Cyprinid Juji (Gobiocypris rarus) as a model fish to study germ cell development and gonadal differentiation

cyprinid-juji-(gobiocypris-rarus)-as-a-model-fish-to-study-germ-cell-development-and-gonadal-differentiation
Cyprinid Juji (Gobiocypris rarus) as a model fish to study germ cell development and gonadal differentiation

References

  1. Nagahama, Y., Chakraborty, T., Paul-Prasanth, B., Ohta, K. & Nakamura, M. Sex determination, gonadal sex differentiation, and plasticity in vertebrate species. Physiol. Rev. 101, 1237–1308 (2021).

    Google Scholar 

  2. Li, J. & Ge, W. Zebrafish as a model for studying ovarian development: Recent advances from targeted gene knockout studies. Mol. Cell Endocrinol. 507, 110778 (2020).

    Google Scholar 

  3. Ren, Z. et al. foxl2l is a germ cell-intrinsic gatekeeper of oogenesis in zebrafish. Zool. Res. 45, 1116–1130 (2024).

    Google Scholar 

  4. Kossack, M. E. & Draper, B. W. Genetic regulation of sex determination and maintenance in zebrafish (Danio rerio). Curr. Top. Dev. Biol. 134, 119–149 (2019).

    Google Scholar 

  5. Wang, X., Bártfai, R., Sleptsova-Freidrich, I. & Orbán, L. The timing and extent of ‘juvenile ovary’ phase are highly variable during zebrafish testis differentiation. J. Fish. Biol. 70, 33–44 (2007).

    Google Scholar 

  6. Zhang, Q. et al. Zebrafish cyp11c1 Knockout Reveals the Roles of 11-ketotestosterone and Cortisol in Sexual Development and Reproduction. Endocrinology 161, https://doi.org/10.1210/endocr/bqaa048 (2020).

  7. Aharon, D. & Marlow, F. L. Sexual determination in zebrafish. Cell Mol. Life Sci 79, 8 (2021).

    Google Scholar 

  8. Wilson, C. A. et al. Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. Genetics 198, 1291–1308 (2014).

    Google Scholar 

  9. Siegfried, K. R. & Nüsslein-Volhard, C. Germ line control of female sex determination in zebrafish. Dev. Biol. 324, 277–287 (2008).

    Google Scholar 

  10. Ye, D. et al. Abundance of Early Embryonic Primordial Germ Cells Promotes Zebrafish Female Differentiation as Revealed by Lifetime Labeling of Germline. Mar. Biotechnol. 21, 217–228 (2019).

    Google Scholar 

  11. Dranow, D. B., Tucker, R. P. & Draper, B. W. Germ cells are required to maintain a stable sexual phenotype in adult zebrafish. Dev. Biol. 376, 43–50 (2013).

    Google Scholar 

  12. Tzung, K. W. et al. Early depletion of primordial germ cells in zebrafish promotes testis formation. Stem Cell Rep 4, 61–73 (2015).

    Google Scholar 

  13. Houwing, S. et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129, 69–82 (2007).

    Google Scholar 

  14. Zhang, R. et al. A germline-specific regulator of mitochondrial fusion is required for maintenance and differentiation of germline stem and progenitor cells. Adv. Sci. 9, e2203631 (2022).

    Google Scholar 

  15. Wu, K. et al. Genetic evidence for differential functions of figla and nobox in zebrafish ovarian differentiation and folliculogenesis. Commun. Biol. 6, 1185 (2023).

    Google Scholar 

  16. Xiong, X., Luo, S., Wu, B. & Wang, J. Comparative Developmental Toxicity and Stress Protein Responses of Dimethyl Sulfoxide to Rare Minnow and Zebrafish Embryos/Larvae. Zebrafish 14, 60–68 (2017).

    Google Scholar 

  17. Bai, Y. et al. Species and Life-Stage Sensitivity of Chinese Rare Minnow (Gobiocypris rarus) to Chemical Exposure: A Critical Review. Environ. Toxicol. Chem. 40, 2680–2692 (2021).

    Google Scholar 

  18. Liang, X. & Zha, J. Toxicogenomic applications of Chinese rare minnow (Gobiocypris rarus) in aquatic toxicology. Comp. Biochem Physiol. Part D. Genomics Proteom. 19, 174–180 (2016).

    Google Scholar 

  19. Hu, X. et al. Genomic deciphering of sex determination and unique immune system of a potential model species rare minnow (Gobiocypris rarus). Sci. Adv. 8, eabl7253 (2022).

    Google Scholar 

  20. Zhang, F. et al. Surrogate production of genome-edited sperm from a different subfamily by spermatogonial stem cell transplantation. Sci. China Life Sci 65, 969–987 (2022).

    Google Scholar 

  21. Wang, X. et al. Induced formation of primordial germ cells from zebrafish blastomeres by germplasm factors. Nat. Commun. 14, 7918 (2023).

    Google Scholar 

  22. Xu, C., Cao, Y. & Bao, J. Building RNA-protein germ granules: insights from the multifaceted functions of DEAD-box helicase Vasa/Ddx4 in germline development. Cell Mol. Life Sci 79, 4 (2021).

    Google Scholar 

  23. Hay, B., Jan, L. Y. & Jan, Y. N. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55, 577–587 (1988).

    Google Scholar 

  24. Raz, E. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1, REVIEWS1017 (2000).

    Google Scholar 

  25. Knaut, H., Pelegri, F., Bohmann, K., Schwarz, H. & Nüsslein-Volhard, C. Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J. Cell Biol. 149, 875–888 (2000).

    Google Scholar 

  26. Krøvel, A. V. & Olsen, L. C. Expression of a vas::EGFP transgene in primordial germ cells of the zebrafish. Mech. Dev. 116, 141–150 (2002).

    Google Scholar 

  27. Tanaka, M., Kinoshita, M., Kobayashi, D. & Nagahama, Y. Establishment of medaka (Oryzias latipes) transgenic lines with the expression of green fluorescent protein fluorescence exclusively in germ cells: a useful model to monitor germ cells in a live vertebrate. Proc. Natl. Acad. Sci. USA 98, 2544–2549 (2001).

    Google Scholar 

  28. Yoshizaki, G., Takeuchi, Y., Sakatani, S. & Takeuchi, T. Germ cell-specific expression of green fluorescent protein in transgenic rainbow trout under control of the rainbow trout vasa-like gene promoter. Int. J. Dev. Biol. 44, 323–326 (2000).

    Google Scholar 

  29. Krøvel, A. V. & Olsen, L. C. Sexual dimorphic expression pattern of a splice variant of zebrafish vasa during gonadal development. Dev. Biol. 271, 190–197 (2004).

    Google Scholar 

  30. Nishimura, T. et al. Sex determination. foxl3 is a germ cell-intrinsic factor involved in sperm-egg fate decision in medaka. Science 349, 328–331 (2015).

    Google Scholar 

  31. Yan, Y.-L. et al. A Hormone That Lost Its Receptor: Anti-Müllerian Hormone (AMH) in Zebrafish Gonad Development and Sex Determination. Genetics 213, 529–553 (2019).

    Google Scholar 

  32. Zhang, Z., Wu, K., Ren, Z. & Ge, W. Genetic evidence for Amh modulation of gonadotropin actions to control gonadal homeostasis and gametogenesis in zebrafish and its noncanonical signaling through Bmpr2a receptor. Development 147, https://doi.org/10.1242/dev.189811 (2020).

  33. Lin, Q. et al. Distinct and Cooperative Roles of amh and dmrt1 in Self-Renewal and Differentiation of Male Germ Cells in Zebrafish. Genetics 207, 1007–1022 (2017).

    Google Scholar 

  34. Nanda, I. et al. 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 (2002).

    Google Scholar 

  35. Webster, K. A. et al. Dmrt1 is necessary for male sexual development in zebrafish. Dev. Biol. 422, 33–46 (2017).

    Google Scholar 

  36. Herpin, A. & Schartl, M. Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J. 278, 1010–1019 (2011).

    Google Scholar 

  37. Rey, R. A. & Grinspon, R. P. Anti-Müllerian hormone, testicular descent and cryptorchidism. Front Endocrinol. (Lausanne) 15, 1361032 (2024).

    Google Scholar 

  38. Shang, G. et al. Steroidogenic acute regulatory protein and luteinizing hormone are required for normal ovarian steroidogenesis and oocyte maturation in zebrafish. Biol. Reprod. 101, 760–770 (2019).

    Google Scholar 

  39. Zirkin, B. R. & Papadopoulos, V. Leydig cells: formation, function, and regulation. Biol. Reprod. 99, 101–111 (2018).

    Google Scholar 

  40. Zhai, G. et al. Characterization of Sexual Trait Development in cyp17a1-Deficient Zebrafish. Endocrinology 159, 3549–3562 (2018).

    Google Scholar 

  41. Tanaka, M. Germline stem cells are critical for sexual fate decision of germ cells. Bioessays 38, 1227–1233 (2016).

    Google Scholar 

  42. Gross-Thebing, T. & Raz, E. Dead end and Detour: The function of the RNA-binding protein Dnd in posttranscriptional regulation in the germline. Curr. Top. Dev. Biol. 140, 181–208 (2020).

    Google Scholar 

  43. Wu, Y.-K. & Fan, H.-Y. Revisiting ZAR proteins: the understudied regulator of female fertility and beyond. Cell Mol. Life Sci 79, 92 (2022).

    Google Scholar 

  44. Shi, D.-L. Interplay of RNA-binding proteins controls germ cell development in zebrafish. J. Genet Genomics 51, 889–899 (2024).

    Google Scholar 

  45. Yang, Y.-J., Wang, Y., Li, Z., Zhou, L. & Gui, J.-F. Sequential, Divergent, and Cooperative Requirements of Foxl2a and Foxl2b in Ovary Development and Maintenance of Zebrafish. Genetics 205, 1551–1572 (2017).

    Google Scholar 

  46. Costa, Y. & Cooke, H. J. Dissecting the mammalian synaptonemal complex using targeted mutations. Chromosome Res 15, 579–589 (2007).

    Google Scholar 

  47. Biswas, L. et al. Meiosis interrupted: the genetics of female infertility via meiotic failure. Reproduction 161, R13–R35 (2021).

    Google Scholar 

  48. Qin, Y., Jiao, X., Simpson, J. L. & Chen, Z.-J. Genetics of primary ovarian insufficiency: new developments and opportunities. Hum. Reprod. Update 21, 787–808 (2015).

    Google Scholar 

  49. de Boer, E. & Heyting, C. The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115, 220–234 (2006).

    Google Scholar 

  50. Strunnikov, A. Cohesin complexes with a potential to link mammalian meiosis to cancer. Cell Regen 2, 4 (2013).

    Google Scholar 

  51. Ito, M., Fujita, Y. & Shinohara, A. Positive and negative regulators of RAD51/DMC1 in homologous recombination and DNA replication. DNA Repair 134, 103613 (2024).

    Google Scholar 

  52. San Filippo, J., Sung, P. & Klein, H. Mechanism of eukaryotic homologous recombination. Annu Rev. Biochem 77, 229–257 (2008).

    Google Scholar 

  53. Li, X.-Y., Mei, J., Ge, C.-T., Liu, X.-L. & Gui, J.-F. Sex determination mechanisms and sex control approaches in aquaculture animals. Sci. China Life Sci 65, 1091–1122 (2022).

    Google Scholar 

  54. Kikuchi, M. et al. Novel components of germline sex determination acting downstream of foxl3 in medaka. Dev. Biol. 445, 80–89 (2019).

    Google Scholar 

  55. Kikuchi, M., Nishimura, T., Ishishita, S., Matsuda, Y. & Tanaka, M. foxl3, a sexual switch in germ cells, initiates two independent molecular pathways for commitment to oogenesis in medaka. Proc. Natl. Acad. Sci. USA 117, 12174–12181 (2020).

    Google Scholar 

  56. Dai, S. et al. Germline sexual fate is determined by the antagonistic action of dmrt1 and foxl3/foxl2 in tilapia. Development 148, https://doi.org/10.1242/dev.199380 (2021).

  57. Josso, N. & di Clemente, N. TGF-beta Family Members and Gonadal Development. Trends Endocrinol. Metab. 10, 216–222 (1999).

    Google Scholar 

  58. Grinspon, R. P., Bergadá, I. & Rey, R. A. Male Hypogonadism and Disorders of Sex. Development. Front Endocrinol. (Lausanne) 11, 211 (2020).

    Google Scholar 

  59. Li, M. et al. 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 (2015).

    Google Scholar 

  60. Zhang, Z., Zhu, B., Chen, W. & Ge, W. Anti-Müllerian hormone (Amh/amh) plays dual roles in maintaining gonadal homeostasis and gametogenesis in zebrafish. Mol. Cell Endocrinol. 517, 110963 (2020).

    Google Scholar 

  61. Morinaga, C. et al. 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, 9691–9696 (2007).

    Google Scholar 

  62. Nakamura, S. et al. Hyperproliferation of mitotically active germ cells due to defective anti-Müllerian hormone signaling mediates sex reversal in medaka. Development 139, 2283–2287 (2012).

    Google Scholar 

  63. Yi, W., Ross, J. M. & Zarkower, D. Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development 127, 4469–4480 (2000).

    Google Scholar 

  64. Matsuda, M. et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417, 559–563 (2002).

    Google Scholar 

  65. Masuyama, H. et al. Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosome Res. 20, 163–176 (2012).

    Google Scholar 

  66. Lewis, Z. R., McClellan, M. C., Postlethwait, J. H., Cresko, W. A. & Kaplan, R. H. Female-specific increase in primordial germ cells marks sex differentiation in threespine stickleback (Gasterosteus aculeatus). J. Morphol. 269, 909–921 (2008).

    Google Scholar 

  67. Li, Q., Fujii, W., Naito, K. & Yoshizaki, G. Application of dead end-knockout zebrafish as recipients of germ cell transplantation. Mol. Reprod. Dev. 84, 1100–1111 (2017).

    Google Scholar 

  68. Saito, D. et al. Proliferation of germ cells during gonadal sex differentiation in medaka: Insights from germ cell-depleted mutant zenzai. Dev. Biol. 310, 280–290 (2007).

    Google Scholar 

  69. Ye, D. et al. Identification of fish spermatogenic cells through high-throughput immunofluorescence against testis with an antibody set. Front Endocrinol 14, 1044318 (2023).

    Google Scholar 

  70. Luzio, A., Santos, D., Monteiro, S. M. & Coimbra, A. M. Zebrafish male differentiation: Do all testes go through a “juvenile ovary” stage? Tissue Cell 72, 101545 (2021).

    Google Scholar 

  71. Lau, E. S.-W., Zhang, Z., Qin, M. & Ge, W. Knockout of Zebrafish Ovarian Aromatase Gene (cyp19a1a) by TALEN and CRISPR/Cas9 Leads to All-male Offspring Due to Failed Ovarian Differentiation. Sci. Rep. 6, 37357 (2016).

    Google Scholar 

  72. Nakamoto, M. et al. Ovarian aromatase loss-of-function mutant medaka undergo ovary degeneration and partial female-to-male sex reversal after puberty. Mol. Cell Endocrinol. 460, 104–122 (2018).

    Google Scholar 

  73. Zhang, F. et al. Efficient generation of zebrafish maternal-zygotic mutants through transplantation of ectopically induced and Cas9/gRNA targeted primordial germ cells. J. Genet Genomics 47, 37–47 (2020).

    Google Scholar 

  74. Li, Y. et al. Endogenous biosynthesis of docosahexaenoic acid (DHA) regulates fish oocyte maturation by promoting pregnenolone production. Zool. Res. 45, 176–188 (2024).

    Google Scholar 

  75. Chen, Z. et al. Intestinal DHA-PA-PG axis promotes digestive organ expansion by mediating usage of maternally deposited yolk lipids. Nat. Commun. 15, 9769 (2024).

    Google Scholar 

  76. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    Google Scholar 

  77. Wang, Y. et al. Cyp11a2 Is Essential for Oocyte Development and Spermatogonial Stem Cell Differentiation in Zebrafish. Endocrinology 163, https://doi.org/10.1210/endocr/bqab258 (2022).

  78. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15, 550 (2014).

    Google Scholar 

Download references