXuRVKTDlvJK1rYJJbJRqF1lhkppWisZWiLZPSGNkAcNuUrLKMd7JsKBquqODQWX5IPux9d8H_mDFOenDRYt-bEf0cNWWlUkKqiv2fShmTyVZCon7cU23wMQbs9C64wYR7TUEvteit_rsWvdSiodQJkvzd46W5GbB9Ev_pIREu9gRM0dw5DDpah6PF1oWUv269e-6lT_8Y2d6NS5Xf8R7j1s9hTPFrqmPS6OvlRZYPoQyApeD5b_lSu9s</recordid><startdate>2013</startdate><enddate>2013</enddate><creator>Sierksma, Annerieke S.R</creator><creator>Prickaerts, Jos</creator><creator>Chouliaras, Leonidas</creator><creator>Rostamian, Somayeh</creator><creator>Delbroek, Lore</creator><creator>Rutten, Bart P.F</creator><creator>Steinbusch, Harry W.M</creator><creator>van den Hove, Daniel L.A</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7TK</scope></search><sort><creationdate>2013</creationdate><title>Behavioral and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice</title><author>Sierksma, Annerieke S.R ; Prickaerts, Jos ; Chouliaras, Leonidas ; Rostamian, Somayeh ; Delbroek, Lore ; Rutten, Bart P.F ; Steinbusch, Harry W.M ; van den Hove, Daniel L.A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-3b61990263c74b7ecace2ad64bc871d266aa6b003cb528c23f65b1ea371430fc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>5-hydroxymethylcytidine (5hmc)</topic><topic>5-methylcytidine (5mC)</topic><topic>5-Methylcytosine - metabolism</topic><topic>Aging</topic><topic>Alzheimer Disease - complications</topic><topic>Alzheimer Disease - genetics</topic><topic>Alzheimer's disease</topic><topic>Amyloid beta-Protein Precursor - genetics</topic><topic>Amyloid precursor protein</topic><topic>Animal models</topic><topic>Animals</topic><topic>APPswe</topic><topic>Behavioral Symptoms - etiology</topic><topic>Benzofurans</topic><topic>Cognition Disorders - etiology</topic><topic>Cognitive ability</topic><topic>Cytosine - analogs & derivatives</topic><topic>Cytosine - metabolism</topic><topic>Dentate gyrus</topic><topic>Disease Models, Animal</topic><topic>DNA (Cytosine-5-)-Methyltransferases - metabolism</topic><topic>DNA hydroxymethylation</topic><topic>DNA methylation</topic><topic>DNA methyltransferase</topic><topic>Epigenetics</topic><topic>Female</topic><topic>Gestation</topic><topic>Hippocampus</topic><topic>Hippocampus - enzymology</topic><topic>Humans</topic><topic>Immunoreactivity</topic><topic>Internal Medicine</topic><topic>Male</topic><topic>Memory Disorders - etiology</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>Nervous system</topic><topic>Neurodegenerative diseases</topic><topic>Neurology</topic><topic>Neuropathology</topic><topic>Plaques</topic><topic>Pregnancy</topic><topic>Prenatal experience</topic><topic>Prenatal Exposure Delayed Effects - physiopathology</topic><topic>Prenatal stress</topic><topic>Presenilin-1 - genetics</topic><topic>PS1dE9</topic><topic>Quinolines</topic><topic>Sex differences</topic><topic>Sexual dimorphism</topic><topic>Space Perception - physiology</topic><topic>spatial memory</topic><topic>Stress</topic><topic>Stress, Psychological - complications</topic><topic>Stress, Psychological - pathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sierksma, Annerieke S.R</creatorcontrib><creatorcontrib>Prickaerts, Jos</creatorcontrib><creatorcontrib>Chouliaras, Leonidas</creatorcontrib><creatorcontrib>Rostamian, Somayeh</creatorcontrib><creatorcontrib>Delbroek, Lore</creatorcontrib><creatorcontrib>Rutten, Bart P.F</creatorcontrib><creatorcontrib>Steinbusch, Harry W.M</creatorcontrib><creatorcontrib>van den Hove, Daniel L.A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><jtitle>Neurobiology of aging</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sierksma, Annerieke S.R</au><au>Prickaerts, Jos</au><au>Chouliaras, Leonidas</au><au>Rostamian, Somayeh</au><au>Delbroek, Lore</au><au>Rutten, Bart P.F</au><au>Steinbusch, Harry W.M</au><au>van den Hove, Daniel L.A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Behavioral and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice</atitle><jtitle>Neurobiology of aging</jtitle><addtitle>Neurobiol Aging</addtitle><date>2013</date><risdate>2013</risdate><volume>34</volume><issue>1</issue><spage>319</spage><epage>337</epage><pages>319-337</pages><issn>0197-4580</issn><eissn>1558-1497</eissn><abstract>Abstract Epidemiological evidence implies a role for chronic stress and stress-related disorders in the etiopathogenesis of sporadic Alzheimer's disease (AD). Although chronic stress exposure during various stages of life has been shown to exacerbate AD-related cognitive deficits and neuropathology in AD mouse models, the role of stress exposure during the prenatal period on AD development and progression remained to be investigated. The present study therefore explored the effects of prenatal maternal stress (PMS) in both male and female APPswe/PS1dE9 mouse offspring in terms of cognition, affect, and AD-related neuropathology. As prenatal perturbations are likely to mediate their effects via alterations in epigenetic regulation, changes in hippocampal DNA methyltransferase 3a, 5-methylcytosine and 5-hydroxymethylcytosine levels were assessed as underlying mechanisms. Repetitive restraint stress during the first week of gestation exerted a sex-dependent effect, with male PMS mice showing spatial memory deficits and a blunted hypothalamus-pituitary-adrenal axis response, while female PMS mice showed improved spatial memory performance, increased depressive-like behavior, as well as a decrease in hippocampal plaque load. In addition, sex differences were observed among APPswe/PS1dE9 mice, independent of PMS (i.e., female mice showed impaired spatial memory performance, higher hippocampal plaque load, altered amyloid precursor protein processing in the CA3 and lower DNA methyltransferase 3a immunoreactivity in the dentate gyrus when compared with male mice of the same age). In conclusion, PMS exposure impacts on the behavioral phenotype and neuropathology of APPswe/PS1dE9 mice. Moreover, given the remarkable sex differences observed, one should not overlook the impact of sex-specific responses to environmental exposures when investigating gene-environment interactions in AD.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22738723</pmid><doi>10.1016/j.neurobiolaging.2012.05.012</doi><tpages>19</tpages></addata></record> |
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subjects | 5-hydroxymethylcytidine (5hmc) 5-methylcytidine (5mC) 5-Methylcytosine - metabolism Aging Alzheimer Disease - complications Alzheimer Disease - genetics Alzheimer's disease Amyloid beta-Protein Precursor - genetics Amyloid precursor protein Animal models Animals APPswe Behavioral Symptoms - etiology Benzofurans Cognition Disorders - etiology Cognitive ability Cytosine - analogs & derivatives Cytosine - metabolism Dentate gyrus Disease Models, Animal DNA (Cytosine-5-)-Methyltransferases - metabolism DNA hydroxymethylation DNA methylation DNA methyltransferase Epigenetics Female Gestation Hippocampus Hippocampus - enzymology Humans Immunoreactivity Internal Medicine Male Memory Disorders - etiology Mice Mice, Transgenic Nervous system Neurodegenerative diseases Neurology Neuropathology Plaques Pregnancy Prenatal experience Prenatal Exposure Delayed Effects - physiopathology Prenatal stress Presenilin-1 - genetics PS1dE9 Quinolines Sex differences Sexual dimorphism Space Perception - physiology spatial memory Stress Stress, Psychological - complications Stress, Psychological - pathology |
title | Behavioral and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice |
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