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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Veröffentlicht in:Neurobiology of aging 2013, Vol.34 (1), p.319-337
Hauptverfasser: 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
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container_issue 1
container_start_page 319
container_title Neurobiology of aging
container_volume 34
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 &amp; 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. 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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><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 &amp; 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 &amp; 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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