Dmrt1 is necessary for male sexual development in zebrafish

Agbor, 2012, A Wt1-Dmrt1 transgene restores DMRT1 to sertoli cells of Dmrt1-/- testes: * a novel model of DMRT1-deficient germ cells, Biol. Reprod., 88 Anderson, 2012, Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics, PLoS One, 7 Ayers, 2013, The molecular genetics of avian sex determination and its manipulation, Genesis, 51, 325, 10.1002/dvg.22382 Bradley, K.M., Breyer, J.P., Melville, D.B., Broman, K.W., Knapik, E.W., Smith, J.R., 2011. An SNP-Based Linkage Map for Zebrafish Reveals Sex Determination Loci. G3: Genes|Genomes|Genetics 1, 3–9. doi:10.1534/g3.111.000190. Cermak, 2011, Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting, Nucleic Acids Res., 39, e82, 10.1093/nar/gkr218 Chiang, 2001, Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites, Dev. Biol., 231, 149, 10.1006/dbio.2000.0129 Dahlem, 2012, Simple methods for generating and detecting, PLoS Genet., 8, e1002861, 10.1371/journal.pgen.1002861 Dranow, 2016, Bmp15 Is an oocyte-produced signal required for maintenance of the adult female sexual phenotype in Zebrafish, PLoS Genet., 12, e1006323, 10.1371/journal.pgen.1006323 Dranow, 2013, Germ cells are required to maintain a stable sexual phenotype in adult zebrafish, Dev. Biol., 376, 43, 10.1016/j.ydbio.2013.01.016 Eggers, 2014, Genetic regulation of mammalian gonad development, Nat. Rev. Endocrinol., 10, 673, 10.1038/nrendo.2014.163 Fujimoto, 2010, Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish, Proc. Natl. Acad. Sci. USA, 107, 17211, 10.1073/pnas.1007032107 Georges, 2014, The transcription factor FOXL2 mobilizes estrogen signaling to maintain the identity of ovarian granulosa cells, Elife, 3, e04207, 10.7554/eLife.04207 Goto, 2012, Germ cells are not the primary factor for sexual fate determination in goldfish, Dev. Biol., 370, 98, 10.1016/j.ydbio.2012.07.010 Guo, 2005, Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1, Biochem. Biophys. Res. Commun., 10.1016/j.bbrc.2005.03.066 Hattori, 2012, A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination, Proc. Natl. Acad. Sci., 109, 2955, 10.1073/pnas.1018392109 Herpin, 2009, A highly conserved cis-regulatory motif directs differential gonadal synexpression of Dmrt1 transcripts during gonad development, Nucleic Acids Res., 10.1093/nar/gkn1065 Howe, 2013, The zebrafish reference genome sequence and its relationship to the human genome, 496, 498 Kamiya, 2012, A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu), PLoS Genet., 8, e1002798, 10.1371/journal.pgen.1002798 Kanetsky, 2011, A second independent locus within DMRT1 is associated with testicular germ cell tumor susceptibility, Hum. Mol. Genet., 20, 3109, 10.1093/hmg/ddr207 Kim, 2007, Cell type-autonomous and non-autonomous requirements for Dmrt1 in postnatal testis differentiation, Dev. Biol., 307, 314, 10.1016/j.ydbio.2007.04.046 Kobayashi, 2004, Two DM domain genes, DMY DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes, Dev. Dyn., 231, 518, 10.1002/dvdy.20158 Kozielska, 2010, Segregation distortion and the evolution of sex-determining mechanisms, Heredity (Edinb.)., 104, 100, 10.1038/hdy.2009.104 Kratz, 2011, Variants in or near KITLG, BAK1, DMRT1, and TERT-CLPTM1L predispose to familial testicular germ cell tumour, J. Med. Genet., 48, 473, 10.1136/jmedgenet-2011-100001 Krentz, 2009, The DM domain protein DMRT1 is a dose-sensitive regulator of fetal germ cell proliferation and pluripotency, Proc. Natl. Acad. Sci. USA, 106, 22323, 10.1073/pnas.0905431106 Kurokawa, 2007, Germ cells are essential for sexual dimorphism in the medaka gonad, Proc. Natl. Acad. Sci. USA, 104, 16958, 10.1073/pnas.0609932104 Lambeth, 2014, Over-expression of DMRT1 induces the male pathway in embryonic chicken gonads, Dev. Biol., 10.1016/j.ydbio.2014.02.012 Leal, 2009, Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations, Biol. Reprod., 81, 177, 10.1095/biolreprod.109.076299 Li, 2013, Antagonistic roles of Dmrt1 and Foxl2 in sex differentiation via estrogen production in tilapia as demonstrated by TALENs, Endocrinology, 154, 4814, 10.1210/en.2013-1451 Li, 2015, A tandem duplicate of Anti-Müllerian Hormone with a Missense SNP on the Y chromosome is essential for male sex determination in Nile Tilapia, Oreochromis niloticus, PLoS Genet., 11, e1005678, 10.1371/journal.pgen.1005678 Liew, 2012, Polygenic sex determination system in zebrafish, PLoS One, 7 Liew, 2014, Zebrafish sex: a complicated affair, Brief. Funct. Genom., 13, 172, 10.1093/bfgp/elt041 Lindeman, 2015, Sexual cell-fate reprogramming in the ovary by DMRT1, Curr. Biol., 25, 764, 10.1016/j.cub.2015.01.034 Luzio, 2015, Screening and identification of potential sex-associated sequences in Danio rerio, Mol. Reprod. Dev., 82, 756, 10.1002/mrd.22508 Luzio, 2015, Screening and identification of potential sex-associated sequences in Danio rerio, Mol. Reprod. Dev., 10.1002/mrd.22508 Maack, 2003, Morphological development of the gonads in zebrafish, J. Fish. Biol., 10.1046/j.1095-8649.2003.00074.x Masuyama, 2012, Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka, Chromosom. Res., 20, 163, 10.1007/s10577-011-9264-x Matson, 2011, DMRT1 prevents female reprogramming in the postnatal mammalian testis, Nature, 476, 101, 10.1038/nature10239 Matson, 2012, Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity, Nat. Rev. Genet., 10.1038/nrg3161 Matsuda, 2002, DMY is a Y-specific DM-domain gene required for male development in the medaka fish, Nature, 10.1038/nature751 Matsuda, 2007, DMY gene induces male development in genetically female (XX) medaka fish, Proc. Natl. Acad. Sci. USA, 104, 3865, 10.1073/pnas.0611707104 McMillan, 2015, Pectoral fin breeding tubercle clusters: a method to determine zebrafish sex, Zebrafish, 12, 121, 10.1089/zeb.2014.1060 Morinaga, 2007, The hotei mutation of medaka in the anti-Mullerian hormone receptor causes the dysregulation of germ cell and sexual development, Proc. Natl. Acad. Sci. USA, 104, 9691, 10.1073/pnas.0611379104 Murphy, 2010, Genome-wide analysis of DNA binding and transcriptional regulation by the mammalian doublesex homolog DMRT1 in the juvenile testis: editorial comment, Proc. Natl. Acad. Sci. USA, 107, 13360, 10.1073/pnas.1006243107 Nakamura, 2012, Hyperproliferation of mitotically active germ cells due to defective anti-Mullerian hormone signaling mediates sex reversal in medaka, Development, 139, 2283, 10.1242/dev.076307 Nanda, 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, 10.1073/pnas.182314699 Nishimura, 2015, Sex determination. foxl3 is a germ cell-intrinsic factor involved in sperm-egg fate decision in medaka, Science, 349, 328, 10.1126/science.aaa2657 Pfaffl, 2001, A new mathematical model for relative quantification in real-time RT-PCR, Nucleic Acids Res., 29, e45, 10.1093/nar/29.9.e45 Picard, 2015, The roles of Dmrt (Double sex/male-abnormal-3 related transcription factor) genes in sex determination and differentiation mechanisms: ubiquity and diversity across the animal kingdom, C. R. Biol., 338, 451, 10.1016/j.crvi.2015.04.010 Pradhan, 2012, Activation of NF-κB protein prevents the transition from juvenile ovary to testis and promotes ovarian development in Zebrafish, J. Biol. Chem., 287, 37926, 10.1074/jbc.M112.386284 Rodríguez-Marí, 2010, Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis, PLoS Genet., 6, e1001034, 10.1371/journal.pgen.1001034 Rodríguez-Marí, 2005, Characterization and expression pattern of zebrafish anti-Müllerian hormone (amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development, Gene Expr. Patterns, 10.1016/j.modgep.2005.02.008 Salz, 2010 Schulz, 2007, Estrogen-induced alterations in amh and dmrt1 expression signal for disruption in male sexual development in the Zebrafish estrogen-induced alterations in amh and dmrt1 expression signal for disruption in male sexual development in the Zebrafish, Environ. Sci. Technol., 41, 6305, 10.1021/es070785+ Selman, 1993, Stages of oocyte development in the zebrafish, Brachydanio rerio,, J. Morphol., 218, 203, 10.1002/jmor.1052180209 Siegfried, 2008, Germ line control of female sex determination in Zebrafish, Dev. Biol., 324, 277, 10.1016/j.ydbio.2008.09.025 Slanchev, 2005, Development without germ cells: the role of the germ line in Zebrafish sex differentiation, Proc. Natl. Acad. Sci. USA, 10.1073/pnas.0407475102 Smith, 2008, Gene expression analysis on sections of zebrafish regenerating fins reveals limitations in the whole-mount in situ hybridization method, Dev. Dyn., 237, 417, 10.1002/dvdy.21417 Smith, 2009, The avian Z-linked gene DMRT1 is required for male sex determination in the chicken, Nature, 461, 267, 10.1038/nature08298 Sreenivasan, 2014, Gonad differentiation in zebrafish is regulated by the canonical Wnt signaling pathway, Biol. Reprod., 90, 45, 10.1095/biolreprod.113.110874 Takahashi, 1977, Juvenile hermaphroditism in the Zebrafish, Brachydanio rerio, Bull. Fac. Fish. (Hokkaido Univ.), 28, 57 Tang, 2007, Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization, Acta Biochim. Biophys. Sin. (Shanghai), 39, 384, 10.1111/j.1745-7270.2007.00283.x Trukhina, 2013, The variety of vertebrate mechanisms of sex determination, Biomed. Res. Int., 2013, 587460, 10.1155/2013/587460 Tzung, 2015, Early depletion of primordial germ cells in Zebrafish promotes testis formation, Stem Cell Rep., 4, 61, 10.1016/j.stemcr.2014.10.011 Uchida, 2002, Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish, J. Exp. Biol., 10.1242/jeb.205.6.711 Uhlenhaut, 2009, Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation, Cell, 139, 1130, 10.1016/j.cell.2009.11.021 Verhulst, 2015, Double nexus–Doublesex is the connecting element in sex determination, Brief. Funct. Genom., 1 Wang, 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, 10.1210/me.2006-0248 Wang, 2007, The timing and extent of “juvenile ovary” phase are highly variable during zebrafish testis differentiation, J. Fish. Biol., 70, 33, 10.1111/j.1095-8649.2007.01363.x Wang, 2007, Anti-Müllerian hormone and 11 beta-hydroxylase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males, Dev. Dyn., 236, 1329, 10.1002/dvdy.21129 Weidinger, 2003, dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival, Curr. Biol., 13, 1429, 10.1016/S0960-9822(03)00537-2 Wilson, 2014, Wild sex in Zebrafish: loss of the natural sex determinant in domesticated strains, Genetics, 10.1534/genetics.114.169284 Yamamoto, 1969, Sex differentiation, Vol. III, 117 Yoshimoto, 2011, A ZZ/ZW-type sex determination in xenopus laevis, FEBS J., 10.1111/j.1742-4658.2011.08031.x Zhao, 2015, Female-to-male sex reversal in mice caused by transgenic overexpression of Dmrt1, Development, 142, 1083