Enhancer of polycomb coordinates multiple signaling pathways to promote both cyst and germline stem cell differentiation in the Drosophila adult testis
Stem cells reside in a particular microenvironment known as a niche. The interaction between extrinsic cues originating from the niche and intrinsic factors in stem cells determines their identity and activity. Maintenance of stem cell identity and stem cell self-renewal are known to be controlled b...
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| description | Stem cells reside in a particular microenvironment known as a niche. The interaction between extrinsic cues originating from the niche and intrinsic factors in stem cells determines their identity and activity. Maintenance of stem cell identity and stem cell self-renewal are known to be controlled by chromatin factors. Herein, we use the Drosophila adult testis which has two adult stem cell lineages, the germline stem cell (GSC) lineage and the cyst stem cell (CySC) lineage, to study how chromatin factors regulate stem cell differentiation. We find that the chromatin factor Enhancer of Polycomb [E(Pc)] acts in the CySC lineage to negatively control transcription of genes associated with multiple signaling pathways, including JAK-STAT and EGF, to promote cellular differentiation in the CySC lineage. E(Pc) also has a non-cell-autonomous role in regulating GSC lineage differentiation. When E(Pc) is specifically inactivated in the CySC lineage, defects occur in both germ cell differentiation and maintenance of germline identity. Furthermore, compromising Tip60 histone acetyltransferase activity in the CySC lineage recapitulates loss-of-function phenotypes of E(Pc), suggesting that Tip60 and E(Pc) act together, consistent with published biochemical data. In summary, our results demonstrate that E(Pc) plays a central role in coordinating differentiation between the two adult stem cell lineages in Drosophila testes. |
| doi_str_mv | 10.1371/journal.pgen.1006571 |
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The interaction between extrinsic cues originating from the niche and intrinsic factors in stem cells determines their identity and activity. Maintenance of stem cell identity and stem cell self-renewal are known to be controlled by chromatin factors. Herein, we use the Drosophila adult testis which has two adult stem cell lineages, the germline stem cell (GSC) lineage and the cyst stem cell (CySC) lineage, to study how chromatin factors regulate stem cell differentiation. We find that the chromatin factor Enhancer of Polycomb [E(Pc)] acts in the CySC lineage to negatively control transcription of genes associated with multiple signaling pathways, including JAK-STAT and EGF, to promote cellular differentiation in the CySC lineage. E(Pc) also has a non-cell-autonomous role in regulating GSC lineage differentiation. When E(Pc) is specifically inactivated in the CySC lineage, defects occur in both germ cell differentiation and maintenance of germline identity. Furthermore, compromising Tip60 histone acetyltransferase activity in the CySC lineage recapitulates loss-of-function phenotypes of E(Pc), suggesting that Tip60 and E(Pc) act together, consistent with published biochemical data. In summary, our results demonstrate that E(Pc) plays a central role in coordinating differentiation between the two adult stem cell lineages in Drosophila testes.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006571</identifier><identifier>PMID: 28196077</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult Stem Cells - metabolism ; Analysis ; Animals ; Animals, Genetically Modified ; Biology ; Biology and Life Sciences ; Cell differentiation ; Cell Differentiation - genetics ; Cell division ; Cell Lineage - genetics ; Cell Self Renewal - genetics ; Cysts ; Datasets ; Drosophila ; Drosophila - genetics ; Drosophila - growth & development ; Drosophila Proteins - biosynthesis ; Drosophila Proteins - genetics ; Enhancer Elements, Genetic ; Funding ; Gene expression ; Gene Expression Regulation, Developmental ; Genetic aspects ; Germ Cells - growth & development ; Histone Acetyltransferases - biosynthesis ; Histone Acetyltransferases - genetics ; Histones ; Insects ; Janus Kinases - biosynthesis ; Janus Kinases - genetics ; Male ; Medicine and Health Sciences ; Polycomb-Group Proteins - genetics ; Research and Analysis Methods ; Signal Transduction ; Stem cells ; Stem Cells - metabolism ; Studies ; Testis - growth & development ; Testis - metabolism ; Transcription (Genetics)</subject><ispartof>PLoS genetics, 2017-02, Vol.13 (2), p.e1006571-e1006571</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: adult testis. PLoS Genet 13(2): e1006571. doi:10.1371/journal.pgen.1006571</rights><rights>2017 Feng et al 2017 Feng et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: adult testis. PLoS Genet 13(2): e1006571. doi:10.1371/journal.pgen.1006571</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c825t-b92f5442a06eab802638becf231499942ab810f9c90209a9630f95afbd66e5be3</citedby><cites>FETCH-LOGICAL-c825t-b92f5442a06eab802638becf231499942ab810f9c90209a9630f95afbd66e5be3</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/PMC5308785/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5308785/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2101,2927,23865,27923,27924,53790,53792,79471,79472</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28196077$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Barsh, Gregory S.</contributor><creatorcontrib>Feng, Lijuan</creatorcontrib><creatorcontrib>Shi, Zhen</creatorcontrib><creatorcontrib>Chen, Xin</creatorcontrib><title>Enhancer of polycomb coordinates multiple signaling pathways to promote both cyst and germline stem cell differentiation in the Drosophila adult testis</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Stem cells reside in a particular microenvironment known as a niche. The interaction between extrinsic cues originating from the niche and intrinsic factors in stem cells determines their identity and activity. Maintenance of stem cell identity and stem cell self-renewal are known to be controlled by chromatin factors. Herein, we use the Drosophila adult testis which has two adult stem cell lineages, the germline stem cell (GSC) lineage and the cyst stem cell (CySC) lineage, to study how chromatin factors regulate stem cell differentiation. We find that the chromatin factor Enhancer of Polycomb [E(Pc)] acts in the CySC lineage to negatively control transcription of genes associated with multiple signaling pathways, including JAK-STAT and EGF, to promote cellular differentiation in the CySC lineage. E(Pc) also has a non-cell-autonomous role in regulating GSC lineage differentiation. When E(Pc) is specifically inactivated in the CySC lineage, defects occur in both germ cell differentiation and maintenance of germline identity. Furthermore, compromising Tip60 histone acetyltransferase activity in the CySC lineage recapitulates loss-of-function phenotypes of E(Pc), suggesting that Tip60 and E(Pc) act together, consistent with published biochemical data. In summary, our results demonstrate that E(Pc) plays a central role in coordinating differentiation between the two adult stem cell lineages in Drosophila testes.</description><subject>Adult Stem Cells - metabolism</subject><subject>Analysis</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - genetics</subject><subject>Cell division</subject><subject>Cell Lineage - genetics</subject><subject>Cell Self Renewal - genetics</subject><subject>Cysts</subject><subject>Datasets</subject><subject>Drosophila</subject><subject>Drosophila - genetics</subject><subject>Drosophila - growth & development</subject><subject>Drosophila Proteins - biosynthesis</subject><subject>Drosophila Proteins - genetics</subject><subject>Enhancer Elements, Genetic</subject><subject>Funding</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genetic aspects</subject><subject>Germ Cells - growth & development</subject><subject>Histone Acetyltransferases - biosynthesis</subject><subject>Histone Acetyltransferases - genetics</subject><subject>Histones</subject><subject>Insects</subject><subject>Janus Kinases - biosynthesis</subject><subject>Janus Kinases - genetics</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Polycomb-Group Proteins - genetics</subject><subject>Research and Analysis Methods</subject><subject>Signal Transduction</subject><subject>Stem cells</subject><subject>Stem Cells - metabolism</subject><subject>Studies</subject><subject>Testis - growth & development</subject><subject>Testis - metabolism</subject><subject>Transcription (Genetics)</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVk11v1iAUxxujcXP6DYySmBi9eB7pC1BuTJY5dcniEt9uCaWHlqWFClR9PolfV7o9W_aYXcxwUQq_8z-HP5wse5rjdV6y_M25m72Vw3rqwK5zjClh-b1sPyekXLEKV_dvzPeyRyGcY1ySmrOH2V5R55xixvazP8e2l1aBR06jyQ0b5cYGKed8a6yMENA4D9FMA6BgupTP2A5NMva_5Cag6NDk3egioMbFHqlNiEjaFnXgx4SmoAgjUjAMqDVagwcbjYzGWWQsij2gd94FN_VmkEi2KRVKOaMJj7MHWg4Bnmy_B9m398dfjz6uTs8-nBwdnq5UXZC4anihSVUVElOQTY0LWtYNKF2UecU5TxtNnWPNFccF5pLTMv0QqZuWUiANlAfZ80vdaXBBbD0NIq9ZjRkuKU3EySXROnkuJm9G6TfCSSMuFpzvhPTRqAEEVCyvoCVVodqKFKyu67LArNUNg4Y3Omm93WabmxFaldzwctgR3d2xphed-ylIiVNFJAm82gp492NOTonRhMVeacHNS911zgijmN4BpcsoKU_oi3_Q243YUp1MZzVWu1SiWkTFYcVLRji-qHB9C5VGC6NRzoI2aX0n4PVOQGIi_I6dnEMQJ18-_wf76e7s2fdd9uUNtgc5xD64YV4eatgFq0tQpWcbPOjru8uxWNryyjmxtKXYtmUKe3bz3q-Drvqw_AvlujRn</recordid><startdate>20170214</startdate><enddate>20170214</enddate><creator>Feng, Lijuan</creator><creator>Shi, Zhen</creator><creator>Chen, Xin</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20170214</creationdate><title>Enhancer of polycomb coordinates multiple signaling pathways to promote both cyst and germline stem cell differentiation in the Drosophila adult testis</title><author>Feng, Lijuan ; Shi, Zhen ; Chen, Xin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c825t-b92f5442a06eab802638becf231499942ab810f9c90209a9630f95afbd66e5be3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adult Stem Cells - metabolism</topic><topic>Analysis</topic><topic>Animals</topic><topic>Animals, Genetically Modified</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - genetics</topic><topic>Cell division</topic><topic>Cell Lineage - genetics</topic><topic>Cell Self Renewal - genetics</topic><topic>Cysts</topic><topic>Datasets</topic><topic>Drosophila</topic><topic>Drosophila - genetics</topic><topic>Drosophila - growth & development</topic><topic>Drosophila Proteins - biosynthesis</topic><topic>Drosophila Proteins - genetics</topic><topic>Enhancer Elements, Genetic</topic><topic>Funding</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genetic aspects</topic><topic>Germ Cells - growth & development</topic><topic>Histone Acetyltransferases - biosynthesis</topic><topic>Histone Acetyltransferases - genetics</topic><topic>Histones</topic><topic>Insects</topic><topic>Janus Kinases - biosynthesis</topic><topic>Janus Kinases - genetics</topic><topic>Male</topic><topic>Medicine and Health Sciences</topic><topic>Polycomb-Group Proteins - genetics</topic><topic>Research and Analysis Methods</topic><topic>Signal Transduction</topic><topic>Stem cells</topic><topic>Stem Cells - metabolism</topic><topic>Studies</topic><topic>Testis - growth & development</topic><topic>Testis - metabolism</topic><topic>Transcription (Genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Feng, Lijuan</creatorcontrib><creatorcontrib>Shi, Zhen</creatorcontrib><creatorcontrib>Chen, Xin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</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>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>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content 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 China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Feng, Lijuan</au><au>Shi, Zhen</au><au>Chen, Xin</au><au>Barsh, Gregory S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Enhancer of polycomb coordinates multiple signaling pathways to promote both cyst and germline stem cell differentiation in the Drosophila adult testis</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2017-02-14</date><risdate>2017</risdate><volume>13</volume><issue>2</issue><spage>e1006571</spage><epage>e1006571</epage><pages>e1006571-e1006571</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Stem cells reside in a particular microenvironment known as a niche. The interaction between extrinsic cues originating from the niche and intrinsic factors in stem cells determines their identity and activity. Maintenance of stem cell identity and stem cell self-renewal are known to be controlled by chromatin factors. Herein, we use the Drosophila adult testis which has two adult stem cell lineages, the germline stem cell (GSC) lineage and the cyst stem cell (CySC) lineage, to study how chromatin factors regulate stem cell differentiation. We find that the chromatin factor Enhancer of Polycomb [E(Pc)] acts in the CySC lineage to negatively control transcription of genes associated with multiple signaling pathways, including JAK-STAT and EGF, to promote cellular differentiation in the CySC lineage. E(Pc) also has a non-cell-autonomous role in regulating GSC lineage differentiation. When E(Pc) is specifically inactivated in the CySC lineage, defects occur in both germ cell differentiation and maintenance of germline identity. Furthermore, compromising Tip60 histone acetyltransferase activity in the CySC lineage recapitulates loss-of-function phenotypes of E(Pc), suggesting that Tip60 and E(Pc) act together, consistent with published biochemical data. In summary, our results demonstrate that E(Pc) plays a central role in coordinating differentiation between the two adult stem cell lineages in Drosophila testes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28196077</pmid><doi>10.1371/journal.pgen.1006571</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Adult Stem Cells - metabolism Analysis Animals Animals, Genetically Modified Biology Biology and Life Sciences Cell differentiation Cell Differentiation - genetics Cell division Cell Lineage - genetics Cell Self Renewal - genetics Cysts Datasets Drosophila Drosophila - genetics Drosophila - growth & development Drosophila Proteins - biosynthesis Drosophila Proteins - genetics Enhancer Elements, Genetic Funding Gene expression Gene Expression Regulation, Developmental Genetic aspects Germ Cells - growth & development Histone Acetyltransferases - biosynthesis Histone Acetyltransferases - genetics Histones Insects Janus Kinases - biosynthesis Janus Kinases - genetics Male Medicine and Health Sciences Polycomb-Group Proteins - genetics Research and Analysis Methods Signal Transduction Stem cells Stem Cells - metabolism Studies Testis - growth & development Testis - metabolism Transcription (Genetics) |
| title | Enhancer of polycomb coordinates multiple signaling pathways to promote both cyst and germline stem cell differentiation in the Drosophila adult testis |
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