Single‐cell RNA sequencing reveals the landscape of early female germ cell development
Meiosis initiation is a crucial step for the production of haploid gametes, which occurs from anterior to posterior in fetal ovaries. The asynchrony of the transition from mitosis to meiosis results in heterogeneity in the female germ cell populations, which limits the studies of meiosis initiation...
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Veröffentlicht in: | The FASEB journal 2020-09, Vol.34 (9), p.12634-12645 |
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creator | Zhao, Zheng‐Hui Ma, Jun‐Yu Meng, Tie‐Gang Wang, Zhen‐Bo Yue, Wei Zhou, Qian Li, Sen Feng, Xie Hou, Yi Schatten, Heide Ou, Xiang‐Hong Sun, Qing‐Yuan |
description | Meiosis initiation is a crucial step for the production of haploid gametes, which occurs from anterior to posterior in fetal ovaries. The asynchrony of the transition from mitosis to meiosis results in heterogeneity in the female germ cell populations, which limits the studies of meiosis initiation and progression at a higher resolution level. To dissect the process of meiosis initiation, we investigated the transcriptional profiles of 19 363 single germ cells collected from E12.5, E14.5, and E16.5 mouse fetal ovaries. Clustering analysis identified seven groups and defined dozens of corresponding transcription factors, providing a global view of cellular differentiation from primordial germ cells toward meiocytes. Furthermore, we explored the dynamics of gene expression within the developmental trajectory with special focus on the critical state of meiosis. We found that meiosis initiation occurs as early as E12.5 and the cluster of oogonia_4 is the critical state between mitosis and meiosis. Our data provide key insights into the transcriptome features of peri‐meiotic female germ cells, which offers new information not only on meiosis initiation and progression but also on screening pathogenic mutations in meiosis‐associated diseases. |
doi_str_mv | 10.1096/fj.202001034RR |
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The asynchrony of the transition from mitosis to meiosis results in heterogeneity in the female germ cell populations, which limits the studies of meiosis initiation and progression at a higher resolution level. To dissect the process of meiosis initiation, we investigated the transcriptional profiles of 19 363 single germ cells collected from E12.5, E14.5, and E16.5 mouse fetal ovaries. Clustering analysis identified seven groups and defined dozens of corresponding transcription factors, providing a global view of cellular differentiation from primordial germ cells toward meiocytes. Furthermore, we explored the dynamics of gene expression within the developmental trajectory with special focus on the critical state of meiosis. We found that meiosis initiation occurs as early as E12.5 and the cluster of oogonia_4 is the critical state between mitosis and meiosis. Our data provide key insights into the transcriptome features of peri‐meiotic female germ cells, which offers new information not only on meiosis initiation and progression but also on screening pathogenic mutations in meiosis‐associated diseases.</description><identifier>ISSN: 0892-6638</identifier><identifier>EISSN: 1530-6860</identifier><identifier>DOI: 10.1096/fj.202001034RR</identifier><identifier>PMID: 32716582</identifier><language>eng</language><publisher>United States</publisher><subject>Animals ; Cell Differentiation ; developmental trajectory ; Female ; Gene Expression Regulation, Developmental ; Meiosis ; meiosis initiation ; Mice ; Mice, Inbred C57BL ; Mitosis ; oocyte ; Oogenesis ; Oogonia - cytology ; Ovary - cytology ; scRNA‐seq ; Sequence Analysis, RNA ; Single-Cell Analysis ; Transcriptome</subject><ispartof>The FASEB journal, 2020-09, Vol.34 (9), p.12634-12645</ispartof><rights>2020 Federation of American Societies for Experimental Biology</rights><rights>2020 Federation of American Societies for Experimental Biology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4264-48ca1d2552dd7f0eb12af76978b192490c472e2717ccf9a7902cbbccc6cd010c3</citedby><cites>FETCH-LOGICAL-c4264-48ca1d2552dd7f0eb12af76978b192490c472e2717ccf9a7902cbbccc6cd010c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1096%2Ffj.202001034RR$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1096%2Ffj.202001034RR$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32716582$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhao, Zheng‐Hui</creatorcontrib><creatorcontrib>Ma, Jun‐Yu</creatorcontrib><creatorcontrib>Meng, Tie‐Gang</creatorcontrib><creatorcontrib>Wang, Zhen‐Bo</creatorcontrib><creatorcontrib>Yue, Wei</creatorcontrib><creatorcontrib>Zhou, Qian</creatorcontrib><creatorcontrib>Li, Sen</creatorcontrib><creatorcontrib>Feng, Xie</creatorcontrib><creatorcontrib>Hou, Yi</creatorcontrib><creatorcontrib>Schatten, Heide</creatorcontrib><creatorcontrib>Ou, Xiang‐Hong</creatorcontrib><creatorcontrib>Sun, Qing‐Yuan</creatorcontrib><title>Single‐cell RNA sequencing reveals the landscape of early female germ cell development</title><title>The FASEB journal</title><addtitle>FASEB J</addtitle><description>Meiosis initiation is a crucial step for the production of haploid gametes, which occurs from anterior to posterior in fetal ovaries. The asynchrony of the transition from mitosis to meiosis results in heterogeneity in the female germ cell populations, which limits the studies of meiosis initiation and progression at a higher resolution level. To dissect the process of meiosis initiation, we investigated the transcriptional profiles of 19 363 single germ cells collected from E12.5, E14.5, and E16.5 mouse fetal ovaries. Clustering analysis identified seven groups and defined dozens of corresponding transcription factors, providing a global view of cellular differentiation from primordial germ cells toward meiocytes. Furthermore, we explored the dynamics of gene expression within the developmental trajectory with special focus on the critical state of meiosis. We found that meiosis initiation occurs as early as E12.5 and the cluster of oogonia_4 is the critical state between mitosis and meiosis. Our data provide key insights into the transcriptome features of peri‐meiotic female germ cells, which offers new information not only on meiosis initiation and progression but also on screening pathogenic mutations in meiosis‐associated diseases.</description><subject>Animals</subject><subject>Cell Differentiation</subject><subject>developmental trajectory</subject><subject>Female</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Meiosis</subject><subject>meiosis initiation</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mitosis</subject><subject>oocyte</subject><subject>Oogenesis</subject><subject>Oogonia - cytology</subject><subject>Ovary - cytology</subject><subject>scRNA‐seq</subject><subject>Sequence Analysis, RNA</subject><subject>Single-Cell Analysis</subject><subject>Transcriptome</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkDFPwzAUhC0EoqWwMiKPLCn2S-IkY6koIFUgtSCxWY7zXFI5SYlbUDd-Ar-RX4JLC2JjetLpu9O9I-SUsz5nmbgw8z4wYIyzMJpM9kiXxyELRCrYPumyNINAiDDtkCPn5myDcXFIOiEkXMQpdMnTtKxnFj_fPzRaSyd3A-rwZYW19jpt8RWVdXT5jNSqunBaLZA2hqJq7ZoarJRFOsO2ot_2wvO2WVRYL4_JgfFWPNndHnkcXT0Mb4Lx_fXtcDAOdAQiCqJUK15AHENRJIZhzkGZRGRJmvMMoozpKAH0dROtTaaSjIHOc6210IX_Roc9cr7NXbSN7-2WsirdpoyqsVk5CREkMYSCC4_2t6huG-daNHLRlpVq15IzuVlTmrn8s6Y3nO2yV3mFxS_-M58H4i3wVlpc_xMnR9NLAJaKKPwCAlCA9A</recordid><startdate>202009</startdate><enddate>202009</enddate><creator>Zhao, Zheng‐Hui</creator><creator>Ma, Jun‐Yu</creator><creator>Meng, Tie‐Gang</creator><creator>Wang, Zhen‐Bo</creator><creator>Yue, Wei</creator><creator>Zhou, Qian</creator><creator>Li, Sen</creator><creator>Feng, Xie</creator><creator>Hou, Yi</creator><creator>Schatten, Heide</creator><creator>Ou, Xiang‐Hong</creator><creator>Sun, Qing‐Yuan</creator><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></search><sort><creationdate>202009</creationdate><title>Single‐cell RNA sequencing reveals the landscape of early female germ cell development</title><author>Zhao, Zheng‐Hui ; Ma, Jun‐Yu ; Meng, Tie‐Gang ; Wang, Zhen‐Bo ; Yue, Wei ; Zhou, Qian ; Li, Sen ; Feng, Xie ; Hou, Yi ; Schatten, Heide ; Ou, Xiang‐Hong ; Sun, Qing‐Yuan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4264-48ca1d2552dd7f0eb12af76978b192490c472e2717ccf9a7902cbbccc6cd010c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Cell Differentiation</topic><topic>developmental trajectory</topic><topic>Female</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Meiosis</topic><topic>meiosis initiation</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mitosis</topic><topic>oocyte</topic><topic>Oogenesis</topic><topic>Oogonia - cytology</topic><topic>Ovary - cytology</topic><topic>scRNA‐seq</topic><topic>Sequence Analysis, RNA</topic><topic>Single-Cell Analysis</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhao, Zheng‐Hui</creatorcontrib><creatorcontrib>Ma, Jun‐Yu</creatorcontrib><creatorcontrib>Meng, Tie‐Gang</creatorcontrib><creatorcontrib>Wang, Zhen‐Bo</creatorcontrib><creatorcontrib>Yue, Wei</creatorcontrib><creatorcontrib>Zhou, Qian</creatorcontrib><creatorcontrib>Li, Sen</creatorcontrib><creatorcontrib>Feng, Xie</creatorcontrib><creatorcontrib>Hou, Yi</creatorcontrib><creatorcontrib>Schatten, Heide</creatorcontrib><creatorcontrib>Ou, Xiang‐Hong</creatorcontrib><creatorcontrib>Sun, Qing‐Yuan</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><jtitle>The FASEB journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhao, Zheng‐Hui</au><au>Ma, Jun‐Yu</au><au>Meng, Tie‐Gang</au><au>Wang, Zhen‐Bo</au><au>Yue, Wei</au><au>Zhou, Qian</au><au>Li, Sen</au><au>Feng, Xie</au><au>Hou, Yi</au><au>Schatten, Heide</au><au>Ou, Xiang‐Hong</au><au>Sun, Qing‐Yuan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Single‐cell RNA sequencing reveals the landscape of early female germ cell development</atitle><jtitle>The FASEB journal</jtitle><addtitle>FASEB J</addtitle><date>2020-09</date><risdate>2020</risdate><volume>34</volume><issue>9</issue><spage>12634</spage><epage>12645</epage><pages>12634-12645</pages><issn>0892-6638</issn><eissn>1530-6860</eissn><abstract>Meiosis initiation is a crucial step for the production of haploid gametes, which occurs from anterior to posterior in fetal ovaries. The asynchrony of the transition from mitosis to meiosis results in heterogeneity in the female germ cell populations, which limits the studies of meiosis initiation and progression at a higher resolution level. To dissect the process of meiosis initiation, we investigated the transcriptional profiles of 19 363 single germ cells collected from E12.5, E14.5, and E16.5 mouse fetal ovaries. Clustering analysis identified seven groups and defined dozens of corresponding transcription factors, providing a global view of cellular differentiation from primordial germ cells toward meiocytes. Furthermore, we explored the dynamics of gene expression within the developmental trajectory with special focus on the critical state of meiosis. We found that meiosis initiation occurs as early as E12.5 and the cluster of oogonia_4 is the critical state between mitosis and meiosis. 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subjects | Animals Cell Differentiation developmental trajectory Female Gene Expression Regulation, Developmental Meiosis meiosis initiation Mice Mice, Inbred C57BL Mitosis oocyte Oogenesis Oogonia - cytology Ovary - cytology scRNA‐seq Sequence Analysis, RNA Single-Cell Analysis Transcriptome |
title | Single‐cell RNA sequencing reveals the landscape of early female germ cell development |
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