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 Vol. 83; no. 6; pp. 497 - 508 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Blackwell Publishing Ltd
01.06.2016
Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1040-452X 1098-2795 1098-2795 |
| DOI | 10.1002/mrd.22642 |
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| 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. |
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| AbstractList | 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. 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.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. 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. 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 ( greater than or equal to 58%) developed as intersex, with ovotestes 90 days after hatching (dah), and become completely sex-reversed with ovaries at 180 and 240dah. Those individuals with a low mutation rate (<58%) and XY gsdf super(+/-) fish developed as males with normal testes. In F2 XY gsdf super(-/-) fish, the gonads first expressed Dmrt1, which initiated the male pathway at 10dah, then both male and female pathways were activated, as reflected by the simultaneous expression of Dmrt1 and Cyp19a1a in different cell populations at 18dah, shifted to the female pathway expressing only Cyp19a1a at 36dah, 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 35dah, however, rescued the phenotype, resulting in XY gsdf super(-/-) 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. copyright 2016 Wiley Periodicals, Inc. 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 240dah. 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 10dah, then both male and female pathways were activated, as reflected by the simultaneous expression of Dmrt1 and Cyp19a1a in different cell populations at 18dah, shifted to the female pathway expressing only Cyp19a1a at 36dah, 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 35dah, 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. |
| Author | Shi, Hong-Juan Li, Ming-Hui Wang, De-Shou Zhang, Xian-Bo Yang, Hui-Hui Jiang, Dong-Neng |
| Author_xml | – sequence: 1 givenname: Dong-Neng surname: Jiang fullname: Jiang, Dong-Neng organization: Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing, Beibei, China – sequence: 2 givenname: Hui-Hui surname: Yang fullname: Yang, Hui-Hui organization: Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing, Beibei, China – sequence: 3 givenname: Ming-Hui surname: Li fullname: Li, Ming-Hui organization: Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing, Beibei, China – sequence: 4 givenname: Hong-Juan surname: Shi fullname: Shi, Hong-Juan organization: Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing, Beibei, China – sequence: 5 givenname: Xian-Bo surname: Zhang fullname: Zhang, Xian-Bo organization: Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing, Beibei, China – sequence: 6 givenname: De-Shou surname: Wang fullname: Wang, De-Shou email: Corresponding author:Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education)Key Laboratory of Aquatic Science of ChongqingSchool of Life SciencesSouthwest UniversityNo. 1 Tianshen Road, BeibeiChongqing 400715, China., wdeshou@swu.edu.cn organization: Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing, Beibei, China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27027772$$D View this record in MEDLINE/PubMed |
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| Notes | China Postdoctoral Science Foundation - No. 2015M570765 Fundamental Research Funds for the Central Universities in China - No. XDJK2013D019 ArticleID:MRD22642 Chongqing Postdoctoral Science Foundation - No. Xm2015028 Chongqing Science and Technology Commission - No. cstc2015jcyjB80001; No. cstc2013kjrc-tdjs80003 863 program of China - No. 2011AA100404 ark:/67375/WNG-Q4XWQ75K-W istex:565CBFB79CC28456B6140D2390DF5DDFA8C7E74C Specialized Research Fund for the Doctoral Program of Higher Education of China - No. 20130182130003 NSFC of China - No. 91331119; No. 31030063 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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| PublicationDate | June 2016 |
| PublicationDateYYYYMMDD | 2016-06-01 |
| PublicationDate_xml | – month: 06 year: 2016 text: June 2016 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: Hoboken |
| PublicationTitle | Molecular reproduction and development |
| PublicationTitleAlternate | Mol. Reprod. Dev |
| PublicationYear | 2016 |
| Publisher | Blackwell Publishing Ltd Wiley Subscription Services, Inc |
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| References | Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559-563. Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, Matsuda M, Nagahama Y. 2010. Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr Patterns 10:283-289. Chakraborty T, Zhou LY, Chaudhari A, Iguchi T, Nagahama Y. 2016. Dmy initiates masculinity by altering Gsdf/Sox9a2/Rspo1 expression in medaka (Oryzias latipes). Sci Rep 6:19480. Reichwald K, Petzold A, Koch P, Downie BR, Hartmann N, Pietsch S, Baumgart M, Chalopin D, Felder M, Bens M, Sahm A, Szafranski K, Taudien S, Groth M, Arisi I, Weise A, Bhatt SS, Sharma JM, Kraus F, Schmid S, Priebe T, Liehr M, Gorlach ME, Than M, Hiller HA, Kestler V, Volff JN, Schartl M, Cellerino A, Englert C, Platzer M. 2015. Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell 163:1527-1538. Li M, Sun Y, Zhao J, Shi H, Zeng S, Ye K, Jiang D, Zhou L, Sun L, Tao W, Nagahama Y, Kocher TD, Wang D. 2015. A tandem duplicate of anti-mullerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile Tilapia, Oreochromis niloticus. PLoS Genet 11:e1005678. Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M. 2012. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191:163-170. D'Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller JF. 2001. Search for genes involved in the temperature-induced gonadal sex differentiation in the tilapia, Oreochromis niloticusa. J Exp Zool 290:574-585. Doghman M, Figueiredo BC, Volante M, Papotti M, Lalli E. 2013. Integrative analysis of SF-1 transcription factor dosage impact on genome-wide binding and gene expression regulation. Nucleic Acids Res 41:8896-8907. Gautier A, Sohm F, Joly JS, Le Gac F, Lareyre JJ. 2011. The proximal promoter region of the zebrafish gsdf gene is sufficient to mimic the spatio-temporal expression pattern of the endogenous gene in Sertoli and granulosa cells. Biol Reprod 85:1240-1251. Hatano O, Takayama K, Imai T, Waterman MR, Takakusu A, Omura T, Morohashi K. 1994. Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development 120:2787-2797. Sun LN, Jiang XL, Xie QP, Yuan J, Huang BF, Tao WJ, Zhou LY, Nagahama Y, Wang DS. 2014a. Transdifferentiation of differentiated ovary into functional testis by long-term treatment of aromatase inhibitor in Nile tilapia. Endocrinology 155:1476-1488. Kaneko H, Ijiri S, Kobayashi T, Izumi H, Kuramochi Y, Wang DS, Mizuno S, Nagahama Y. 2015. Gonadal soma-derived factor (gsdf), a TGF-beta superfamily gene, induces testis differentiation in the teleost fish Oreochromis niloticus. Mol Cell Endocrinol 415:87-99. Horiguchi R, Nozu R, Hirai T, Kobayashi Y, Nagahama Y, Nakamura M. 2013. Characterization of gonadal soma-derived factor expression during sex change in the protogynous wrasse, Halichoeres trimaculatus. Dev Dyn 242:388-399. Sawatari E, Shikina S, Takeuchi T, Yoshizaki G. 2007. A novel transforming growth factor-beta superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss). Dev Biol 301:266-275. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y. 2008. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78:333-341. Nakamoto M, Fukasawa M, Tanaka S, Shimamori K, Suzuki A, Matsuda M, Kobayashi T, Nagahama Y, Shibata N. 2012. Expression of 3β-hydroxysteroid dehydrogenase (hsd3b), star and ad4bp/sf-1 during gonadal development in medaka (Oryzias latipes). Gen Comp Endocrinol 176:222-230. Zhang Z, Zhu B, Ge W. 2015. Genetic analysis of zebrafish gonadotropin (FSH and LH) functions by TALEN-mediated gene disruption. Mol Endocrinol 29:76-98. Murphy MW, Zarkower D, Bardwell VJ. 2007. Vertebrate DM domain proteins bind similar DNA sequences and can heterodimerize on DNA. BMC Mol Biol 8:58. Ramayya MS, Zhou J, Kino T, Segars JH, Bondy CA, Chrousos GP. 1997. Steroidogenic factor 1 messenger ribonucleic acid expression in steroidogenic and nonsteroidogenic human tissues: Northern blot and in situ hybridization studies. J Clin Endocr Metab 82:1799-1806. Tao W, Yuan J, Zhou L, Sun L, Sun Y, Yang S, Li M, Zeng S, Huang B, Wang D. 2013. Characterization of gonadal transcriptomes from Nile tilapia (Oreochromis niloticus) reveals differentially expressed genes. PLoS ONE 8:e63604. Zhang X, Wang H, Li M, Cheng Y, Jiang D, Sun L, Tao W, Zhou L, Wang Z, Wang D. 2014. Isolation of doublesex- and mab-3-related transcription factor 6 and its involvement in spermatogenesis in tilapia. Biol Reprod 91:1-10. Li M, Yang H, Zhao J, Fang L, Shi H, Sun Y, Zhang X, Jiang D, Zhou L, Wang D. 2014. Efficient and heritable gene targeting in tilapia by CRISPR/Cas9. Genetics 197:591-599. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi K, Nagahama Y. 2007. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 21:712-725. Zhang X, Guan G, Li M, Zhu F, Liu Q, Naruse K, Herpin A, Nagahama Y, Li J, Hong Y. 2016. Autosomal gsdf acts as a male sex initiator in the fish medaka. Sci Rep 6:19738. Wang DS, Zhou LY, Kobayashi T, Matsuda M, Shibata Y, Sakai F, Nagahama Y. 2010. Doublesex- and Mab-3-related transcription factor-1 repression of aromatase transcription, a possible mechanism favoring the male pathway in tilapia. Endocrinology 151:1331-1340. Chen L, Jiang X, Feng H, Shi H, Sun L, Tao W, Xie Q, Wang D. 2016. Simultaneous exposure to estrogen and androgen resulted in feminization and endocrine disruption. J Endocrinol 228:205-218. Guiguen Y, Fostier A, Piferrer F, Chang CF. 2010. Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165:352-366. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. 2003. Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet Genome Res 101:289-294. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M. 2002. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99:11778-11783. Chen Y, Hong WS, Wang Q, Chen SX. 2015. Cloning and expression pattern of gsdf during the first maleness reproductive phase in the protandrous Acanthopagrus latus. Gen Comp Endocrinol 217-218:71-80. Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K. 2012. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet 8:e1002798. Sun YL, Jiang DN, Zeng S, Hu CJ, Ye K, Yang C, Yang SJ, Li MH, Wang DS. 2014b. Screening and characterization of sex-linked DNA markers and marker-assisted selection in the Nile tilapia (Oreochromis niloticus). Aquaculture 433:19-27. De Caestecker M. 2004. The transforming growth factor-β superfamily of receptors. Cytokine Growth Factor Rev 15:1-11. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strussmann CA. 2012. A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109:2955-2959. Rondeau EB, Messmer AM, Sanderson DS, Jantzen SG, von Schalburg KR, Minkley DR, Leong JS, Macdonald GM, Davidsen AE, Parker WA, Mazzola RS, Campbell B, Koop BF. 2013. Genomics of sablefish (Anoplopoma fimbria): Expressed genes, mitochondrial phylogeny, linkage map, and identification of a putative sex gene. BMC Genomics 14:452. Morohashi K, Iida H, Nomura M, Hatano O, Honda S-i, Tsukiyama T, Niwa O, Hara T, Takakusu A, Shibata Y. 1994. Functional difference between Ad4BP and ELP, and their distributions in steroidogenic tissues. Mol Endocrinol 8:643-653. Shi Y, Massagué J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700. Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y. 2004. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231:518-526. Imai T, Saino K, Matsuda M. 2015. Mutation of Gonadal soma-derived factor induces medaka XY gonads to undergo ovarian development. Biochem Bioph Res Commun 467:109-114. 2007; 301 2015; 163 2010; 10 2014; 91 1997; 82 2015; 467 2015; 217–218 2016; 228 2015; 11 2013; 41 2002; 99 2010; 165 2008; 78 2014a; 155 2013; 242 2002; 417 2013; 8 2003; 113 2014; 197 2012; 109 1994; 8 2016; 6 2004; 231 2012; 176 2013; 14 2015; 29 2001; 290 2000 2004; 15 1994; 120 2012; 191 2007; 8 2011; 85 2010; 151 2015; 415 2007; 21 2014b; 433 2003; 101 2012; 8 e_1_2_8_28_1 e_1_2_8_29_1 e_1_2_8_24_1 e_1_2_8_26_1 e_1_2_8_27_1 Nagahama Y (e_1_2_8_25_1) 2000 e_1_2_8_3_1 e_1_2_8_2_1 e_1_2_8_5_1 e_1_2_8_4_1 e_1_2_8_7_1 e_1_2_8_6_1 e_1_2_8_9_1 e_1_2_8_8_1 e_1_2_8_20_1 e_1_2_8_21_1 e_1_2_8_22_1 e_1_2_8_23_1 e_1_2_8_41_1 e_1_2_8_40_1 e_1_2_8_17_1 e_1_2_8_18_1 e_1_2_8_39_1 e_1_2_8_19_1 e_1_2_8_13_1 e_1_2_8_36_1 e_1_2_8_14_1 e_1_2_8_35_1 e_1_2_8_15_1 e_1_2_8_38_1 e_1_2_8_16_1 e_1_2_8_37_1 e_1_2_8_32_1 e_1_2_8_10_1 e_1_2_8_31_1 e_1_2_8_11_1 e_1_2_8_34_1 e_1_2_8_12_1 e_1_2_8_33_1 e_1_2_8_30_1 |
| References_xml | – reference: Wang DS, Zhou LY, Kobayashi T, Matsuda M, Shibata Y, Sakai F, Nagahama Y. 2010. Doublesex- and Mab-3-related transcription factor-1 repression of aromatase transcription, a possible mechanism favoring the male pathway in tilapia. Endocrinology 151:1331-1340. – reference: Tao W, Yuan J, Zhou L, Sun L, Sun Y, Yang S, Li M, Zeng S, Huang B, Wang D. 2013. Characterization of gonadal transcriptomes from Nile tilapia (Oreochromis niloticus) reveals differentially expressed genes. PLoS ONE 8:e63604. – reference: Imai T, Saino K, Matsuda M. 2015. Mutation of Gonadal soma-derived factor induces medaka XY gonads to undergo ovarian development. Biochem Bioph Res Commun 467:109-114. – reference: Sun YL, Jiang DN, Zeng S, Hu CJ, Ye K, Yang C, Yang SJ, Li MH, Wang DS. 2014b. Screening and characterization of sex-linked DNA markers and marker-assisted selection in the Nile tilapia (Oreochromis niloticus). Aquaculture 433:19-27. – reference: Rondeau EB, Messmer AM, Sanderson DS, Jantzen SG, von Schalburg KR, Minkley DR, Leong JS, Macdonald GM, Davidsen AE, Parker WA, Mazzola RS, Campbell B, Koop BF. 2013. Genomics of sablefish (Anoplopoma fimbria): Expressed genes, mitochondrial phylogeny, linkage map, and identification of a putative sex gene. BMC Genomics 14:452. – reference: Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strussmann CA. 2012. A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109:2955-2959. – reference: Reichwald K, Petzold A, Koch P, Downie BR, Hartmann N, Pietsch S, Baumgart M, Chalopin D, Felder M, Bens M, Sahm A, Szafranski K, Taudien S, Groth M, Arisi I, Weise A, Bhatt SS, Sharma JM, Kraus F, Schmid S, Priebe T, Liehr M, Gorlach ME, Than M, Hiller HA, Kestler V, Volff JN, Schartl M, Cellerino A, Englert C, Platzer M. 2015. Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell 163:1527-1538. – reference: Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M. 2002. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99:11778-11783. – reference: Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. 2003. Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet Genome Res 101:289-294. – reference: Chen Y, Hong WS, Wang Q, Chen SX. 2015. Cloning and expression pattern of gsdf during the first maleness reproductive phase in the protandrous Acanthopagrus latus. Gen Comp Endocrinol 217-218:71-80. – reference: Gautier A, Sohm F, Joly JS, Le Gac F, Lareyre JJ. 2011. The proximal promoter region of the zebrafish gsdf gene is sufficient to mimic the spatio-temporal expression pattern of the endogenous gene in Sertoli and granulosa cells. Biol Reprod 85:1240-1251. – reference: Morohashi K, Iida H, Nomura M, Hatano O, Honda S-i, Tsukiyama T, Niwa O, Hara T, Takakusu A, Shibata Y. 1994. Functional difference between Ad4BP and ELP, and their distributions in steroidogenic tissues. Mol Endocrinol 8:643-653. – reference: Chakraborty T, Zhou LY, Chaudhari A, Iguchi T, Nagahama Y. 2016. Dmy initiates masculinity by altering Gsdf/Sox9a2/Rspo1 expression in medaka (Oryzias latipes). Sci Rep 6:19480. – reference: D'Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller JF. 2001. Search for genes involved in the temperature-induced gonadal sex differentiation in the tilapia, Oreochromis niloticusa. J Exp Zool 290:574-585. – reference: Zhang X, Guan G, Li M, Zhu F, Liu Q, Naruse K, Herpin A, Nagahama Y, Li J, Hong Y. 2016. Autosomal gsdf acts as a male sex initiator in the fish medaka. Sci Rep 6:19738. – reference: Hatano O, Takayama K, Imai T, Waterman MR, Takakusu A, Omura T, Morohashi K. 1994. Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development 120:2787-2797. – reference: Sun LN, Jiang XL, Xie QP, Yuan J, Huang BF, Tao WJ, Zhou LY, Nagahama Y, Wang DS. 2014a. Transdifferentiation of differentiated ovary into functional testis by long-term treatment of aromatase inhibitor in Nile tilapia. Endocrinology 155:1476-1488. – reference: Murphy MW, Zarkower D, Bardwell VJ. 2007. Vertebrate DM domain proteins bind similar DNA sequences and can heterodimerize on DNA. BMC Mol Biol 8:58. – reference: Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M. 2012. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191:163-170. – reference: Kaneko H, Ijiri S, Kobayashi T, Izumi H, Kuramochi Y, Wang DS, Mizuno S, Nagahama Y. 2015. Gonadal soma-derived factor (gsdf), a TGF-beta superfamily gene, induces testis differentiation in the teleost fish Oreochromis niloticus. Mol Cell Endocrinol 415:87-99. – reference: Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, Matsuda M, Nagahama Y. 2010. Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr Patterns 10:283-289. – reference: Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y. 2004. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231:518-526. – reference: Chen L, Jiang X, Feng H, Shi H, Sun L, Tao W, Xie Q, Wang D. 2016. Simultaneous exposure to estrogen and androgen resulted in feminization and endocrine disruption. J Endocrinol 228:205-218. – reference: Zhang Z, Zhu B, Ge W. 2015. Genetic analysis of zebrafish gonadotropin (FSH and LH) functions by TALEN-mediated gene disruption. Mol Endocrinol 29:76-98. – reference: De Caestecker M. 2004. The transforming growth factor-β superfamily of receptors. Cytokine Growth Factor Rev 15:1-11. – reference: Guiguen Y, Fostier A, Piferrer F, Chang CF. 2010. Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165:352-366. – reference: Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y. 2008. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78:333-341. – reference: Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559-563. – reference: Li M, Yang H, Zhao J, Fang L, Shi H, Sun Y, Zhang X, Jiang D, Zhou L, Wang D. 2014. Efficient and heritable gene targeting in tilapia by CRISPR/Cas9. Genetics 197:591-599. – reference: Shi Y, Massagué J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700. – reference: Horiguchi R, Nozu R, Hirai T, Kobayashi Y, Nagahama Y, Nakamura M. 2013. Characterization of gonadal soma-derived factor expression during sex change in the protogynous wrasse, Halichoeres trimaculatus. Dev Dyn 242:388-399. – reference: Nakamoto M, Fukasawa M, Tanaka S, Shimamori K, Suzuki A, Matsuda M, Kobayashi T, Nagahama Y, Shibata N. 2012. Expression of 3β-hydroxysteroid dehydrogenase (hsd3b), star and ad4bp/sf-1 during gonadal development in medaka (Oryzias latipes). Gen Comp Endocrinol 176:222-230. – reference: Zhang X, Wang H, Li M, Cheng Y, Jiang D, Sun L, Tao W, Zhou L, Wang Z, Wang D. 2014. Isolation of doublesex- and mab-3-related transcription factor 6 and its involvement in spermatogenesis in tilapia. Biol Reprod 91:1-10. – reference: Doghman M, Figueiredo BC, Volante M, Papotti M, Lalli E. 2013. Integrative analysis of SF-1 transcription factor dosage impact on genome-wide binding and gene expression regulation. Nucleic Acids Res 41:8896-8907. – reference: Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi K, Nagahama Y. 2007. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 21:712-725. – reference: Sawatari E, Shikina S, Takeuchi T, Yoshizaki G. 2007. A novel transforming growth factor-beta superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss). Dev Biol 301:266-275. – reference: Ramayya MS, Zhou J, Kino T, Segars JH, Bondy CA, Chrousos GP. 1997. Steroidogenic factor 1 messenger ribonucleic acid expression in steroidogenic and nonsteroidogenic human tissues: Northern blot and in situ hybridization studies. J Clin Endocr Metab 82:1799-1806. – reference: Li M, Sun Y, Zhao J, Shi H, Zeng S, Ye K, Jiang D, Zhou L, Sun L, Tao W, Nagahama Y, Kocher TD, Wang D. 2015. A tandem duplicate of anti-mullerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile Tilapia, Oreochromis niloticus. PLoS Genet 11:e1005678. – reference: Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K. 2012. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet 8:e1002798. – volume: 11 start-page: e1005678 year: 2015 article-title: A tandem duplicate of anti‐mullerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile Tilapia, publication-title: PLoS Genet – start-page: 211 year: 2000 end-page: 222 – volume: 163 start-page: 1527 year: 2015 end-page: 1538 article-title: Insights into sex chromosome evolution and aging from the genome of a short‐lived fish publication-title: Cell – volume: 228 start-page: 205 year: 2016 end-page: 218 article-title: Simultaneous exposure to estrogen and androgen resulted in feminization and endocrine disruption publication-title: J Endocrinol – volume: 10 start-page: 283 year: 2010 end-page: 289 article-title: Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka publication-title: Gene Expr Patterns – volume: 176 start-page: 222 year: 2012 end-page: 230 article-title: Expression of 3β‐hydroxysteroid dehydrogenase (hsd3b), star and ad4bp/sf‐1 during gonadal development in medaka ( ) publication-title: Gen Comp Endocrinol – volume: 21 start-page: 712 year: 2007 end-page: 725 article-title: Foxl2 up‐regulates aromatase gene transcription in a female‐specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1 publication-title: Mol Endocrinol – volume: 191 start-page: 163 year: 2012 end-page: 170 article-title: Tracing the emergence of a novel sex‐determining gene in medaka, publication-title: Genetics – volume: 467 start-page: 109 year: 2015 end-page: 114 article-title: Mutation of Gonadal soma‐derived factor induces medaka XY gonads to undergo ovarian development publication-title: Biochem Bioph Res Commun – volume: 8 start-page: 58 year: 2007 article-title: Vertebrate DM domain proteins bind similar DNA sequences and can heterodimerize on DNA publication-title: BMC Mol Biol – volume: 8 start-page: 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Gonadal soma‐derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation... Gonadal soma-derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation is... SUMMARY Gonadal soma-derived factor (gsdf) is critical for testicular differentiation in teleosts, yet detailed analysis of Gsdf on testicular differentiation... |
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| SubjectTerms | 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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