Arsenic Induces Polyadenylation of Canonical Histone mRNA by Down-regulating Stem-Loop-binding Protein Gene Expression
The replication-dependent histone genes are the only metazoan genes whose messenger RNA (mRNA) does not terminate with a poly(A) tail at the 3′-end. Instead, the histone mRNAs display a stem-loop structure at their 3′-end. Stem-loop-binding protein (SLBP) binds the stem-loop and regulates canonical...
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| Veröffentlicht in: | The Journal of biological chemistry 2014-11, Vol.289 (46), p.31751-31764 |
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| container_title | The Journal of biological chemistry |
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| creator | Brocato, Jason Fang, Lei Chervona, Yana Chen, Danqi Kiok, Kathrin Sun, Hong Tseng, Hsiang-Chi Xu, Dazhong Shamy, Magdy Jin, Chunyuan Costa, Max |
| description | The replication-dependent histone genes are the only metazoan genes whose messenger RNA (mRNA) does not terminate with a poly(A) tail at the 3′-end. Instead, the histone mRNAs display a stem-loop structure at their 3′-end. Stem-loop-binding protein (SLBP) binds the stem-loop and regulates canonical histone mRNA metabolism. Here we report that exposure to arsenic, a carcinogenic metal, decreased cellular levels of SLBP by inducing its proteasomal degradation and inhibiting SLBP transcription via epigenetic mechanisms. Notably, arsenic exposure dramatically increased polyadenylation of canonical histone H3.1 mRNA possibly through down-regulation of SLBP expression. The polyadenylated H3.1 mRNA induced by arsenic was not susceptible to normal degradation that occurs at the end of S phase, resulting in continued presence into mitosis, increased total H3.1 mRNA, and increased H3 protein levels. Excess expression of canonical histones have been shown to increase sensitivity to DNA damage as well as increase the frequency of missing chromosomes and induce genomic instability. Thus, polyadenylation of canonical histone mRNA following arsenic exposure may contribute to arsenic-induced carcinogenesis. |
| doi_str_mv | 10.1074/jbc.M114.591883 |
| format | Article |
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Instead, the histone mRNAs display a stem-loop structure at their 3′-end. Stem-loop-binding protein (SLBP) binds the stem-loop and regulates canonical histone mRNA metabolism. Here we report that exposure to arsenic, a carcinogenic metal, decreased cellular levels of SLBP by inducing its proteasomal degradation and inhibiting SLBP transcription via epigenetic mechanisms. Notably, arsenic exposure dramatically increased polyadenylation of canonical histone H3.1 mRNA possibly through down-regulation of SLBP expression. The polyadenylated H3.1 mRNA induced by arsenic was not susceptible to normal degradation that occurs at the end of S phase, resulting in continued presence into mitosis, increased total H3.1 mRNA, and increased H3 protein levels. Excess expression of canonical histones have been shown to increase sensitivity to DNA damage as well as increase the frequency of missing chromosomes and induce genomic instability. Thus, polyadenylation of canonical histone mRNA following arsenic exposure may contribute to arsenic-induced carcinogenesis.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M114.591883</identifier><identifier>PMID: 25266719</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Arsenic - chemistry ; Cell Biology ; Cell Line, Tumor ; Chromosomes - ultrastructure ; DNA Damage ; Epigenesis, Genetic - drug effects ; Gene Expression Regulation ; HEK293 Cells ; Histones - chemistry ; Humans ; Leukocytes, Mononuclear - drug effects ; Mitosis ; mRNA Cleavage and Polyadenylation Factors - metabolism ; Nuclear Proteins - metabolism ; Polyadenylation ; Protein Binding ; RNA, Messenger - metabolism ; S Phase - drug effects</subject><ispartof>The Journal of biological chemistry, 2014-11, Vol.289 (46), p.31751-31764</ispartof><rights>2014 © 2014 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>2014 by The American Society for Biochemistry and Molecular Biology, Inc.</rights><rights>2014 by The American Society for Biochemistry and Molecular Biology, Inc. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-2ae7eb16e51c608e80f25b7c35acdc049111687e7808361b037a527a825bdf3d3</citedby><cites>FETCH-LOGICAL-c509t-2ae7eb16e51c608e80f25b7c35acdc049111687e7808361b037a527a825bdf3d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4231654/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4231654/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,724,777,781,882,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25266719$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brocato, Jason</creatorcontrib><creatorcontrib>Fang, Lei</creatorcontrib><creatorcontrib>Chervona, Yana</creatorcontrib><creatorcontrib>Chen, Danqi</creatorcontrib><creatorcontrib>Kiok, Kathrin</creatorcontrib><creatorcontrib>Sun, Hong</creatorcontrib><creatorcontrib>Tseng, Hsiang-Chi</creatorcontrib><creatorcontrib>Xu, Dazhong</creatorcontrib><creatorcontrib>Shamy, Magdy</creatorcontrib><creatorcontrib>Jin, Chunyuan</creatorcontrib><creatorcontrib>Costa, Max</creatorcontrib><title>Arsenic Induces Polyadenylation of Canonical Histone mRNA by Down-regulating Stem-Loop-binding Protein Gene Expression</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>The replication-dependent histone genes are the only metazoan genes whose messenger RNA (mRNA) does not terminate with a poly(A) tail at the 3′-end. Instead, the histone mRNAs display a stem-loop structure at their 3′-end. Stem-loop-binding protein (SLBP) binds the stem-loop and regulates canonical histone mRNA metabolism. Here we report that exposure to arsenic, a carcinogenic metal, decreased cellular levels of SLBP by inducing its proteasomal degradation and inhibiting SLBP transcription via epigenetic mechanisms. Notably, arsenic exposure dramatically increased polyadenylation of canonical histone H3.1 mRNA possibly through down-regulation of SLBP expression. The polyadenylated H3.1 mRNA induced by arsenic was not susceptible to normal degradation that occurs at the end of S phase, resulting in continued presence into mitosis, increased total H3.1 mRNA, and increased H3 protein levels. Excess expression of canonical histones have been shown to increase sensitivity to DNA damage as well as increase the frequency of missing chromosomes and induce genomic instability. Thus, polyadenylation of canonical histone mRNA following arsenic exposure may contribute to arsenic-induced carcinogenesis.</description><subject>Arsenic - chemistry</subject><subject>Cell Biology</subject><subject>Cell Line, Tumor</subject><subject>Chromosomes - ultrastructure</subject><subject>DNA Damage</subject><subject>Epigenesis, Genetic - drug effects</subject><subject>Gene Expression Regulation</subject><subject>HEK293 Cells</subject><subject>Histones - chemistry</subject><subject>Humans</subject><subject>Leukocytes, Mononuclear - drug effects</subject><subject>Mitosis</subject><subject>mRNA Cleavage and Polyadenylation Factors - metabolism</subject><subject>Nuclear Proteins - metabolism</subject><subject>Polyadenylation</subject><subject>Protein Binding</subject><subject>RNA, Messenger - metabolism</subject><subject>S Phase - drug effects</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUtP4zAUhS00CDoMa3Yj_4EU3yROnM1IVYeX1AE0D2l2lmPfFKPUruy00H8_jjogWODNlezvHOvcQ8gZsCmwujx_bPX0B0A55Q0IURyQCTBRZAWHv5_IhLEcsibn4ph8jvGRpVM2cESOc55XVQ3NhGxnIaKzmt44s9EY6b3vd8qg2_VqsN5R39G5cj4hqqfXNg7eIV39vJ3Rdke_-yeXBVxuRtgt6a8BV9nC-3XWWmfGm_vgB7SOXmGSXTyvA8aYbL-Qw071EU__zxPy5_Li9_w6W9xd3cxni0xz1gxZrrDGFirkoCsmULAu522tC6600WMYgErUWIuUuoKWFbXiea1EokxXmOKEfNv7rjftCo1GNwTVy3WwKxV20isr3784-yCXfivLvICKl8ngfG-gg48xYPeqBSbHCmSqQI4VyH0FSfH17Zev_MvOE9DsAUzBtxaDjNqi02hsQD1I4-2H5v8AJ5mYVw</recordid><startdate>20141114</startdate><enddate>20141114</enddate><creator>Brocato, Jason</creator><creator>Fang, Lei</creator><creator>Chervona, Yana</creator><creator>Chen, Danqi</creator><creator>Kiok, Kathrin</creator><creator>Sun, Hong</creator><creator>Tseng, Hsiang-Chi</creator><creator>Xu, Dazhong</creator><creator>Shamy, Magdy</creator><creator>Jin, Chunyuan</creator><creator>Costa, Max</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><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>5PM</scope></search><sort><creationdate>20141114</creationdate><title>Arsenic Induces Polyadenylation of Canonical Histone mRNA by Down-regulating Stem-Loop-binding Protein Gene Expression</title><author>Brocato, Jason ; Fang, Lei ; Chervona, Yana ; Chen, Danqi ; Kiok, Kathrin ; Sun, Hong ; Tseng, Hsiang-Chi ; Xu, Dazhong ; Shamy, Magdy ; Jin, Chunyuan ; Costa, Max</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c509t-2ae7eb16e51c608e80f25b7c35acdc049111687e7808361b037a527a825bdf3d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Arsenic - chemistry</topic><topic>Cell Biology</topic><topic>Cell Line, Tumor</topic><topic>Chromosomes - ultrastructure</topic><topic>DNA Damage</topic><topic>Epigenesis, Genetic - drug effects</topic><topic>Gene Expression Regulation</topic><topic>HEK293 Cells</topic><topic>Histones - chemistry</topic><topic>Humans</topic><topic>Leukocytes, Mononuclear - drug effects</topic><topic>Mitosis</topic><topic>mRNA Cleavage and Polyadenylation Factors - metabolism</topic><topic>Nuclear Proteins - metabolism</topic><topic>Polyadenylation</topic><topic>Protein Binding</topic><topic>RNA, Messenger - metabolism</topic><topic>S Phase - drug effects</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brocato, Jason</creatorcontrib><creatorcontrib>Fang, Lei</creatorcontrib><creatorcontrib>Chervona, Yana</creatorcontrib><creatorcontrib>Chen, Danqi</creatorcontrib><creatorcontrib>Kiok, Kathrin</creatorcontrib><creatorcontrib>Sun, Hong</creatorcontrib><creatorcontrib>Tseng, Hsiang-Chi</creatorcontrib><creatorcontrib>Xu, Dazhong</creatorcontrib><creatorcontrib>Shamy, Magdy</creatorcontrib><creatorcontrib>Jin, Chunyuan</creatorcontrib><creatorcontrib>Costa, Max</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brocato, Jason</au><au>Fang, Lei</au><au>Chervona, Yana</au><au>Chen, Danqi</au><au>Kiok, Kathrin</au><au>Sun, Hong</au><au>Tseng, Hsiang-Chi</au><au>Xu, Dazhong</au><au>Shamy, Magdy</au><au>Jin, Chunyuan</au><au>Costa, Max</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Arsenic Induces Polyadenylation of Canonical Histone mRNA by Down-regulating Stem-Loop-binding Protein Gene Expression</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2014-11-14</date><risdate>2014</risdate><volume>289</volume><issue>46</issue><spage>31751</spage><epage>31764</epage><pages>31751-31764</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>The replication-dependent histone genes are the only metazoan genes whose messenger RNA (mRNA) does not terminate with a poly(A) tail at the 3′-end. Instead, the histone mRNAs display a stem-loop structure at their 3′-end. Stem-loop-binding protein (SLBP) binds the stem-loop and regulates canonical histone mRNA metabolism. Here we report that exposure to arsenic, a carcinogenic metal, decreased cellular levels of SLBP by inducing its proteasomal degradation and inhibiting SLBP transcription via epigenetic mechanisms. Notably, arsenic exposure dramatically increased polyadenylation of canonical histone H3.1 mRNA possibly through down-regulation of SLBP expression. The polyadenylated H3.1 mRNA induced by arsenic was not susceptible to normal degradation that occurs at the end of S phase, resulting in continued presence into mitosis, increased total H3.1 mRNA, and increased H3 protein levels. Excess expression of canonical histones have been shown to increase sensitivity to DNA damage as well as increase the frequency of missing chromosomes and induce genomic instability. 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| subjects | Arsenic - chemistry Cell Biology Cell Line, Tumor Chromosomes - ultrastructure DNA Damage Epigenesis, Genetic - drug effects Gene Expression Regulation HEK293 Cells Histones - chemistry Humans Leukocytes, Mononuclear - drug effects Mitosis mRNA Cleavage and Polyadenylation Factors - metabolism Nuclear Proteins - metabolism Polyadenylation Protein Binding RNA, Messenger - metabolism S Phase - drug effects |
| title | Arsenic Induces Polyadenylation of Canonical Histone mRNA by Down-regulating Stem-Loop-binding Protein Gene Expression |
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