DNA Oxidation as Triggered by H3K9me2 Demethylation Drives Estrogen-Induced Gene Expression
Modifications at the N-terminal tails of nucleosomal histones are required for efficient transcription in vivo. We analyzed how H3 histone methylation and demethylation control expression of estrogen-responsive genes and show that a DNA-bound estrogen receptor directs transcription by participating...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2008-01, Vol.319 (5860), p.202-206 |
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| creator | Perillo, Bruno Ombra, Maria Neve Bertoni, Alessandra Cuozzo, Concetta Sacchetti, Silvana Sasso, Annarita Chiariotti, Lorenzo Malorni, Antonio Abbondanza, Ciro Avvedimento, Enrico V |
| description | Modifications at the N-terminal tails of nucleosomal histones are required for efficient transcription in vivo. We analyzed how H3 histone methylation and demethylation control expression of estrogen-responsive genes and show that a DNA-bound estrogen receptor directs transcription by participating in bending chromatin to contact the RNA polymerase II recruited to the promoter. This process is driven by receptor-targeted demethylation of H3 lysine 9 at both enhancer and promoter sites and is achieved by activation of resident LSD1 demethylase. Localized demethylation produces hydrogen peroxide, which modifies the surrounding DNA and recruits 8-oxoguanine-DNA glycosylase 1 and topoisomeraseIIβ, triggering chromatin and DNA conformational changes that are essential for estrogen-induced transcription. Our data show a strategy that uses controlled DNA damage and repair to guide productive transcription. |
| doi_str_mv | 10.1126/science.1147674 |
| format | Article |
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We analyzed how H3 histone methylation and demethylation control expression of estrogen-responsive genes and show that a DNA-bound estrogen receptor directs transcription by participating in bending chromatin to contact the RNA polymerase II recruited to the promoter. This process is driven by receptor-targeted demethylation of H3 lysine 9 at both enhancer and promoter sites and is achieved by activation of resident LSD1 demethylase. Localized demethylation produces hydrogen peroxide, which modifies the surrounding DNA and recruits 8-oxoguanine-DNA glycosylase 1 and topoisomeraseIIβ, triggering chromatin and DNA conformational changes that are essential for estrogen-induced transcription. Our data show a strategy that uses controlled DNA damage and repair to guide productive transcription.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1147674</identifier><identifier>PMID: 18187655</identifier><identifier>CODEN: SCIEAS</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Cell Line, Tumor ; Cells, Cultured ; Chromatin ; Chromatin - metabolism ; DNA ; DNA - metabolism ; DNA Damage ; DNA Glycosylases - metabolism ; DNA Repair ; DNA Topoisomerases, Type II - metabolism ; DNA-Binding Proteins - metabolism ; Enhancer Elements, Genetic ; Enzymes ; Estradiol - metabolism ; Estrogen Receptor alpha - metabolism ; Estrogens ; Gene expression ; Gene Expression Regulation ; Genes ; Genes, bcl-2 ; Genetics ; Guanine - analogs & derivatives ; Guanine - metabolism ; Histone Demethylases ; Histones ; Histones - metabolism ; Humans ; Hydrogen Peroxide - metabolism ; Lysine - metabolism ; Methylation ; Molecular biology ; Nucleic Acid Conformation ; Oxidation-Reduction ; Oxidoreductases, N-Demethylating - metabolism ; Promoter regions ; Promoter Regions, Genetic ; Receptors ; RNA ; RNA polymerase ; RNA Polymerase II - metabolism ; Small interfering RNA ; Transcription, Genetic</subject><ispartof>Science (American Association for the Advancement of Science), 2008-01, Vol.319 (5860), p.202-206</ispartof><rights>Copyright 2008 American Association for the Advancement of Science</rights><rights>Copyright © 2008, American Association for the Advancement of Science</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c495t-cd25f8160cacff9e1847d11ef4e09a92513306d40d89ff21240dd510d875fe253</citedby><cites>FETCH-LOGICAL-c495t-cd25f8160cacff9e1847d11ef4e09a92513306d40d89ff21240dd510d875fe253</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/20051978$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/20051978$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,776,780,799,2871,2872,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18187655$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Perillo, Bruno</creatorcontrib><creatorcontrib>Ombra, Maria Neve</creatorcontrib><creatorcontrib>Bertoni, Alessandra</creatorcontrib><creatorcontrib>Cuozzo, Concetta</creatorcontrib><creatorcontrib>Sacchetti, Silvana</creatorcontrib><creatorcontrib>Sasso, Annarita</creatorcontrib><creatorcontrib>Chiariotti, Lorenzo</creatorcontrib><creatorcontrib>Malorni, Antonio</creatorcontrib><creatorcontrib>Abbondanza, Ciro</creatorcontrib><creatorcontrib>Avvedimento, Enrico V</creatorcontrib><title>DNA Oxidation as Triggered by H3K9me2 Demethylation Drives Estrogen-Induced Gene Expression</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Modifications at the N-terminal tails of nucleosomal histones are required for efficient transcription in vivo. We analyzed how H3 histone methylation and demethylation control expression of estrogen-responsive genes and show that a DNA-bound estrogen receptor directs transcription by participating in bending chromatin to contact the RNA polymerase II recruited to the promoter. This process is driven by receptor-targeted demethylation of H3 lysine 9 at both enhancer and promoter sites and is achieved by activation of resident LSD1 demethylase. Localized demethylation produces hydrogen peroxide, which modifies the surrounding DNA and recruits 8-oxoguanine-DNA glycosylase 1 and topoisomeraseIIβ, triggering chromatin and DNA conformational changes that are essential for estrogen-induced transcription. Our data show a strategy that uses controlled DNA damage and repair to guide productive transcription.</description><subject>Cell Line, Tumor</subject><subject>Cells, Cultured</subject><subject>Chromatin</subject><subject>Chromatin - metabolism</subject><subject>DNA</subject><subject>DNA - metabolism</subject><subject>DNA Damage</subject><subject>DNA Glycosylases - metabolism</subject><subject>DNA Repair</subject><subject>DNA Topoisomerases, Type II - metabolism</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Enhancer Elements, Genetic</subject><subject>Enzymes</subject><subject>Estradiol - metabolism</subject><subject>Estrogen Receptor alpha - metabolism</subject><subject>Estrogens</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Genes</subject><subject>Genes, bcl-2</subject><subject>Genetics</subject><subject>Guanine - analogs & derivatives</subject><subject>Guanine - metabolism</subject><subject>Histone Demethylases</subject><subject>Histones</subject><subject>Histones - metabolism</subject><subject>Humans</subject><subject>Hydrogen Peroxide - metabolism</subject><subject>Lysine - metabolism</subject><subject>Methylation</subject><subject>Molecular biology</subject><subject>Nucleic Acid Conformation</subject><subject>Oxidation-Reduction</subject><subject>Oxidoreductases, N-Demethylating - metabolism</subject><subject>Promoter regions</subject><subject>Promoter Regions, Genetic</subject><subject>Receptors</subject><subject>RNA</subject><subject>RNA polymerase</subject><subject>RNA Polymerase II - metabolism</subject><subject>Small interfering RNA</subject><subject>Transcription, Genetic</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUFv1DAQhS0EokvhzAmIOHALnbHjJD5W3aWtqOih7akHy7XHS1abZGsnqPvv8SoRlXrhNDN637yx9Rj7iPAdkZcn0TbUWUpDUZVV8YotEJTMFQfxmi0ARJnXUMkj9i7GDUDSlHjLjrDGuiqlXLD75a_T7PqpcWZo-i4zMbsNzXpNgVz2sM8uxE_VEs-W1NLwe7-dqGVo_lDMVnEI_Zq6_LJzo00L59RRtnraBYoxce_ZG2-2kT7M9Zjd_Vjdnl3kV9fnl2enV7ktlBxy67j0NZZgjfVeEdZF5RDJFwTKKC5RCChdAa5W3nPkqXMS01hJT1yKY_Zt8t2F_nGkOOi2iZa2W9NRP0ZdAR5cyv-CqCpMxw7g1xfgph9Dlz6hOQpZK8VFgk4myIY-xkBe70LTmrDXCPqQjp7T0XM6aePzbDs-tOSe-TmOBHyagE0c-vBP5wAyva1O-pdJ96bXZh2aqO9uOKAAqAspFYq_FTidKg</recordid><startdate>20080111</startdate><enddate>20080111</enddate><creator>Perillo, Bruno</creator><creator>Ombra, Maria Neve</creator><creator>Bertoni, Alessandra</creator><creator>Cuozzo, Concetta</creator><creator>Sacchetti, Silvana</creator><creator>Sasso, Annarita</creator><creator>Chiariotti, Lorenzo</creator><creator>Malorni, Antonio</creator><creator>Abbondanza, Ciro</creator><creator>Avvedimento, Enrico V</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</general><scope>FBQ</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>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7QO</scope><scope>7X8</scope></search><sort><creationdate>20080111</creationdate><title>DNA Oxidation as Triggered by H3K9me2 Demethylation Drives Estrogen-Induced Gene Expression</title><author>Perillo, Bruno ; Ombra, Maria Neve ; Bertoni, Alessandra ; Cuozzo, Concetta ; Sacchetti, Silvana ; Sasso, Annarita ; Chiariotti, Lorenzo ; Malorni, Antonio ; Abbondanza, Ciro ; Avvedimento, Enrico V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c495t-cd25f8160cacff9e1847d11ef4e09a92513306d40d89ff21240dd510d875fe253</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Cell Line, Tumor</topic><topic>Cells, Cultured</topic><topic>Chromatin</topic><topic>Chromatin - 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metabolism</topic><topic>Promoter regions</topic><topic>Promoter Regions, Genetic</topic><topic>Receptors</topic><topic>RNA</topic><topic>RNA polymerase</topic><topic>RNA Polymerase II - metabolism</topic><topic>Small interfering RNA</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Perillo, Bruno</creatorcontrib><creatorcontrib>Ombra, Maria Neve</creatorcontrib><creatorcontrib>Bertoni, Alessandra</creatorcontrib><creatorcontrib>Cuozzo, Concetta</creatorcontrib><creatorcontrib>Sacchetti, Silvana</creatorcontrib><creatorcontrib>Sasso, Annarita</creatorcontrib><creatorcontrib>Chiariotti, Lorenzo</creatorcontrib><creatorcontrib>Malorni, Antonio</creatorcontrib><creatorcontrib>Abbondanza, Ciro</creatorcontrib><creatorcontrib>Avvedimento, Enrico V</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Biotechnology Research Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Perillo, Bruno</au><au>Ombra, Maria Neve</au><au>Bertoni, Alessandra</au><au>Cuozzo, Concetta</au><au>Sacchetti, Silvana</au><au>Sasso, Annarita</au><au>Chiariotti, Lorenzo</au><au>Malorni, Antonio</au><au>Abbondanza, Ciro</au><au>Avvedimento, Enrico V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>DNA Oxidation as Triggered by H3K9me2 Demethylation Drives Estrogen-Induced Gene Expression</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2008-01-11</date><risdate>2008</risdate><volume>319</volume><issue>5860</issue><spage>202</spage><epage>206</epage><pages>202-206</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><coden>SCIEAS</coden><abstract>Modifications at the N-terminal tails of nucleosomal histones are required for efficient transcription in vivo. We analyzed how H3 histone methylation and demethylation control expression of estrogen-responsive genes and show that a DNA-bound estrogen receptor directs transcription by participating in bending chromatin to contact the RNA polymerase II recruited to the promoter. This process is driven by receptor-targeted demethylation of H3 lysine 9 at both enhancer and promoter sites and is achieved by activation of resident LSD1 demethylase. Localized demethylation produces hydrogen peroxide, which modifies the surrounding DNA and recruits 8-oxoguanine-DNA glycosylase 1 and topoisomeraseIIβ, triggering chromatin and DNA conformational changes that are essential for estrogen-induced transcription. Our data show a strategy that uses controlled DNA damage and repair to guide productive transcription.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>18187655</pmid><doi>10.1126/science.1147674</doi><tpages>5</tpages></addata></record> |
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| ispartof | Science (American Association for the Advancement of Science), 2008-01, Vol.319 (5860), p.202-206 |
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| source | American Association for the Advancement of Science; Jstor Complete Legacy; MEDLINE |
| subjects | Cell Line, Tumor Cells, Cultured Chromatin Chromatin - metabolism DNA DNA - metabolism DNA Damage DNA Glycosylases - metabolism DNA Repair DNA Topoisomerases, Type II - metabolism DNA-Binding Proteins - metabolism Enhancer Elements, Genetic Enzymes Estradiol - metabolism Estrogen Receptor alpha - metabolism Estrogens Gene expression Gene Expression Regulation Genes Genes, bcl-2 Genetics Guanine - analogs & derivatives Guanine - metabolism Histone Demethylases Histones Histones - metabolism Humans Hydrogen Peroxide - metabolism Lysine - metabolism Methylation Molecular biology Nucleic Acid Conformation Oxidation-Reduction Oxidoreductases, N-Demethylating - metabolism Promoter regions Promoter Regions, Genetic Receptors RNA RNA polymerase RNA Polymerase II - metabolism Small interfering RNA Transcription, Genetic |
| title | DNA Oxidation as Triggered by H3K9me2 Demethylation Drives Estrogen-Induced Gene Expression |
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