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Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans
In Caenorhabditis elegans , numerous ‘synMuv’ (synthetic multivulval) genes encode for chromatin‐associated proteins involved in transcriptional repression, including an orthologue of Rb and components of the NuRD histone deacetylase complex. These genes antagonize Ras signalling to prevent erroneou...
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| Published in: | The EMBO journal 2005-07, Vol.24 (14), p.2613-2623 |
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| creator | Poulin, Gino Dong, Yan Fraser, Andrew G Hopper, Neil A Ahringer, Julie |
| description | In
Caenorhabditis elegans
, numerous ‘synMuv’ (synthetic multivulval) genes encode for chromatin‐associated proteins involved in transcriptional repression, including an orthologue of Rb and components of the NuRD histone deacetylase complex. These genes antagonize Ras signalling to prevent erroneous adoption of vulval fate. To identify new components of this mechanism, we performed a genome‐wide RNA interference (RNAi) screen. After RNAi of 16 757 genes, we found nine new synMuv genes. Based on predicted functions and genetic epistasis experiments, we propose that at least four post‐translational modifications converge to inhibit Ras‐stimulated vulval development: sumoylation, histone tail deacetylation, methylation, and acetylation. In addition, we demonstrate a novel role for sumoylation in inhibiting LIN‐12/Notch signalling in the vulva. We further show that many of the synMuv genes are involved in gene regulation outside the vulva, negatively regulating the expression of the Delta homologue
lag‐2
. As most of the genes identified in this screen are conserved in humans, we suggest that similar interactions may be relevant in mammals for control of Ras and Notch signalling, crosstalk between these pathways, and cell proliferation. |
| doi_str_mv | 10.1038/sj.emboj.7600726 |
| format | article |
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Caenorhabditis elegans
, numerous ‘synMuv’ (synthetic multivulval) genes encode for chromatin‐associated proteins involved in transcriptional repression, including an orthologue of Rb and components of the NuRD histone deacetylase complex. These genes antagonize Ras signalling to prevent erroneous adoption of vulval fate. To identify new components of this mechanism, we performed a genome‐wide RNA interference (RNAi) screen. After RNAi of 16 757 genes, we found nine new synMuv genes. Based on predicted functions and genetic epistasis experiments, we propose that at least four post‐translational modifications converge to inhibit Ras‐stimulated vulval development: sumoylation, histone tail deacetylation, methylation, and acetylation. In addition, we demonstrate a novel role for sumoylation in inhibiting LIN‐12/Notch signalling in the vulva. We further show that many of the synMuv genes are involved in gene regulation outside the vulva, negatively regulating the expression of the Delta homologue
lag‐2
. As most of the genes identified in this screen are conserved in humans, we suggest that similar interactions may be relevant in mammals for control of Ras and Notch signalling, crosstalk between these pathways, and cell proliferation.</description><identifier>ISSN: 0261-4189</identifier><identifier>EISSN: 1460-2075</identifier><identifier>DOI: 10.1038/sj.emboj.7600726</identifier><identifier>PMID: 15990876</identifier><identifier>CODEN: EMJODG</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Animals ; C. elegans ; Caenorhabditis elegans ; Caenorhabditis elegans - embryology ; Caenorhabditis elegans Proteins - antagonists & inhibitors ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Caenorhabditis elegans Proteins - physiology ; Chromatin - metabolism ; chromatin remodelling ; EMBO09 ; EMBO11 ; Female ; Genes, Reporter ; Ligands ; Mammals ; Membrane Proteins - antagonists & inhibitors ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Methylation ; ras Proteins - physiology ; Ras signalling ; Receptors, Notch ; Repressor Proteins - physiology ; RNAi ; Signal Transduction - genetics ; Signal Transduction - physiology ; SUMO-1 Protein - metabolism ; SUMO-1 Protein - physiology ; Transcription, Genetic - physiology ; vulva ; Vulva - embryology ; Vulva - metabolism</subject><ispartof>The EMBO journal, 2005-07, Vol.24 (14), p.2613-2623</ispartof><rights>European Molecular Biology Organization 2005</rights><rights>Copyright © 2005 European Molecular Biology Organization</rights><rights>Copyright Nature Publishing Group Jul 20, 2005</rights><rights>Copyright © 2005, European Molecular Biology Organization 2005</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6706-38be6539190cc6080ad892a538cbbc910c4b3fd29814ab4a7f0ee46d2238e34a3</citedby><cites>FETCH-LOGICAL-c6706-38be6539190cc6080ad892a538cbbc910c4b3fd29814ab4a7f0ee46d2238e34a3</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/PMC1176455/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1176455/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15990876$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Poulin, Gino</creatorcontrib><creatorcontrib>Dong, Yan</creatorcontrib><creatorcontrib>Fraser, Andrew G</creatorcontrib><creatorcontrib>Hopper, Neil A</creatorcontrib><creatorcontrib>Ahringer, Julie</creatorcontrib><title>Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans</title><title>The EMBO journal</title><addtitle>EMBO J</addtitle><addtitle>EMBO J</addtitle><description>In
Caenorhabditis elegans
, numerous ‘synMuv’ (synthetic multivulval) genes encode for chromatin‐associated proteins involved in transcriptional repression, including an orthologue of Rb and components of the NuRD histone deacetylase complex. These genes antagonize Ras signalling to prevent erroneous adoption of vulval fate. To identify new components of this mechanism, we performed a genome‐wide RNA interference (RNAi) screen. After RNAi of 16 757 genes, we found nine new synMuv genes. Based on predicted functions and genetic epistasis experiments, we propose that at least four post‐translational modifications converge to inhibit Ras‐stimulated vulval development: sumoylation, histone tail deacetylation, methylation, and acetylation. In addition, we demonstrate a novel role for sumoylation in inhibiting LIN‐12/Notch signalling in the vulva. We further show that many of the synMuv genes are involved in gene regulation outside the vulva, negatively regulating the expression of the Delta homologue
lag‐2
. As most of the genes identified in this screen are conserved in humans, we suggest that similar interactions may be relevant in mammals for control of Ras and Notch signalling, crosstalk between these pathways, and cell proliferation.</description><subject>Animals</subject><subject>C. elegans</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - embryology</subject><subject>Caenorhabditis elegans Proteins - antagonists & inhibitors</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Caenorhabditis elegans Proteins - physiology</subject><subject>Chromatin - metabolism</subject><subject>chromatin remodelling</subject><subject>EMBO09</subject><subject>EMBO11</subject><subject>Female</subject><subject>Genes, Reporter</subject><subject>Ligands</subject><subject>Mammals</subject><subject>Membrane Proteins - antagonists & inhibitors</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Methylation</subject><subject>ras Proteins - physiology</subject><subject>Ras signalling</subject><subject>Receptors, Notch</subject><subject>Repressor Proteins - physiology</subject><subject>RNAi</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - physiology</subject><subject>SUMO-1 Protein - metabolism</subject><subject>SUMO-1 Protein - physiology</subject><subject>Transcription, Genetic - physiology</subject><subject>vulva</subject><subject>Vulva - embryology</subject><subject>Vulva - metabolism</subject><issn>0261-4189</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><recordid>eNqFUU1v0zAYjhCIjcGdCyjiwC3l9Uds54JEq7EBZSAE4mg5yds2JbGLnRT67_GWqh1IaKfX9vPhx36S5CmBCQGmXoX1BLvSrSdSAEgq7iWnhAvIKMj8fnIKVJCME1WcJI9CWANAriR5mJyQvChASXGa-NnKu870jU09Loc2rpxNja3TMHRut99HtF9hHKumbG5O3CL9YkLW2HqosE63Q7s1bVrjFlu36dD215qZQev8ypR1FIUUW1waGx4nDxamDfhkP8-Sb2_Pv84us_mni3ezN_OsEhJExlSJImcFKaCqBCgwtSqoyZmqyrIqCFS8ZIuaFopwU3IjF4DIRU0pU8i4YWfJ69F3M5Qd1lUM5U2rN77pjN9pZxr9N2KblV66rSZECp7n0eDl3sC7nwOGXndNqLBtjUU3BC0U5FIxfieRgmKUcBKJL_4hrt3gbfwFTYqcCq4YiyQYSZV3IXhcHCIT0Ne167DWN7Xrfe1R8vz2U4-Cfc-RUIyEX02LuzsN9fnH6fujORm1IcrsEv2t0P8P9GzUWNMPHg8XHvFsxJvQ4-8DbPwPLSSTuf5-daEv6dX0A0w_6zn7A0ec6GE</recordid><startdate>20050720</startdate><enddate>20050720</enddate><creator>Poulin, Gino</creator><creator>Dong, Yan</creator><creator>Fraser, Andrew G</creator><creator>Hopper, Neil A</creator><creator>Ahringer, Julie</creator><general>John Wiley & Sons, Ltd</general><general>Nature Publishing Group UK</general><general>Blackwell Publishing Ltd</general><scope>BSCLL</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20050720</creationdate><title>Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans</title><author>Poulin, Gino ; Dong, Yan ; Fraser, Andrew G ; Hopper, Neil A ; Ahringer, Julie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6706-38be6539190cc6080ad892a538cbbc910c4b3fd29814ab4a7f0ee46d2238e34a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Animals</topic><topic>C. elegans</topic><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans - 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physiology</topic><topic>vulva</topic><topic>Vulva - embryology</topic><topic>Vulva - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Poulin, Gino</creatorcontrib><creatorcontrib>Dong, Yan</creatorcontrib><creatorcontrib>Fraser, Andrew G</creatorcontrib><creatorcontrib>Hopper, Neil A</creatorcontrib><creatorcontrib>Ahringer, Julie</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>ProQuest Health and Medical</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest research library</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The EMBO journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Poulin, Gino</au><au>Dong, Yan</au><au>Fraser, Andrew G</au><au>Hopper, Neil A</au><au>Ahringer, Julie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans</atitle><jtitle>The EMBO journal</jtitle><stitle>EMBO J</stitle><addtitle>EMBO J</addtitle><date>2005-07-20</date><risdate>2005</risdate><volume>24</volume><issue>14</issue><spage>2613</spage><epage>2623</epage><pages>2613-2623</pages><issn>0261-4189</issn><eissn>1460-2075</eissn><coden>EMJODG</coden><abstract>In
Caenorhabditis elegans
, numerous ‘synMuv’ (synthetic multivulval) genes encode for chromatin‐associated proteins involved in transcriptional repression, including an orthologue of Rb and components of the NuRD histone deacetylase complex. These genes antagonize Ras signalling to prevent erroneous adoption of vulval fate. To identify new components of this mechanism, we performed a genome‐wide RNA interference (RNAi) screen. After RNAi of 16 757 genes, we found nine new synMuv genes. Based on predicted functions and genetic epistasis experiments, we propose that at least four post‐translational modifications converge to inhibit Ras‐stimulated vulval development: sumoylation, histone tail deacetylation, methylation, and acetylation. In addition, we demonstrate a novel role for sumoylation in inhibiting LIN‐12/Notch signalling in the vulva. We further show that many of the synMuv genes are involved in gene regulation outside the vulva, negatively regulating the expression of the Delta homologue
lag‐2
. As most of the genes identified in this screen are conserved in humans, we suggest that similar interactions may be relevant in mammals for control of Ras and Notch signalling, crosstalk between these pathways, and cell proliferation.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>15990876</pmid><doi>10.1038/sj.emboj.7600726</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | The EMBO journal, 2005-07, Vol.24 (14), p.2613-2623 |
| issn | 0261-4189 1460-2075 |
| language | eng |
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| subjects | Animals C. elegans Caenorhabditis elegans Caenorhabditis elegans - embryology Caenorhabditis elegans Proteins - antagonists & inhibitors Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Caenorhabditis elegans Proteins - physiology Chromatin - metabolism chromatin remodelling EMBO09 EMBO11 Female Genes, Reporter Ligands Mammals Membrane Proteins - antagonists & inhibitors Membrane Proteins - genetics Membrane Proteins - metabolism Methylation ras Proteins - physiology Ras signalling Receptors, Notch Repressor Proteins - physiology RNAi Signal Transduction - genetics Signal Transduction - physiology SUMO-1 Protein - metabolism SUMO-1 Protein - physiology Transcription, Genetic - physiology vulva Vulva - embryology Vulva - metabolism |
| title | Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans |
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