Functional and molecular features of the Id4+ germline stem cell population in mouse testes
The maintenance of cycling cell lineages relies on undifferentiated subpopulations consisting of stem and progenitor pools. Features that delineate these cell types are undefined for many lineages, including spermatogenesis, which is supported by an undifferentiated spermatogonial population. Here,...
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| Veröffentlicht in: | Genes & development 2014-06, Vol.28 (12), p.1351-1362 |
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| creator | Chan, Frieda Oatley, Melissa J Kaucher, Amy V Yang, Qi-En Bieberich, Charles J Shashikant, Cooduvalli S Oatley, Jon M |
| description | The maintenance of cycling cell lineages relies on undifferentiated subpopulations consisting of stem and progenitor pools. Features that delineate these cell types are undefined for many lineages, including spermatogenesis, which is supported by an undifferentiated spermatogonial population. Here, we generated a transgenic mouse line in which spermatogonial stem cells are marked by expression of an inhibitor of differentiation 4 (Id4)-green fluorescent protein (Gfp) transgene. We found that Id4-Gfp(+) cells exist primarily as a subset of the type A(single) pool, and their frequency is greatest in neonatal development and then decreases in proportion during establishment of the spermatogenic lineage, eventually comprising ∼ 2% of the undifferentiated spermatogonial population in adulthood. RNA sequencing analysis revealed that expression of 11 and 25 genes is unique for the Id4-Gfp(+)/stem cell and Id4-Gfp(-)/progenitor fractions, respectively. Collectively, these findings provide the first definitive evidence that stem cells exist as a rare subset of the A(single) pool and reveal transcriptome features distinguishing stem cell and progenitor states within the mammalian male germline. |
| doi_str_mv | 10.1101/gad.240465.114 |
| format | Article |
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Features that delineate these cell types are undefined for many lineages, including spermatogenesis, which is supported by an undifferentiated spermatogonial population. Here, we generated a transgenic mouse line in which spermatogonial stem cells are marked by expression of an inhibitor of differentiation 4 (Id4)-green fluorescent protein (Gfp) transgene. We found that Id4-Gfp(+) cells exist primarily as a subset of the type A(single) pool, and their frequency is greatest in neonatal development and then decreases in proportion during establishment of the spermatogenic lineage, eventually comprising ∼ 2% of the undifferentiated spermatogonial population in adulthood. RNA sequencing analysis revealed that expression of 11 and 25 genes is unique for the Id4-Gfp(+)/stem cell and Id4-Gfp(-)/progenitor fractions, respectively. Collectively, these findings provide the first definitive evidence that stem cells exist as a rare subset of the A(single) pool and reveal transcriptome features distinguishing stem cell and progenitor states within the mammalian male germline.</description><identifier>ISSN: 0890-9369</identifier><identifier>EISSN: 1549-5477</identifier><identifier>DOI: 10.1101/gad.240465.114</identifier><identifier>PMID: 24939937</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>Animals ; Cell Differentiation ; Gene Expression Regulation, Developmental ; Germ Cells - cytology ; Germ Cells - metabolism ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; Inhibitor of Differentiation Proteins - genetics ; Inhibitor of Differentiation Proteins - metabolism ; Male ; Mice ; Mice, Transgenic ; Research Paper ; Spermatogenesis - genetics ; Spermatogonia - metabolism ; Stem Cells - cytology ; Stem Cells - metabolism ; Testis - cytology ; Testis - metabolism ; Transcriptome</subject><ispartof>Genes & development, 2014-06, Vol.28 (12), p.1351-1362</ispartof><rights>2014 Chan et al.; Published by Cold Spring Harbor Laboratory Press.</rights><rights>2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-cf314b02eab2d57e64f73b045835d56fb6f6b2d8a03e3c69452dfb39bba9fa1c3</citedby><cites>FETCH-LOGICAL-c526t-cf314b02eab2d57e64f73b045835d56fb6f6b2d8a03e3c69452dfb39bba9fa1c3</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/PMC4066404/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4066404/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24939937$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chan, Frieda</creatorcontrib><creatorcontrib>Oatley, Melissa J</creatorcontrib><creatorcontrib>Kaucher, Amy V</creatorcontrib><creatorcontrib>Yang, Qi-En</creatorcontrib><creatorcontrib>Bieberich, Charles J</creatorcontrib><creatorcontrib>Shashikant, Cooduvalli S</creatorcontrib><creatorcontrib>Oatley, Jon M</creatorcontrib><title>Functional and molecular features of the Id4+ germline stem cell population in mouse testes</title><title>Genes & development</title><addtitle>Genes Dev</addtitle><description>The maintenance of cycling cell lineages relies on undifferentiated subpopulations consisting of stem and progenitor pools. Features that delineate these cell types are undefined for many lineages, including spermatogenesis, which is supported by an undifferentiated spermatogonial population. Here, we generated a transgenic mouse line in which spermatogonial stem cells are marked by expression of an inhibitor of differentiation 4 (Id4)-green fluorescent protein (Gfp) transgene. We found that Id4-Gfp(+) cells exist primarily as a subset of the type A(single) pool, and their frequency is greatest in neonatal development and then decreases in proportion during establishment of the spermatogenic lineage, eventually comprising ∼ 2% of the undifferentiated spermatogonial population in adulthood. RNA sequencing analysis revealed that expression of 11 and 25 genes is unique for the Id4-Gfp(+)/stem cell and Id4-Gfp(-)/progenitor fractions, respectively. Collectively, these findings provide the first definitive evidence that stem cells exist as a rare subset of the A(single) pool and reveal transcriptome features distinguishing stem cell and progenitor states within the mammalian male germline.</description><subject>Animals</subject><subject>Cell Differentiation</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Germ Cells - cytology</subject><subject>Germ Cells - metabolism</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Inhibitor of Differentiation Proteins - genetics</subject><subject>Inhibitor of Differentiation Proteins - metabolism</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Research Paper</subject><subject>Spermatogenesis - genetics</subject><subject>Spermatogonia - metabolism</subject><subject>Stem Cells - cytology</subject><subject>Stem Cells - metabolism</subject><subject>Testis - cytology</subject><subject>Testis - metabolism</subject><subject>Transcriptome</subject><issn>0890-9369</issn><issn>1549-5477</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkc1LAzEQxYMotlavHiVHQbYmm49tLoIUq4WCFz15CNnspF3ZL5Ndwf_eLK2ipzC8N7_MzEPokpI5pYTebk0xTznhUsSaH6EpFVwlgmfZMZqShSKJYlJN0FkI74QQSaQ8RZOUK6YUy6bobTU0ti_bxlTYNAWu2wrsUBmPHZh-8BBw63C_A7wu-A3egq-rsgEceqixharCXdtF_4jAZRP7hwC4h6iHc3TiTBXg4vDO0Ovq4WX5lGyeH9fL-01iRSr7xDpGeU5SMHlaiAwkdxnLCRcLJgohXS6djMrCEAbMSsVFWricqTw3yhlq2Qzd7bndkNdQWGh6byrd-bI2_ku3ptT_labc6W37qXm8RrxdBFwfAL79GOLsui7DuJxpIO6jqWCZUCIjLFrne6v1bQge3O83lOgxER0T0ftEYj2yr_4O92v_iYB9A_smiWU</recordid><startdate>20140615</startdate><enddate>20140615</enddate><creator>Chan, Frieda</creator><creator>Oatley, Melissa J</creator><creator>Kaucher, Amy V</creator><creator>Yang, Qi-En</creator><creator>Bieberich, Charles J</creator><creator>Shashikant, Cooduvalli S</creator><creator>Oatley, Jon M</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20140615</creationdate><title>Functional and molecular features of the Id4+ germline stem cell population in mouse testes</title><author>Chan, Frieda ; Oatley, Melissa J ; Kaucher, Amy V ; Yang, Qi-En ; Bieberich, Charles J ; Shashikant, Cooduvalli S ; Oatley, Jon M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-cf314b02eab2d57e64f73b045835d56fb6f6b2d8a03e3c69452dfb39bba9fa1c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Cell Differentiation</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Germ Cells - cytology</topic><topic>Germ Cells - metabolism</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Inhibitor of Differentiation Proteins - genetics</topic><topic>Inhibitor of Differentiation Proteins - metabolism</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>Research Paper</topic><topic>Spermatogenesis - genetics</topic><topic>Spermatogonia - metabolism</topic><topic>Stem Cells - cytology</topic><topic>Stem Cells - metabolism</topic><topic>Testis - cytology</topic><topic>Testis - metabolism</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chan, Frieda</creatorcontrib><creatorcontrib>Oatley, Melissa J</creatorcontrib><creatorcontrib>Kaucher, Amy V</creatorcontrib><creatorcontrib>Yang, Qi-En</creatorcontrib><creatorcontrib>Bieberich, Charles J</creatorcontrib><creatorcontrib>Shashikant, Cooduvalli S</creatorcontrib><creatorcontrib>Oatley, Jon M</creatorcontrib><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>PubMed Central (Full Participant titles)</collection><jtitle>Genes & development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chan, Frieda</au><au>Oatley, Melissa J</au><au>Kaucher, Amy V</au><au>Yang, Qi-En</au><au>Bieberich, Charles J</au><au>Shashikant, Cooduvalli S</au><au>Oatley, Jon M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional and molecular features of the Id4+ germline stem cell population in mouse testes</atitle><jtitle>Genes & development</jtitle><addtitle>Genes Dev</addtitle><date>2014-06-15</date><risdate>2014</risdate><volume>28</volume><issue>12</issue><spage>1351</spage><epage>1362</epage><pages>1351-1362</pages><issn>0890-9369</issn><eissn>1549-5477</eissn><abstract>The maintenance of cycling cell lineages relies on undifferentiated subpopulations consisting of stem and progenitor pools. Features that delineate these cell types are undefined for many lineages, including spermatogenesis, which is supported by an undifferentiated spermatogonial population. Here, we generated a transgenic mouse line in which spermatogonial stem cells are marked by expression of an inhibitor of differentiation 4 (Id4)-green fluorescent protein (Gfp) transgene. We found that Id4-Gfp(+) cells exist primarily as a subset of the type A(single) pool, and their frequency is greatest in neonatal development and then decreases in proportion during establishment of the spermatogenic lineage, eventually comprising ∼ 2% of the undifferentiated spermatogonial population in adulthood. RNA sequencing analysis revealed that expression of 11 and 25 genes is unique for the Id4-Gfp(+)/stem cell and Id4-Gfp(-)/progenitor fractions, respectively. 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| subjects | Animals Cell Differentiation Gene Expression Regulation, Developmental Germ Cells - cytology Germ Cells - metabolism Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Inhibitor of Differentiation Proteins - genetics Inhibitor of Differentiation Proteins - metabolism Male Mice Mice, Transgenic Research Paper Spermatogenesis - genetics Spermatogonia - metabolism Stem Cells - cytology Stem Cells - metabolism Testis - cytology Testis - metabolism Transcriptome |
| title | Functional and molecular features of the Id4+ germline stem cell population in mouse testes |
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