Developmental exposure to 50 parts-per-billion arsenic influences histone modifications and associated epigenetic machinery in a region- and sex-specific manner in the adult mouse brain
Epidemiological studies report that arsenic exposure via drinking water adversely impacts cognitive development in children and, in adults, can lead to greater psychiatric disease susceptibility, among other conditions. While it is known that arsenic toxicity has a profound effect on the epigenetic...
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| description | Epidemiological studies report that arsenic exposure via drinking water adversely impacts cognitive development in children and, in adults, can lead to greater psychiatric disease susceptibility, among other conditions. While it is known that arsenic toxicity has a profound effect on the epigenetic landscape, very few studies have investigated its effects on chromatin architecture in the brain. We have previously demonstrated that exposure to a low level of arsenic (50ppb) during all three trimesters of fetal/neonatal development induces deficits in adult hippocampal neurogenesis in the dentate gyrus (DG), depressive-like symptoms, and alterations in gene expression in the adult mouse brain. As epigenetic processes control these outcomes, here we assess the impact of our developmental arsenic exposure (DAE) paradigm on global histone posttranslational modifications and associated chromatin-modifying proteins in the dentate gyrus and frontal cortex (FC) of adult male and female mice. DAE influenced histone 3K4 trimethylation with increased levels in the male DG and FC and decreased levels in the female DG (no change in female FC). The histone methyltransferase MLL exhibited a similar sex- and region-specific expression profile as H3K4me3 levels, while histone demethylase KDM5B expression trended in the opposite direction. DAE increased histone 3K9 acetylation levels in the male DG along with histone acetyltransferase (HAT) expression of GCN5 and decreased H3K9ac levels in the male FC along with decreased HAT expression of GCN5 and PCAF. DAE decreased expression of histone deacetylase enzymes HDAC1 and HDAC2, which were concurrent with increased H3K9ac levels but only in the female DG. Levels of H3 and H3K9me3 were not influenced by DAE in either brain region of either sex. These findings suggest that exposure to a low, environmentally relevant level of arsenic during development leads to long-lasting changes in histone methylation and acetylation in the adult brain due to aberrant expression of epigenetic machinery based on region and sex.
•Brain tissue from adult mice with developmental arsenic exposure (DAE) was used.•DAE impacted histone methylation and associated methyltransferases based on sex.•DAE differentially altered histone acetylation based on brain region.•DAE altered HATs in males and HDACs in females.•Epigenetic modifier expression correlated with the associated histone modification. |
| doi_str_mv | 10.1016/j.taap.2015.07.013 |
| format | Article |
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•Brain tissue from adult mice with developmental arsenic exposure (DAE) was used.•DAE impacted histone methylation and associated methyltransferases based on sex.•DAE differentially altered histone acetylation based on brain region.•DAE altered HATs in males and HDACs in females.•Epigenetic modifier expression correlated with the associated histone modification.</description><identifier>ISSN: 0041-008X</identifier><identifier>EISSN: 1096-0333</identifier><identifier>DOI: 10.1016/j.taap.2015.07.013</identifier><identifier>PMID: 26193056</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>60 APPLIED LIFE SCIENCES ; ACETYLATION ; Acetyltransferase ; Age Factors ; Animals ; Animals, Newborn ; Arsenates - toxicity ; ARSENIC ; BRAIN ; CHROMATIN ; Chromatin Assembly and Disassembly - drug effects ; Dealkylation ; Dentate Gyrus - drug effects ; Dentate Gyrus - metabolism ; DNA-Binding Proteins - metabolism ; DRINKING WATER ; Epigenesis, Genetic ; Female ; Frontal Lobe - drug effects ; Frontal Lobe - metabolism ; Gene Expression Regulation ; Gestational Age ; Histone ; Histone Deacetylase 1 - metabolism ; Histone Deacetylase 2 - metabolism ; Histone-Lysine N-Methyltransferase - metabolism ; HISTONES ; Histones - metabolism ; Jumonji Domain-Containing Histone Demethylases - metabolism ; Male ; METHYL TRANSFERASES ; METHYLATION ; Methyltransferase ; MICE ; Mice, Inbred C57BL ; MODIFICATIONS ; Myeloid-Lymphoid Leukemia Protein - metabolism ; p300-CBP Transcription Factors - metabolism ; Pregnancy ; Prenatal Exposure Delayed Effects ; Sex ; Sex Factors ; Water Pollutants, Chemical - toxicity</subject><ispartof>Toxicology and applied pharmacology, 2015-10, Vol.288 (1), p.40-51</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c516t-c7a7f6d077d2169f146b1c85171cada213618903a87ff81ca0f436cba442c5763</citedby><cites>FETCH-LOGICAL-c516t-c7a7f6d077d2169f146b1c85171cada213618903a87ff81ca0f436cba442c5763</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0041008X15300399$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26193056$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/22687765$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Tyler, Christina R.</creatorcontrib><creatorcontrib>Hafez, Alexander K.</creatorcontrib><creatorcontrib>Solomon, Elizabeth R.</creatorcontrib><creatorcontrib>Allan, Andrea M.</creatorcontrib><title>Developmental exposure to 50 parts-per-billion arsenic influences histone modifications and associated epigenetic machinery in a region- and sex-specific manner in the adult mouse brain</title><title>Toxicology and applied pharmacology</title><addtitle>Toxicol Appl Pharmacol</addtitle><description>Epidemiological studies report that arsenic exposure via drinking water adversely impacts cognitive development in children and, in adults, can lead to greater psychiatric disease susceptibility, among other conditions. While it is known that arsenic toxicity has a profound effect on the epigenetic landscape, very few studies have investigated its effects on chromatin architecture in the brain. We have previously demonstrated that exposure to a low level of arsenic (50ppb) during all three trimesters of fetal/neonatal development induces deficits in adult hippocampal neurogenesis in the dentate gyrus (DG), depressive-like symptoms, and alterations in gene expression in the adult mouse brain. As epigenetic processes control these outcomes, here we assess the impact of our developmental arsenic exposure (DAE) paradigm on global histone posttranslational modifications and associated chromatin-modifying proteins in the dentate gyrus and frontal cortex (FC) of adult male and female mice. DAE influenced histone 3K4 trimethylation with increased levels in the male DG and FC and decreased levels in the female DG (no change in female FC). The histone methyltransferase MLL exhibited a similar sex- and region-specific expression profile as H3K4me3 levels, while histone demethylase KDM5B expression trended in the opposite direction. DAE increased histone 3K9 acetylation levels in the male DG along with histone acetyltransferase (HAT) expression of GCN5 and decreased H3K9ac levels in the male FC along with decreased HAT expression of GCN5 and PCAF. DAE decreased expression of histone deacetylase enzymes HDAC1 and HDAC2, which were concurrent with increased H3K9ac levels but only in the female DG. Levels of H3 and H3K9me3 were not influenced by DAE in either brain region of either sex. These findings suggest that exposure to a low, environmentally relevant level of arsenic during development leads to long-lasting changes in histone methylation and acetylation in the adult brain due to aberrant expression of epigenetic machinery based on region and sex.
•Brain tissue from adult mice with developmental arsenic exposure (DAE) was used.•DAE impacted histone methylation and associated methyltransferases based on sex.•DAE differentially altered histone acetylation based on brain region.•DAE altered HATs in males and HDACs in females.•Epigenetic modifier expression correlated with the associated histone modification.</description><subject>60 APPLIED LIFE SCIENCES</subject><subject>ACETYLATION</subject><subject>Acetyltransferase</subject><subject>Age Factors</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Arsenates - toxicity</subject><subject>ARSENIC</subject><subject>BRAIN</subject><subject>CHROMATIN</subject><subject>Chromatin Assembly and Disassembly - drug effects</subject><subject>Dealkylation</subject><subject>Dentate Gyrus - drug effects</subject><subject>Dentate Gyrus - metabolism</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>DRINKING WATER</subject><subject>Epigenesis, Genetic</subject><subject>Female</subject><subject>Frontal Lobe - drug effects</subject><subject>Frontal Lobe - metabolism</subject><subject>Gene Expression Regulation</subject><subject>Gestational Age</subject><subject>Histone</subject><subject>Histone Deacetylase 1 - metabolism</subject><subject>Histone Deacetylase 2 - metabolism</subject><subject>Histone-Lysine N-Methyltransferase - metabolism</subject><subject>HISTONES</subject><subject>Histones - metabolism</subject><subject>Jumonji Domain-Containing Histone Demethylases - metabolism</subject><subject>Male</subject><subject>METHYL TRANSFERASES</subject><subject>METHYLATION</subject><subject>Methyltransferase</subject><subject>MICE</subject><subject>Mice, Inbred C57BL</subject><subject>MODIFICATIONS</subject><subject>Myeloid-Lymphoid Leukemia Protein - metabolism</subject><subject>p300-CBP Transcription Factors - metabolism</subject><subject>Pregnancy</subject><subject>Prenatal Exposure Delayed Effects</subject><subject>Sex</subject><subject>Sex Factors</subject><subject>Water Pollutants, Chemical - toxicity</subject><issn>0041-008X</issn><issn>1096-0333</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9ks1u1DAUhSMEotPCC7BAltiwyXCdHzuREFJVKCBVYgMSO-vGuZnxKLGD7YzaR-PtcJhSwYaVJfs75_74ZNkLDlsOXLw5bCPivC2A11uQW-Dlo2zDoRU5lGX5ONsAVDwHaL6fZechHACgrSr-NDsrBG9LqMUm-_mejjS6eSIbcWR0O7uweGLRsRrYjD6GfCafd2YcjbMMfSBrNDN2GBeymgLbmxCdJTa53gxGY0xcYGh7hiE4bTBSz2g2O7IUk3RCvTeW_F0yYcg87ZIg_y0IdJuHmfTqkzibqBWKe2LYL2NMNZZArPNo7LPsyYBjoOf350X27frD16tP-c2Xj5-vLm9yXXMRcy1RDqIHKfuCi3bglei4bmouucYeC14K3rRQYiOHoUl3MFSl0B1WVaFrKcqL7N3Jd166iXqdFuVxVLM3E_o75dCof1-s2audO6qqlslXJoNXJwMXolFBm0h6r10aTkdVFKKRUtSJen1fxrsfC4WoJhM0jSNaSkMrLmtepCnq1bA4odq7EDwND81wUGsy1EGtyVBrMhRIlZKRRC__HuNB8icKCXh7Aigt82jIr62uP9wbv3baO_M__190Os8F</recordid><startdate>20151001</startdate><enddate>20151001</enddate><creator>Tyler, Christina R.</creator><creator>Hafez, Alexander K.</creator><creator>Solomon, Elizabeth R.</creator><creator>Allan, Andrea M.</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>7TK</scope><scope>7U7</scope><scope>C1K</scope><scope>OTOTI</scope><scope>5PM</scope></search><sort><creationdate>20151001</creationdate><title>Developmental exposure to 50 parts-per-billion arsenic influences histone modifications and associated epigenetic machinery in a region- and sex-specific manner in the adult mouse brain</title><author>Tyler, Christina R. ; Hafez, Alexander K. ; Solomon, Elizabeth R. ; Allan, Andrea M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c516t-c7a7f6d077d2169f146b1c85171cada213618903a87ff81ca0f436cba442c5763</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>60 APPLIED LIFE SCIENCES</topic><topic>ACETYLATION</topic><topic>Acetyltransferase</topic><topic>Age Factors</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Arsenates - toxicity</topic><topic>ARSENIC</topic><topic>BRAIN</topic><topic>CHROMATIN</topic><topic>Chromatin Assembly and Disassembly - drug effects</topic><topic>Dealkylation</topic><topic>Dentate Gyrus - drug effects</topic><topic>Dentate Gyrus - metabolism</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>DRINKING WATER</topic><topic>Epigenesis, Genetic</topic><topic>Female</topic><topic>Frontal Lobe - drug effects</topic><topic>Frontal Lobe - metabolism</topic><topic>Gene Expression Regulation</topic><topic>Gestational Age</topic><topic>Histone</topic><topic>Histone Deacetylase 1 - metabolism</topic><topic>Histone Deacetylase 2 - metabolism</topic><topic>Histone-Lysine N-Methyltransferase - metabolism</topic><topic>HISTONES</topic><topic>Histones - metabolism</topic><topic>Jumonji Domain-Containing Histone Demethylases - metabolism</topic><topic>Male</topic><topic>METHYL TRANSFERASES</topic><topic>METHYLATION</topic><topic>Methyltransferase</topic><topic>MICE</topic><topic>Mice, Inbred C57BL</topic><topic>MODIFICATIONS</topic><topic>Myeloid-Lymphoid Leukemia Protein - metabolism</topic><topic>p300-CBP Transcription Factors - metabolism</topic><topic>Pregnancy</topic><topic>Prenatal Exposure Delayed Effects</topic><topic>Sex</topic><topic>Sex Factors</topic><topic>Water Pollutants, Chemical - toxicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tyler, Christina R.</creatorcontrib><creatorcontrib>Hafez, Alexander K.</creatorcontrib><creatorcontrib>Solomon, Elizabeth R.</creatorcontrib><creatorcontrib>Allan, Andrea M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Toxicology and applied pharmacology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tyler, Christina R.</au><au>Hafez, Alexander K.</au><au>Solomon, Elizabeth R.</au><au>Allan, Andrea M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Developmental exposure to 50 parts-per-billion arsenic influences histone modifications and associated epigenetic machinery in a region- and sex-specific manner in the adult mouse brain</atitle><jtitle>Toxicology and applied pharmacology</jtitle><addtitle>Toxicol Appl Pharmacol</addtitle><date>2015-10-01</date><risdate>2015</risdate><volume>288</volume><issue>1</issue><spage>40</spage><epage>51</epage><pages>40-51</pages><issn>0041-008X</issn><eissn>1096-0333</eissn><abstract>Epidemiological studies report that arsenic exposure via drinking water adversely impacts cognitive development in children and, in adults, can lead to greater psychiatric disease susceptibility, among other conditions. While it is known that arsenic toxicity has a profound effect on the epigenetic landscape, very few studies have investigated its effects on chromatin architecture in the brain. We have previously demonstrated that exposure to a low level of arsenic (50ppb) during all three trimesters of fetal/neonatal development induces deficits in adult hippocampal neurogenesis in the dentate gyrus (DG), depressive-like symptoms, and alterations in gene expression in the adult mouse brain. As epigenetic processes control these outcomes, here we assess the impact of our developmental arsenic exposure (DAE) paradigm on global histone posttranslational modifications and associated chromatin-modifying proteins in the dentate gyrus and frontal cortex (FC) of adult male and female mice. DAE influenced histone 3K4 trimethylation with increased levels in the male DG and FC and decreased levels in the female DG (no change in female FC). The histone methyltransferase MLL exhibited a similar sex- and region-specific expression profile as H3K4me3 levels, while histone demethylase KDM5B expression trended in the opposite direction. DAE increased histone 3K9 acetylation levels in the male DG along with histone acetyltransferase (HAT) expression of GCN5 and decreased H3K9ac levels in the male FC along with decreased HAT expression of GCN5 and PCAF. DAE decreased expression of histone deacetylase enzymes HDAC1 and HDAC2, which were concurrent with increased H3K9ac levels but only in the female DG. Levels of H3 and H3K9me3 were not influenced by DAE in either brain region of either sex. These findings suggest that exposure to a low, environmentally relevant level of arsenic during development leads to long-lasting changes in histone methylation and acetylation in the adult brain due to aberrant expression of epigenetic machinery based on region and sex.
•Brain tissue from adult mice with developmental arsenic exposure (DAE) was used.•DAE impacted histone methylation and associated methyltransferases based on sex.•DAE differentially altered histone acetylation based on brain region.•DAE altered HATs in males and HDACs in females.•Epigenetic modifier expression correlated with the associated histone modification.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>26193056</pmid><doi>10.1016/j.taap.2015.07.013</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 60 APPLIED LIFE SCIENCES ACETYLATION Acetyltransferase Age Factors Animals Animals, Newborn Arsenates - toxicity ARSENIC BRAIN CHROMATIN Chromatin Assembly and Disassembly - drug effects Dealkylation Dentate Gyrus - drug effects Dentate Gyrus - metabolism DNA-Binding Proteins - metabolism DRINKING WATER Epigenesis, Genetic Female Frontal Lobe - drug effects Frontal Lobe - metabolism Gene Expression Regulation Gestational Age Histone Histone Deacetylase 1 - metabolism Histone Deacetylase 2 - metabolism Histone-Lysine N-Methyltransferase - metabolism HISTONES Histones - metabolism Jumonji Domain-Containing Histone Demethylases - metabolism Male METHYL TRANSFERASES METHYLATION Methyltransferase MICE Mice, Inbred C57BL MODIFICATIONS Myeloid-Lymphoid Leukemia Protein - metabolism p300-CBP Transcription Factors - metabolism Pregnancy Prenatal Exposure Delayed Effects Sex Sex Factors Water Pollutants, Chemical - toxicity |
| title | Developmental exposure to 50 parts-per-billion arsenic influences histone modifications and associated epigenetic machinery in a region- and sex-specific manner in the adult mouse brain |
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