Polycomb Associates Genome-wide with a Specific RNA Polymerase II Variant, and Regulates Metabolic Genes in ESCs
Polycomb repressor complexes (PRCs) are important chromatin modifiers fundamentally implicated in pluripotency and cancer. Polycomb silencing in embryonic stem cells (ESCs) can be accompanied by active chromatin and primed RNA polymerase II (RNAPII), but the relationship between PRCs and RNAPII rema...
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| creator | Brookes, Emily de Santiago, Inês Hebenstreit, Daniel Morris, Kelly J. Carroll, Tom Xie, Sheila Q. Stock, Julie K. Heidemann, Martin Eick, Dirk Nozaki, Naohito Kimura, Hiroshi Ragoussis, Jiannis Teichmann, Sarah A. Pombo, Ana |
| description | Polycomb repressor complexes (PRCs) are important chromatin modifiers fundamentally implicated in pluripotency and cancer. Polycomb silencing in embryonic stem cells (ESCs) can be accompanied by active chromatin and primed RNA polymerase II (RNAPII), but the relationship between PRCs and RNAPII remains unclear genome-wide. We mapped PRC repression markers and four RNAPII states in ESCs using ChIP-seq, and found that PRC targets exhibit a range of RNAPII variants. First, developmental PRC targets are bound by unproductive RNAPII (S5p+S7p−S2p−) genome-wide. Sequential ChIP, Ring1B depletion, and genome-wide correlations show that PRCs and RNAPII-S5p physically bind to the same chromatin and functionally synergize. Second, we identify a cohort of genes marked by PRC and elongating RNAPII (S5p+S7p+S2p+); they produce mRNA and protein, and their expression increases upon PRC1 knockdown. We show that this group of PRC targets switches between active and PRC-repressed states within the ESC population, and that many have roles in metabolism.
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► A unique RNAPII variant (S5p+S7p−S2p−) binds PRC targets genome-wide in ESCs ► RNAPII-S5p and PRC coincide in time and localization, and show proportional abundance ► Novel, active PRC-target genes identified in ESCs include metabolic genes ► Active PRC targets switch between on/off (active/PRC) states in the ESC population |
| doi_str_mv | 10.1016/j.stem.2011.12.017 |
| format | Article |
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[Display omitted]
► A unique RNAPII variant (S5p+S7p−S2p−) binds PRC targets genome-wide in ESCs ► RNAPII-S5p and PRC coincide in time and localization, and show proportional abundance ► Novel, active PRC-target genes identified in ESCs include metabolic genes ► Active PRC targets switch between on/off (active/PRC) states in the ESC population</description><identifier>ISSN: 1934-5909</identifier><identifier>EISSN: 1875-9777</identifier><identifier>DOI: 10.1016/j.stem.2011.12.017</identifier><identifier>PMID: 22305566</identifier><language>eng</language><publisher>Cambridge, MA: Elsevier Inc</publisher><subject>Animals ; Biological and medical sciences ; Cell Cycle - genetics ; Cell differentiation, maturation, development, hematopoiesis ; Cell Line ; Cell physiology ; Chromatin - metabolism ; Embryonic Stem Cells - cytology ; Embryonic Stem Cells - metabolism ; Energy Metabolism - genetics ; Fundamental and applied biological sciences. Psychology ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Gene Knockdown Techniques ; Genome-Wide Association Study ; Mice ; Molecular and cellular biology ; Polycomb Repressive Complex 1 ; Polycomb-Group Proteins ; Protein Binding - genetics ; Protein Transport ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; RNA Polymerase II - genetics ; RNA Polymerase II - metabolism ; Ubiquitin-Protein Ligases - genetics ; Ubiquitin-Protein Ligases - metabolism</subject><ispartof>Cell stem cell, 2012-02, Vol.10 (2), p.157-170</ispartof><rights>2012 Elsevier Inc.</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2012 Elsevier Inc. All rights reserved.</rights><rights>2012 ELL & Excerpta Medica. 2012 Elsevier Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c560t-81aea589a4415f4eb270e99b014d250aec1e751a1e8dd48d72141da8cfb0f7993</citedby><cites>FETCH-LOGICAL-c560t-81aea589a4415f4eb270e99b014d250aec1e751a1e8dd48d72141da8cfb0f7993</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1934590911005984$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25483364$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22305566$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brookes, Emily</creatorcontrib><creatorcontrib>de Santiago, Inês</creatorcontrib><creatorcontrib>Hebenstreit, Daniel</creatorcontrib><creatorcontrib>Morris, Kelly J.</creatorcontrib><creatorcontrib>Carroll, Tom</creatorcontrib><creatorcontrib>Xie, Sheila Q.</creatorcontrib><creatorcontrib>Stock, Julie K.</creatorcontrib><creatorcontrib>Heidemann, Martin</creatorcontrib><creatorcontrib>Eick, Dirk</creatorcontrib><creatorcontrib>Nozaki, Naohito</creatorcontrib><creatorcontrib>Kimura, Hiroshi</creatorcontrib><creatorcontrib>Ragoussis, Jiannis</creatorcontrib><creatorcontrib>Teichmann, Sarah A.</creatorcontrib><creatorcontrib>Pombo, Ana</creatorcontrib><title>Polycomb Associates Genome-wide with a Specific RNA Polymerase II Variant, and Regulates Metabolic Genes in ESCs</title><title>Cell stem cell</title><addtitle>Cell Stem Cell</addtitle><description>Polycomb repressor complexes (PRCs) are important chromatin modifiers fundamentally implicated in pluripotency and cancer. Polycomb silencing in embryonic stem cells (ESCs) can be accompanied by active chromatin and primed RNA polymerase II (RNAPII), but the relationship between PRCs and RNAPII remains unclear genome-wide. We mapped PRC repression markers and four RNAPII states in ESCs using ChIP-seq, and found that PRC targets exhibit a range of RNAPII variants. First, developmental PRC targets are bound by unproductive RNAPII (S5p+S7p−S2p−) genome-wide. Sequential ChIP, Ring1B depletion, and genome-wide correlations show that PRCs and RNAPII-S5p physically bind to the same chromatin and functionally synergize. Second, we identify a cohort of genes marked by PRC and elongating RNAPII (S5p+S7p+S2p+); they produce mRNA and protein, and their expression increases upon PRC1 knockdown. We show that this group of PRC targets switches between active and PRC-repressed states within the ESC population, and that many have roles in metabolism.
[Display omitted]
► A unique RNAPII variant (S5p+S7p−S2p−) binds PRC targets genome-wide in ESCs ► RNAPII-S5p and PRC coincide in time and localization, and show proportional abundance ► Novel, active PRC-target genes identified in ESCs include metabolic genes ► Active PRC targets switch between on/off (active/PRC) states in the ESC population</description><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Cell Cycle - genetics</subject><subject>Cell differentiation, maturation, development, hematopoiesis</subject><subject>Cell Line</subject><subject>Cell physiology</subject><subject>Chromatin - metabolism</subject><subject>Embryonic Stem Cells - cytology</subject><subject>Embryonic Stem Cells - metabolism</subject><subject>Energy Metabolism - genetics</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Knockdown Techniques</subject><subject>Genome-Wide Association Study</subject><subject>Mice</subject><subject>Molecular and cellular biology</subject><subject>Polycomb Repressive Complex 1</subject><subject>Polycomb-Group Proteins</subject><subject>Protein Binding - genetics</subject><subject>Protein Transport</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>RNA Polymerase II - genetics</subject><subject>RNA Polymerase II - metabolism</subject><subject>Ubiquitin-Protein Ligases - genetics</subject><subject>Ubiquitin-Protein Ligases - metabolism</subject><issn>1934-5909</issn><issn>1875-9777</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkVFvFCEUhSdGY2v1D_hgeDG-OFtgYBgSY7LZ1LpJq6ZVX8kduNOymRlWmG3Tfy_bXau-GJ-A8J3D5ZyieMnojFFWH69macJhxiljM8ZnlKlHxSFrlCy1Uupx3utKlFJTfVA8S2lFqVSMqqfFAecVlbKuD4v1l9Df2TC0ZJ5SsB4mTOQUxzBgeesdkls_XRMgl2u0vvOWXHyak61mwAgJyXJJvkP0ME5vCYyOXODVpr83OccJ2tBnSbbLZz-Sk8tFel486aBP-GK_HhXfPpx8XXwszz6fLhfzs9LKmk5lwwBBNhqEYLIT2HJFUeuWMuG4pICWoZIMGDbOicYpzgRz0NiupZ3Sujoq3u9815t2QGdxnCL0Zh39APHOBPDm75vRX5urcGOquuE5xGzwZm8Qw48NpskMPlnsexgxbJLRvGJa6P8iac67rkUm-Y60MaQUsXuYh1Gz7dSszLZTs-3UMG5yp1n06s-fPEh-lZiB13sAkoW-izBan35zUjRVdf_6ux2HOfcbj9Ek63G06HxEOxkX_L_m-An9HsBb</recordid><startdate>20120203</startdate><enddate>20120203</enddate><creator>Brookes, Emily</creator><creator>de Santiago, Inês</creator><creator>Hebenstreit, Daniel</creator><creator>Morris, Kelly J.</creator><creator>Carroll, Tom</creator><creator>Xie, Sheila Q.</creator><creator>Stock, Julie K.</creator><creator>Heidemann, Martin</creator><creator>Eick, Dirk</creator><creator>Nozaki, Naohito</creator><creator>Kimura, Hiroshi</creator><creator>Ragoussis, Jiannis</creator><creator>Teichmann, Sarah A.</creator><creator>Pombo, Ana</creator><general>Elsevier Inc</general><general>Cell Press</general><scope>6I.</scope><scope>AAFTH</scope><scope>IQODW</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>7X8</scope><scope>7QO</scope><scope>7T5</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>5PM</scope></search><sort><creationdate>20120203</creationdate><title>Polycomb Associates Genome-wide with a Specific RNA Polymerase II Variant, and Regulates Metabolic Genes in ESCs</title><author>Brookes, Emily ; de Santiago, Inês ; Hebenstreit, Daniel ; Morris, Kelly J. ; Carroll, Tom ; Xie, Sheila Q. ; Stock, Julie K. ; Heidemann, Martin ; Eick, Dirk ; Nozaki, Naohito ; Kimura, Hiroshi ; Ragoussis, Jiannis ; Teichmann, Sarah A. ; Pombo, Ana</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c560t-81aea589a4415f4eb270e99b014d250aec1e751a1e8dd48d72141da8cfb0f7993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Cell Cycle - genetics</topic><topic>Cell differentiation, maturation, development, hematopoiesis</topic><topic>Cell Line</topic><topic>Cell physiology</topic><topic>Chromatin - metabolism</topic><topic>Embryonic Stem Cells - cytology</topic><topic>Embryonic Stem Cells - metabolism</topic><topic>Energy Metabolism - genetics</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Knockdown Techniques</topic><topic>Genome-Wide Association Study</topic><topic>Mice</topic><topic>Molecular and cellular biology</topic><topic>Polycomb Repressive Complex 1</topic><topic>Polycomb-Group Proteins</topic><topic>Protein Binding - genetics</topic><topic>Protein Transport</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>RNA Polymerase II - genetics</topic><topic>RNA Polymerase II - metabolism</topic><topic>Ubiquitin-Protein Ligases - genetics</topic><topic>Ubiquitin-Protein Ligases - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brookes, Emily</creatorcontrib><creatorcontrib>de Santiago, Inês</creatorcontrib><creatorcontrib>Hebenstreit, Daniel</creatorcontrib><creatorcontrib>Morris, Kelly J.</creatorcontrib><creatorcontrib>Carroll, Tom</creatorcontrib><creatorcontrib>Xie, Sheila Q.</creatorcontrib><creatorcontrib>Stock, Julie K.</creatorcontrib><creatorcontrib>Heidemann, Martin</creatorcontrib><creatorcontrib>Eick, Dirk</creatorcontrib><creatorcontrib>Nozaki, Naohito</creatorcontrib><creatorcontrib>Kimura, Hiroshi</creatorcontrib><creatorcontrib>Ragoussis, Jiannis</creatorcontrib><creatorcontrib>Teichmann, Sarah A.</creatorcontrib><creatorcontrib>Pombo, Ana</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Pascal-Francis</collection><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>Biotechnology Research Abstracts</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell stem cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brookes, Emily</au><au>de Santiago, Inês</au><au>Hebenstreit, Daniel</au><au>Morris, Kelly J.</au><au>Carroll, Tom</au><au>Xie, Sheila Q.</au><au>Stock, Julie K.</au><au>Heidemann, Martin</au><au>Eick, Dirk</au><au>Nozaki, Naohito</au><au>Kimura, Hiroshi</au><au>Ragoussis, Jiannis</au><au>Teichmann, Sarah A.</au><au>Pombo, Ana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Polycomb Associates Genome-wide with a Specific RNA Polymerase II Variant, and Regulates Metabolic Genes in ESCs</atitle><jtitle>Cell stem cell</jtitle><addtitle>Cell Stem Cell</addtitle><date>2012-02-03</date><risdate>2012</risdate><volume>10</volume><issue>2</issue><spage>157</spage><epage>170</epage><pages>157-170</pages><issn>1934-5909</issn><eissn>1875-9777</eissn><abstract>Polycomb repressor complexes (PRCs) are important chromatin modifiers fundamentally implicated in pluripotency and cancer. Polycomb silencing in embryonic stem cells (ESCs) can be accompanied by active chromatin and primed RNA polymerase II (RNAPII), but the relationship between PRCs and RNAPII remains unclear genome-wide. We mapped PRC repression markers and four RNAPII states in ESCs using ChIP-seq, and found that PRC targets exhibit a range of RNAPII variants. First, developmental PRC targets are bound by unproductive RNAPII (S5p+S7p−S2p−) genome-wide. Sequential ChIP, Ring1B depletion, and genome-wide correlations show that PRCs and RNAPII-S5p physically bind to the same chromatin and functionally synergize. Second, we identify a cohort of genes marked by PRC and elongating RNAPII (S5p+S7p+S2p+); they produce mRNA and protein, and their expression increases upon PRC1 knockdown. We show that this group of PRC targets switches between active and PRC-repressed states within the ESC population, and that many have roles in metabolism.
[Display omitted]
► A unique RNAPII variant (S5p+S7p−S2p−) binds PRC targets genome-wide in ESCs ► RNAPII-S5p and PRC coincide in time and localization, and show proportional abundance ► Novel, active PRC-target genes identified in ESCs include metabolic genes ► Active PRC targets switch between on/off (active/PRC) states in the ESC population</abstract><cop>Cambridge, MA</cop><pub>Elsevier Inc</pub><pmid>22305566</pmid><doi>10.1016/j.stem.2011.12.017</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological and medical sciences Cell Cycle - genetics Cell differentiation, maturation, development, hematopoiesis Cell Line Cell physiology Chromatin - metabolism Embryonic Stem Cells - cytology Embryonic Stem Cells - metabolism Energy Metabolism - genetics Fundamental and applied biological sciences. Psychology Gene Expression Profiling Gene Expression Regulation, Developmental Gene Knockdown Techniques Genome-Wide Association Study Mice Molecular and cellular biology Polycomb Repressive Complex 1 Polycomb-Group Proteins Protein Binding - genetics Protein Transport Repressor Proteins - genetics Repressor Proteins - metabolism RNA Polymerase II - genetics RNA Polymerase II - metabolism Ubiquitin-Protein Ligases - genetics Ubiquitin-Protein Ligases - metabolism |
| title | Polycomb Associates Genome-wide with a Specific RNA Polymerase II Variant, and Regulates Metabolic Genes in ESCs |
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