Polycomb group genes Psc and Su(z)2 restrict follicle stem cell self-renewal and extrusion by controlling canonical and noncanonical Wnt signaling
Stem cells are critical for maintaining tissue homeostasis and are commonly governed by their niche microenvironment, although the intrinsic mechanisms controlling their multipotency are poorly understood. Polycomb group (PcG) genes are epigenetic silencers, and have emerged recently as important pl...
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Veröffentlicht in: | Genes & development 2010-05, Vol.24 (9), p.933-946 |
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description | Stem cells are critical for maintaining tissue homeostasis and are commonly governed by their niche microenvironment, although the intrinsic mechanisms controlling their multipotency are poorly understood. Polycomb group (PcG) genes are epigenetic silencers, and have emerged recently as important players in maintaining stem cell multipotency by preventing the initiation of differentiation programs. Here we describe an unexpected role of specific PcG genes in allowing adult stem cell differentiation and preventing stem cell-derived tumor development. We show that Posterior sex combs (Psc), which encodes a core Polycomb-repressive complex 1 (PRC1) component, functions redundantly with a similar gene, Suppressor of zeste two [Su(z)2], to restrict follicle stem cell (FSC) self-renewal in the Drosophila ovary. FSCs carrying deletion mutations of both genes extrude basally from the epithelium and continue to self-propagate at ectopic sites, leading to the development of FSC-like tumors. Furthermore, we show that the propagation of the mutant cells is driven by sustained activation of the canonical Wnt signaling pathway, which is essential for FSC self-renewal, whereas the epithelial extrusion is mediated through the planar cell polarity pathway. This study reveals a novel mechanism of epithelial extrusion, and indicates a novel role of polycomb function in allowing adult stem cell differentiation by antagonizing self-renewal programs. Given evolutionary conservation of PcG genes from Drosophila to mammals, they could have similar functions in mammalian stem cells and cancer. |
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Polycomb group (PcG) genes are epigenetic silencers, and have emerged recently as important players in maintaining stem cell multipotency by preventing the initiation of differentiation programs. Here we describe an unexpected role of specific PcG genes in allowing adult stem cell differentiation and preventing stem cell-derived tumor development. We show that Posterior sex combs (Psc), which encodes a core Polycomb-repressive complex 1 (PRC1) component, functions redundantly with a similar gene, Suppressor of zeste two [Su(z)2], to restrict follicle stem cell (FSC) self-renewal in the Drosophila ovary. FSCs carrying deletion mutations of both genes extrude basally from the epithelium and continue to self-propagate at ectopic sites, leading to the development of FSC-like tumors. Furthermore, we show that the propagation of the mutant cells is driven by sustained activation of the canonical Wnt signaling pathway, which is essential for FSC self-renewal, whereas the epithelial extrusion is mediated through the planar cell polarity pathway. This study reveals a novel mechanism of epithelial extrusion, and indicates a novel role of polycomb function in allowing adult stem cell differentiation by antagonizing self-renewal programs. Given evolutionary conservation of PcG genes from Drosophila to mammals, they could have similar functions in mammalian stem cells and cancer.</description><identifier>ISSN: 0890-9369</identifier><identifier>EISSN: 1549-5477</identifier><identifier>DOI: 10.1101/gad.1901510</identifier><identifier>PMID: 20439432</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>Animals ; Cell Differentiation ; Cell Line ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; Drosophila melanogaster - cytology ; Drosophila melanogaster - genetics ; Drosophila melanogaster - metabolism ; Drosophila melanogaster - physiology ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Female ; Gene Deletion ; Glycoproteins - metabolism ; Ovary - cytology ; Ovary - pathology ; Polycomb Repressive Complex 1 ; Research Paper ; Signal Transduction ; Stem Cells - cytology ; Stem Cells - pathology ; Wnt Proteins - metabolism</subject><ispartof>Genes & development, 2010-05, Vol.24 (9), p.933-946</ispartof><rights>Copyright © 2010 by Cold Spring Harbor Laboratory Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c446t-2b398766d715858dd28ec3ee7ea7d20fadc8418539857bd9d5c1f58b1fa85ec43</citedby><cites>FETCH-LOGICAL-c446t-2b398766d715858dd28ec3ee7ea7d20fadc8418539857bd9d5c1f58b1fa85ec43</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/PMC2861192/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2861192/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20439432$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Xinghua</creatorcontrib><creatorcontrib>Han, Yue</creatorcontrib><creatorcontrib>Xi, Rongwen</creatorcontrib><title>Polycomb group genes Psc and Su(z)2 restrict follicle stem cell self-renewal and extrusion by controlling canonical and noncanonical Wnt signaling</title><title>Genes & development</title><addtitle>Genes Dev</addtitle><description>Stem cells are critical for maintaining tissue homeostasis and are commonly governed by their niche microenvironment, although the intrinsic mechanisms controlling their multipotency are poorly understood. Polycomb group (PcG) genes are epigenetic silencers, and have emerged recently as important players in maintaining stem cell multipotency by preventing the initiation of differentiation programs. Here we describe an unexpected role of specific PcG genes in allowing adult stem cell differentiation and preventing stem cell-derived tumor development. We show that Posterior sex combs (Psc), which encodes a core Polycomb-repressive complex 1 (PRC1) component, functions redundantly with a similar gene, Suppressor of zeste two [Su(z)2], to restrict follicle stem cell (FSC) self-renewal in the Drosophila ovary. FSCs carrying deletion mutations of both genes extrude basally from the epithelium and continue to self-propagate at ectopic sites, leading to the development of FSC-like tumors. Furthermore, we show that the propagation of the mutant cells is driven by sustained activation of the canonical Wnt signaling pathway, which is essential for FSC self-renewal, whereas the epithelial extrusion is mediated through the planar cell polarity pathway. This study reveals a novel mechanism of epithelial extrusion, and indicates a novel role of polycomb function in allowing adult stem cell differentiation by antagonizing self-renewal programs. Given evolutionary conservation of PcG genes from Drosophila to mammals, they could have similar functions in mammalian stem cells and cancer.</description><subject>Animals</subject><subject>Cell Differentiation</subject><subject>Cell Line</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Drosophila melanogaster - cytology</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Drosophila melanogaster - physiology</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Female</subject><subject>Gene Deletion</subject><subject>Glycoproteins - metabolism</subject><subject>Ovary - cytology</subject><subject>Ovary - pathology</subject><subject>Polycomb Repressive Complex 1</subject><subject>Research Paper</subject><subject>Signal Transduction</subject><subject>Stem Cells - cytology</subject><subject>Stem Cells - pathology</subject><subject>Wnt Proteins - metabolism</subject><issn>0890-9369</issn><issn>1549-5477</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU9LAzEQxYMotlZP3iVHRbYmu5vd5CJI8R8ULKh4XLLJ7LqSJiXZqvVj-Ind2lr1NMPM770ZeAgdUjKklNCzWuohFYQySrZQn7JURCzN823UJ1yQSCSZ6KG9EF4IIRnJsl3Ui0maiDSJ--hz4sxCuWmJa-_mM1yDhYAnQWFpNb6fH3-cxNhDaH2jWlw5YxplAIcWpliBMTiAqSLfqd6k-dbAe-vnoXEWlwusnG39UmRrrKR1tlFrrOt_B0-2xaGprVyC-2inkibAwboO0OPV5cPoJhrfXd-OLsaRStOsjeIyETzPMp1TxhnXOuagEoAcZK5jUkmteEo56yiWl1popmjFeEkryRmoNBmg85XvbF5OQSvoXpWmmPlmKv2icLIp_m9s81zU7rWIeUapiDuD05WB8i4ED9VGS0mxjKbooinW0XT00d9zG_Yni-QLVW-Ogw</recordid><startdate>201005</startdate><enddate>201005</enddate><creator>Li, Xinghua</creator><creator>Han, Yue</creator><creator>Xi, Rongwen</creator><general>Cold Spring Harbor Laboratory Press</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>5PM</scope></search><sort><creationdate>201005</creationdate><title>Polycomb group genes Psc and Su(z)2 restrict follicle stem cell self-renewal and extrusion by controlling canonical and noncanonical Wnt signaling</title><author>Li, Xinghua ; Han, Yue ; Xi, Rongwen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c446t-2b398766d715858dd28ec3ee7ea7d20fadc8418539857bd9d5c1f58b1fa85ec43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Animals</topic><topic>Cell Differentiation</topic><topic>Cell Line</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Drosophila melanogaster - cytology</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - metabolism</topic><topic>Drosophila melanogaster - physiology</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Female</topic><topic>Gene Deletion</topic><topic>Glycoproteins - metabolism</topic><topic>Ovary - cytology</topic><topic>Ovary - pathology</topic><topic>Polycomb Repressive Complex 1</topic><topic>Research Paper</topic><topic>Signal Transduction</topic><topic>Stem Cells - cytology</topic><topic>Stem Cells - pathology</topic><topic>Wnt Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Xinghua</creatorcontrib><creatorcontrib>Han, Yue</creatorcontrib><creatorcontrib>Xi, Rongwen</creatorcontrib><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>Genes & development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Xinghua</au><au>Han, Yue</au><au>Xi, Rongwen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Polycomb group genes Psc and Su(z)2 restrict follicle stem cell self-renewal and extrusion by controlling canonical and noncanonical Wnt signaling</atitle><jtitle>Genes & development</jtitle><addtitle>Genes Dev</addtitle><date>2010-05</date><risdate>2010</risdate><volume>24</volume><issue>9</issue><spage>933</spage><epage>946</epage><pages>933-946</pages><issn>0890-9369</issn><eissn>1549-5477</eissn><abstract>Stem cells are critical for maintaining tissue homeostasis and are commonly governed by their niche microenvironment, although the intrinsic mechanisms controlling their multipotency are poorly understood. Polycomb group (PcG) genes are epigenetic silencers, and have emerged recently as important players in maintaining stem cell multipotency by preventing the initiation of differentiation programs. Here we describe an unexpected role of specific PcG genes in allowing adult stem cell differentiation and preventing stem cell-derived tumor development. We show that Posterior sex combs (Psc), which encodes a core Polycomb-repressive complex 1 (PRC1) component, functions redundantly with a similar gene, Suppressor of zeste two [Su(z)2], to restrict follicle stem cell (FSC) self-renewal in the Drosophila ovary. FSCs carrying deletion mutations of both genes extrude basally from the epithelium and continue to self-propagate at ectopic sites, leading to the development of FSC-like tumors. Furthermore, we show that the propagation of the mutant cells is driven by sustained activation of the canonical Wnt signaling pathway, which is essential for FSC self-renewal, whereas the epithelial extrusion is mediated through the planar cell polarity pathway. This study reveals a novel mechanism of epithelial extrusion, and indicates a novel role of polycomb function in allowing adult stem cell differentiation by antagonizing self-renewal programs. Given evolutionary conservation of PcG genes from Drosophila to mammals, they could have similar functions in mammalian stem cells and cancer.</abstract><cop>United States</cop><pub>Cold Spring Harbor Laboratory Press</pub><pmid>20439432</pmid><doi>10.1101/gad.1901510</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cell Differentiation Cell Line DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Drosophila melanogaster - cytology Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Drosophila melanogaster - physiology Drosophila Proteins - genetics Drosophila Proteins - metabolism Female Gene Deletion Glycoproteins - metabolism Ovary - cytology Ovary - pathology Polycomb Repressive Complex 1 Research Paper Signal Transduction Stem Cells - cytology Stem Cells - pathology Wnt Proteins - metabolism |
title | Polycomb group genes Psc and Su(z)2 restrict follicle stem cell self-renewal and extrusion by controlling canonical and noncanonical Wnt signaling |
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