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gsdf is a downstream gene of dmrt1 that functions in the male sex determination pathway of the Nile tilapia
SUMMARY Gonadal soma‐derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation is lacking. In the present study, we knocked out tilapia gsdf using CRISPR/Cas9. F0 gsdf‐deficient XY fish with high mutation rate (≥58%) dev...
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| Published in: | Molecular reproduction and development 2016-06, Vol.83 (6), p.497-508 |
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| cites | cdi_FETCH-LOGICAL-c4942-b275c44378ad4869813e294254d21b2752d976cbd84b05ac10d654e9a480cba03 |
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| container_start_page | 497 |
| container_title | Molecular reproduction and development |
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| creator | Jiang, Dong-Neng Yang, Hui-Hui Li, Ming-Hui Shi, Hong-Juan Zhang, Xian-Bo Wang, De-Shou |
| description | SUMMARY
Gonadal soma‐derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation is lacking. In the present study, we knocked out tilapia gsdf using CRISPR/Cas9. F0 gsdf‐deficient XY fish with high mutation rate (≥58%) developed as intersex, with ovotestes 90 days after hatching (dah), and become completely sex‐reversed with ovaries at 180 and 240 dah. Those individuals with a low mutation rate ( |
| doi_str_mv | 10.1002/mrd.22642 |
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Gonadal soma‐derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation is lacking. In the present study, we knocked out tilapia gsdf using CRISPR/Cas9. F0 gsdf‐deficient XY fish with high mutation rate (≥58%) developed as intersex, with ovotestes 90 days after hatching (dah), and become completely sex‐reversed with ovaries at 180 and 240 dah. Those individuals with a low mutation rate (<58%) and XY gsdf+/− fish developed as males with normal testes. In F2 XY gsdf−/− fish, the gonads first expressed Dmrt1, which initiated the male pathway at 10 dah, then both male and female pathways were activated, as reflected by the simultaneous expression of Dmrt1 and Cyp19a1a in different cell populations at 18 dah, shifted to the female pathway expressing only Cyp19a1a at 36 dah, and finally developed into functional ovaries as adults. The male pathway and Dmrt1 expression was initiated, but failed to be maintained, in the absence of Gsdf. Aromatase‐inhibitor treatment from 10 to 35 dah, however, rescued the phenotype, resulting in XY gsdf−/− with normal testes that expressed Dmrt1 and Cyp11b2. In vitro promoter analyses demonstrated that Dmrt1 activated gsdf expression in a dose‐dependent manner in the presence of Sf1, even though Dmrt1 alone could not. Taken together, our results demonstrated that gsdf is a downstream gene of dmrt1. Gsdf probably inhibits estrogen production to trigger testicular differentiation. Mol. Reprod. Dev. 83: 497–508, 2016. © 2016 Wiley Periodicals, Inc.</description><identifier>ISSN: 1040-452X</identifier><identifier>EISSN: 1098-2795</identifier><identifier>DOI: 10.1002/mrd.22642</identifier><identifier>PMID: 27027772</identifier><identifier>CODEN: MREDEE</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Animals ; Fish Proteins - genetics ; Fish Proteins - metabolism ; Male ; Oreochromis niloticus ; Sex Determination Processes - physiology ; Teleostei ; Testis - embryology ; Tilapia ; Tilapia - embryology ; Tilapia - genetics ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transforming Growth Factor beta - genetics ; Transforming Growth Factor beta - metabolism</subject><ispartof>Molecular reproduction and development, 2016-06, Vol.83 (6), p.497-508</ispartof><rights>2016 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4942-b275c44378ad4869813e294254d21b2752d976cbd84b05ac10d654e9a480cba03</citedby><cites>FETCH-LOGICAL-c4942-b275c44378ad4869813e294254d21b2752d976cbd84b05ac10d654e9a480cba03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fmrd.22642$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fmrd.22642$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,786,790,27957,27958,50923,51032</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27027772$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Dong-Neng</creatorcontrib><creatorcontrib>Yang, Hui-Hui</creatorcontrib><creatorcontrib>Li, Ming-Hui</creatorcontrib><creatorcontrib>Shi, Hong-Juan</creatorcontrib><creatorcontrib>Zhang, Xian-Bo</creatorcontrib><creatorcontrib>Wang, De-Shou</creatorcontrib><title>gsdf is a downstream gene of dmrt1 that functions in the male sex determination pathway of the Nile tilapia</title><title>Molecular reproduction and development</title><addtitle>Mol. Reprod. Dev</addtitle><description>SUMMARY
Gonadal soma‐derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation is lacking. In the present study, we knocked out tilapia gsdf using CRISPR/Cas9. F0 gsdf‐deficient XY fish with high mutation rate (≥58%) developed as intersex, with ovotestes 90 days after hatching (dah), and become completely sex‐reversed with ovaries at 180 and 240 dah. Those individuals with a low mutation rate (<58%) and XY gsdf+/− fish developed as males with normal testes. In F2 XY gsdf−/− fish, the gonads first expressed Dmrt1, which initiated the male pathway at 10 dah, then both male and female pathways were activated, as reflected by the simultaneous expression of Dmrt1 and Cyp19a1a in different cell populations at 18 dah, shifted to the female pathway expressing only Cyp19a1a at 36 dah, and finally developed into functional ovaries as adults. The male pathway and Dmrt1 expression was initiated, but failed to be maintained, in the absence of Gsdf. Aromatase‐inhibitor treatment from 10 to 35 dah, however, rescued the phenotype, resulting in XY gsdf−/− with normal testes that expressed Dmrt1 and Cyp11b2. In vitro promoter analyses demonstrated that Dmrt1 activated gsdf expression in a dose‐dependent manner in the presence of Sf1, even though Dmrt1 alone could not. Taken together, our results demonstrated that gsdf is a downstream gene of dmrt1. Gsdf probably inhibits estrogen production to trigger testicular differentiation. Mol. Reprod. Dev. 83: 497–508, 2016. © 2016 Wiley Periodicals, Inc.</description><subject>Animals</subject><subject>Fish Proteins - genetics</subject><subject>Fish Proteins - metabolism</subject><subject>Male</subject><subject>Oreochromis niloticus</subject><subject>Sex Determination Processes - physiology</subject><subject>Teleostei</subject><subject>Testis - embryology</subject><subject>Tilapia</subject><subject>Tilapia - embryology</subject><subject>Tilapia - genetics</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transforming Growth Factor beta - genetics</subject><subject>Transforming Growth Factor beta - metabolism</subject><issn>1040-452X</issn><issn>1098-2795</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNqFkU9PFTEUxRuCAUQXfAHShI0uBm477bRdElQ0IgajeeyazrQDhfnzbDt5vG9vxwcsTIir29zzOye5PQgdEDgmAPSkD_aY0orRLbRHQMmCCsW35zeDgnF6vYtex3gHAEpJ2EG7VAAVQtA9dH8TbYt9xAbbcTXEFJzp8Y0bHB5bbPuQCE63JuF2GprkxyFiP-SNw73pHI7uAVuXXOj9YGYZL026XZn17J6pS5-p5Duz9OYNetWaLrq3j3Mf_fr08efZ5-Li-_mXs9OLomGK0aKmgjeMlUIay2SlJCkdzQJnlpJZpFaJqqmtZDVw0xCwFWdOGSahqQ2U--jdJncZxt-Ti0n3Pjau68zgxilqIglRUJYV_z8qlKKgqCIZPfoHvRunMORDZkpSKYHPge83VBPGGINr9TL43oS1JqDnsnQuS_8tK7OHj4lT3Tv7TD61k4GTDbDKv7h-OUl_-_HhKbLYOHxM7uHZYcK9rkQpuF5cnusrdr24EvyrXpR_AKXiq1w</recordid><startdate>201606</startdate><enddate>201606</enddate><creator>Jiang, Dong-Neng</creator><creator>Yang, Hui-Hui</creator><creator>Li, Ming-Hui</creator><creator>Shi, Hong-Juan</creator><creator>Zhang, Xian-Bo</creator><creator>Wang, De-Shou</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</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>7QP</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201606</creationdate><title>gsdf is a downstream gene of dmrt1 that functions in the male sex determination pathway of the Nile tilapia</title><author>Jiang, Dong-Neng ; Yang, Hui-Hui ; Li, Ming-Hui ; Shi, Hong-Juan ; Zhang, Xian-Bo ; Wang, De-Shou</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4942-b275c44378ad4869813e294254d21b2752d976cbd84b05ac10d654e9a480cba03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Fish Proteins - genetics</topic><topic>Fish Proteins - metabolism</topic><topic>Male</topic><topic>Oreochromis niloticus</topic><topic>Sex Determination Processes - physiology</topic><topic>Teleostei</topic><topic>Testis - embryology</topic><topic>Tilapia</topic><topic>Tilapia - embryology</topic><topic>Tilapia - genetics</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Transforming Growth Factor beta - genetics</topic><topic>Transforming Growth Factor beta - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiang, Dong-Neng</creatorcontrib><creatorcontrib>Yang, Hui-Hui</creatorcontrib><creatorcontrib>Li, Ming-Hui</creatorcontrib><creatorcontrib>Shi, Hong-Juan</creatorcontrib><creatorcontrib>Zhang, Xian-Bo</creatorcontrib><creatorcontrib>Wang, De-Shou</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>Calcium & Calcified Tissue Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular reproduction and development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Dong-Neng</au><au>Yang, Hui-Hui</au><au>Li, Ming-Hui</au><au>Shi, Hong-Juan</au><au>Zhang, Xian-Bo</au><au>Wang, De-Shou</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>gsdf is a downstream gene of dmrt1 that functions in the male sex determination pathway of the Nile tilapia</atitle><jtitle>Molecular reproduction and development</jtitle><addtitle>Mol. Reprod. Dev</addtitle><date>2016-06</date><risdate>2016</risdate><volume>83</volume><issue>6</issue><spage>497</spage><epage>508</epage><pages>497-508</pages><issn>1040-452X</issn><eissn>1098-2795</eissn><coden>MREDEE</coden><notes>China Postdoctoral Science Foundation - No. 2015M570765</notes><notes>Fundamental Research Funds for the Central Universities in China - No. XDJK2013D019</notes><notes>ArticleID:MRD22642</notes><notes>Chongqing Postdoctoral Science Foundation - No. Xm2015028</notes><notes>Chongqing Science and Technology Commission - No. cstc2015jcyjB80001; No. cstc2013kjrc-tdjs80003</notes><notes>863 program of China - No. 2011AA100404</notes><notes>ark:/67375/WNG-Q4XWQ75K-W</notes><notes>istex:565CBFB79CC28456B6140D2390DF5DDFA8C7E74C</notes><notes>Specialized Research Fund for the Doctoral Program of Higher Education of China - No. 20130182130003</notes><notes>NSFC of China - No. 91331119; No. 31030063</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>SUMMARY
Gonadal soma‐derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation is lacking. In the present study, we knocked out tilapia gsdf using CRISPR/Cas9. F0 gsdf‐deficient XY fish with high mutation rate (≥58%) developed as intersex, with ovotestes 90 days after hatching (dah), and become completely sex‐reversed with ovaries at 180 and 240 dah. Those individuals with a low mutation rate (<58%) and XY gsdf+/− fish developed as males with normal testes. In F2 XY gsdf−/− fish, the gonads first expressed Dmrt1, which initiated the male pathway at 10 dah, then both male and female pathways were activated, as reflected by the simultaneous expression of Dmrt1 and Cyp19a1a in different cell populations at 18 dah, shifted to the female pathway expressing only Cyp19a1a at 36 dah, and finally developed into functional ovaries as adults. The male pathway and Dmrt1 expression was initiated, but failed to be maintained, in the absence of Gsdf. Aromatase‐inhibitor treatment from 10 to 35 dah, however, rescued the phenotype, resulting in XY gsdf−/− with normal testes that expressed Dmrt1 and Cyp11b2. In vitro promoter analyses demonstrated that Dmrt1 activated gsdf expression in a dose‐dependent manner in the presence of Sf1, even though Dmrt1 alone could not. Taken together, our results demonstrated that gsdf is a downstream gene of dmrt1. Gsdf probably inhibits estrogen production to trigger testicular differentiation. Mol. Reprod. Dev. 83: 497–508, 2016. © 2016 Wiley Periodicals, Inc.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>27027772</pmid><doi>10.1002/mrd.22642</doi><tpages>12</tpages></addata></record> |
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| ispartof | Molecular reproduction and development, 2016-06, Vol.83 (6), p.497-508 |
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| subjects | Animals Fish Proteins - genetics Fish Proteins - metabolism Male Oreochromis niloticus Sex Determination Processes - physiology Teleostei Testis - embryology Tilapia Tilapia - embryology Tilapia - genetics Transcription Factors - genetics Transcription Factors - metabolism Transforming Growth Factor beta - genetics Transforming Growth Factor beta - metabolism |
| title | gsdf is a downstream gene of dmrt1 that functions in the male sex determination pathway of the Nile tilapia |
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