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  • Review Article
  • Published:

Primordial germ-cell development: the zebrafish perspective

Nature Reviews Genetics volume 4, pages 690–700 (2003)Cite this article

Key Points

  • Primordial germ cells (PGCs) in zebrafish are specified by the inheritance of maternally provided cytoplasmic determinants, which are collectively known as the germ plasm.

  • Several molecules that are important for PGC development in zebrafish also have a role in germ-cell development in other organisms, invertebrates and vertebrates.

  • During the first day of embryonic development, PGCs migrate from the positions where they are formed towards their target — the somatic part of the gonad — where they differentiate into sperm and eggs.

  • During their migration, PGCs acquire directional cues from somatic cells that attract them towards their intermediate and final targets.

  • A crucial molecule that directs the migrating PGCs is the chemokine Sdf-1a, which is expressed in positions at which PGCs are found.

  • Reducing the level of Sdf-1a or its receptor Cxcr4b results in a severe PGC migration defect; conversely, expression of Sdf-1a in ectopic locations leads to accumulation of PGCs in those sites.

Abstract

Primordial germ cells follow a characteristic developmental path that is manifested in the specialized regulation of basic cell functions and behaviour. Recent studies in zebrafish have greatly enhanced our understanding of the mode of specification of primordial germ cells, cell-fate maintenance and the migration of these cells towards their target, the gonad, where they differentiate into gametes.

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Figure 1: Specification of zebrafish germ cells.
Figure 2: Migration and directional cues for germ cells.
Figure 3: Identification of the chemokine receptor Cxcr4b by genetic screens for genes that affect germ-cell migration.
Figure 4: The role of Cxcr4b and Sdf1a in germ-cell migration.

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References

  1. Seydoux, G. & Strome, S. Launching the germline in Caenorhabditis elegans: regulation of gene expression in early germ cells. Development 126, 3275–3283 (1999).

    CAS  PubMed  Google Scholar 

  2. Wylie, C. Germ cells. Curr. Opin. Genet. Dev. 10, 410–413 (2000).

    CAS  PubMed  Google Scholar 

  3. Starz-Gaiano, M. & Lehmann, R. Moving towards the next generation. Mech. Dev. 105, 5–18 (2001).

    CAS  PubMed  Google Scholar 

  4. Houston, D. & King, M. Germ plasm and molecular determinants of germ cell fate. Curr. Top. Dev. Biol. 50, 155–181 (2000).

    CAS  PubMed  Google Scholar 

  5. Saffman, E. & Lasko, P. Germline development in vertebrates and invertebrates. Cell. Mol. Life Sci. 55, 1141–1163 (1999).

    CAS  PubMed  Google Scholar 

  6. Raz, E. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1, 1017 (2000).

    Google Scholar 

  7. Kimmel, C. Genetics and early development of zebrafish. Trends Genet. 5, 283–288 (1989). This paper describes the genetic tools and general features of the zebrafish that make it a useful model organism for the study of vertebrate development.

    CAS  PubMed  Google Scholar 

  8. Haffter, P. et al. The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1–36 (1996).

    CAS  PubMed  Google Scholar 

  9. Driever, W. et al. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37–46 (1996).

    CAS  PubMed  Google Scholar 

  10. Patton, E. E. & Zon, L. I. The art and design of genetic screens: zebrafish. Nature Rev. Genet. 2, 956–966 (2001). References 8, 9 and 10 report on different screening approaches in zebrafish.

    CAS  PubMed  Google Scholar 

  11. Williamson, A. & Lehmann, R. Germ cell development in Drosophila. Annu. Rev. Cell Dev. Biol. 12, 365–391 (1996).

    CAS  PubMed  Google Scholar 

  12. McLaren, A. Signaling for germ cells. Genes Dev. 13, 373–376 (1999).

    CAS  PubMed  Google Scholar 

  13. Wylie, C. Germ cells. Cell 96, 165–174 (1999).

    CAS  PubMed  Google Scholar 

  14. Zernicka-Goetz, M. Fertile offspring derived from mammalian eggs lacking either animal or vegetal poles. Development 125, 4803–4808 (1998).

    CAS  PubMed  Google Scholar 

  15. Tam, P. & Zhou, S. The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178, 124–132 (1996). An important paper, in which the regulative mode of PGC specification in mouse is shown.

    CAS  PubMed  Google Scholar 

  16. Ying, Y., Qi, X. & Zhao, G. Q. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc. Natl Acad. Sci. USA 98, 7858–7862 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Lawson, K. A. et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424–436 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Ying, Y. & Zhao, G. Q. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 232, 484–492 (2001).

    CAS  PubMed  Google Scholar 

  19. Niewkoop, P. D. & Sutasurya, L. A. Primordial Germ Cells in the Chordates: Embryogenesis and Phylogenesis (Cambridge Univ. Press, Cambridge, 1979).

    Google Scholar 

  20. Walker, C. & Streisinger, G. Induction of mutations by γ-rays in pregonial germ cells of zebrafish embryos. Genetics 103, 125–136 (1983). An elegant genetic study that produced an estimate for the number of PGCs in zebrafish.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Lin, S., Long, W., Chen, J. & Hopkins, N. Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos. Proc. Natl Acad. Sci. USA 89, 4519–4523 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Yoon, C., Kawakami, K. & Hopkins, N. Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124, 3157–3165 (1997). This paper describes the expression pattern of vasa in zebrafish, which is a molecular marker that allows the germ plasm and PGCs to be recognized from early stages of development.

    CAS  PubMed  Google Scholar 

  23. Olsen, L. C., Aasland, R. & Fjose, A. A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech. Dev. 66, 95–105 (1997).

    CAS  PubMed  Google Scholar 

  24. Hay, B., Jan, L. & Jan, Y. 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).

    CAS  PubMed  Google Scholar 

  25. Lasko, P. & Ashburner, M. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335, 611–617 (1988).

    CAS  PubMed  Google Scholar 

  26. Braat, A., Zandbergen, T., van de Water, S., Goos, H. & Zivkovic, D. Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev. Dyn. 216, 153–167 (1999).

    CAS  PubMed  Google Scholar 

  27. Braat, A. K., van de Water, S., Goos, H., Bogerd, J. & Zivkovic, D. Vasa protein expression and localization in the zebrafish. Mech. Dev. 95, 271–274 (2000).

    CAS  PubMed  Google Scholar 

  28. Knaut, H., Pelegri, F., Bohmann, K., Schwarz, H. & Nusslein-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). This study, based on light and electron microscopy, proved that vasa RNA (but not the vasa protein) resides in the zebrafish germ plasm and that the vasa-labelled germ plasm segregates to the blastomeres that become PGCs.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Knaut, H., Steinbeisser, H., Schwarz, H. & Nusslein-Volhard, C. An evolutionary conserved region in the vasa 3′ UTR targets RNA translation to the germ cells in the zebrafish. Curr. Biol. 12, 454–466 (2002).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  31. Pelegri, F., Knaut, H., Maischein, H., Schulte-Merker, S. & Nusslein-Volhard, C. A mutation in the zebrafish maternal-effect gene nebel affects furrow formation and vasa RNA localization. Curr. Biol. 9, 1431–1440 (1999).

    CAS  PubMed  Google Scholar 

  32. Weidinger, G., Wolke, U., Koprunner, M., Klinger, M. & Raz, E. Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development 126, 5295–5307 (1999). This paper gives a detailed description of PGC migration during the first day of zebrafish development, and the role of somatic tissues in providing the cells with guidance cues.

    CAS  PubMed  Google Scholar 

  33. Bashirullah, A. et al. Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J. 18, 2610–2620 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Seydoux, G. & Fire, A. Soma–germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans. Development 120, 2823–2834 (1994).

    CAS  PubMed  Google Scholar 

  35. Wolke, U., Weidinger, G., Köprunner, M. & Raz, E. Multiple levels of post-transcriptional control lead to germ line specific gene expression in the zebrafish. Curr. Biol. 12, 289–294 (2002).

    CAS  PubMed  Google Scholar 

  36. Köprunner, M., Thisse, C., Thisse, B. & Raz, E. A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev. 15, 2877–2885 (2001).

    PubMed  PubMed Central  Google Scholar 

  37. Kudoh, T. et al. A gene expression screen in zebrafish embryogenesis. Genome Res. 11, 1979–1987 (2001).

    CAS  PubMed  Google Scholar 

  38. Thisse, B. et al. Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission [online] <http://zfin.org/cgibin/webdriver?MIval=aa-xpatselect.apg> (2001).

  39. Müller, K., Thisse, C., Thisse, B. & Raz, E. Expression of a linker histone-like gene in the primordial germ cells in zebrafish. Mech. Dev. 117, 253–257 (2002).

    PubMed  Google Scholar 

  40. Wibrand, K. & Olsen, L. C. Linker histone H1M transcripts mark the developing germ line in zebrafish. Mech. Dev. 117, 249–252 (2002).

    CAS  PubMed  Google Scholar 

  41. Weidinger, G. et al. dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr. Biol. (in the press).

  42. Nasevicius, A. & Ekker, S. C. Effective targeted gene 'knockdown' in zebrafish. Nature Genet. 26, 216–220 (2000).

    CAS  PubMed  Google Scholar 

  43. Kobayashi, S., Yamada, M., Asaoka, M. & Kitamura, T. Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature 380, 708–711 (1996).

    CAS  PubMed  Google Scholar 

  44. Forbes, A. & Lehmann, R. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125, 679–690 (1998).

    CAS  PubMed  Google Scholar 

  45. Deshpande, G., Calhoun, G., Yanowitz, J. L. & Schedl, P. D. Novel functions of nanos in downregulating mitosis and transcription during the development of the Drosophila germline. Cell 99, 271–281 (1999).

    CAS  PubMed  Google Scholar 

  46. Subramaniam, K. & Seydoux, G. nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 126, 4861–4871 (1999).

    CAS  PubMed  Google Scholar 

  47. Ciruna, B. et al. Production of maternal-zygotic mutant zebrafish by germ-line replacement. Proc. Natl Acad. Sci. USA 99, 14919–14924 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Gritsman, K. et al. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 97, 121–132 (1999).

    CAS  PubMed  Google Scholar 

  49. Beams, H. W. & Kessel, R. G. The problem of germ cell determinants. Int. Rev. Cytol. 39, 413–479 (1974).

    CAS  PubMed  Google Scholar 

  50. Eddy, E. Fine structural observations on the form and distribution of nuage in germ cells of the rat. Anat. Rec. 178, 731–758 (1974).

    CAS  PubMed  Google Scholar 

  51. Eberhart, C. G., Maines, J. Z. & Wasserman, S. A. Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature 381, 783–785 (1996).

    CAS  PubMed  Google Scholar 

  52. Tanaka, S. et al. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14, 841–853 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Heasman, J. & Wylie, C. C. Contact relations and guidance of primordial germ cells on their migratory route in embryos of Xenopus laevis. Proc. R. Soc. Lond. B 213, 41–58 (1981).

    CAS  PubMed  Google Scholar 

  54. Godin, I., Wylie, C. & Heasman, J. Genital ridges exert long-range effects on mouse primordial germ cell numbers and direction of migration in culture. Development 108, 357–363 (1990).

    CAS  PubMed  Google Scholar 

  55. Moore, L. A., Broihier, H. T., Van Doren, M., Lunsford, L. B. & Lehmann, R. Identification of genes controlling germ cell migration and embryonic gonad formation in Drosophila. Development 125, 667–678 (1998). This paper presents the results of a large-scale screen in which genes and tissue that are important for specific steps of PGC migration in Drosophila are described.

    CAS  PubMed  Google Scholar 

  56. Van Doren, M., Broihier, H. T., Moore, L. A. & Lehmann, R. HMG-CoA reductase guides migrating primordial germ cells. Nature 396, 466–469 (1998).

    CAS  PubMed  Google Scholar 

  57. Kuwana, T. & Rogulska, T. Migratory mechanisms of chick primordial germ cells toward gonadal anlage. Cell Mol. Biol. 45, 725–736 (1999).

    CAS  PubMed  Google Scholar 

  58. Starz-Gaiano, M., Cho, N. K., Forbes, A. & Lehmann, R. Spatially restricted activity of a Drosophila lipid phosphatase guides migrating germ cells. Development 128, 983–991 (2001).

    CAS  PubMed  Google Scholar 

  59. Weidinger, G. et al. Regulation of zebrafish primordial germ cell migration by attraction towards an intermediate target. Development 129, 25–36 (2002).

    CAS  PubMed  Google Scholar 

  60. Griffin, K. J., Amacher, S. L., Kimmel, C. B. & Kimelman, D. Molecular identification of spadetail: regulation of zebrafish trunk and tail mesoderm formation by T-box genes. Development 125, 3379–3388 (1998).

    CAS  PubMed  Google Scholar 

  61. Talbot, W. S. et al. A homeobox gene essential for zebrafish notochord development. Nature 378, 150–157 (1995).

    CAS  PubMed  Google Scholar 

  62. Zhang, N., Zhang, J., Purcell, K. J., Cheng, Y. & Howard, K. The Drosophila protein Wunen repels migrating germ cells. Nature 385, 64–67 (1997).

    CAS  PubMed  Google Scholar 

  63. Stein, J. A., Broihier, H. T., Moore, L. A. & Lehmann, R. Slow as molasses is required for polarized membrane growth and germ cell migration in Drosophila. Development 129, 3925–3934 (2002).

    CAS  PubMed  Google Scholar 

  64. Doitsidou, M. et al. Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111, 647–659 (2002).

    CAS  PubMed  Google Scholar 

  65. Knaut, H., Werz, C., Geisler, R. & Nusslein-Volhard, C. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421, 279–282 (2003). References 64 and 65 describe the identification of Cxcr4b as a PGC guidance molecule that responds to directional cues from the chemokines Sdf1a and Sdf1b, respectively.

    CAS  PubMed  Google Scholar 

  66. Chong, S., Emelyanov, A., Gong, Z. & Korzh, V. Expression pattern of two zebrafish genes, cxcr4a and cxcr4b. Mech. Dev. 109, 347–354 (2001).

    CAS  PubMed  Google Scholar 

  67. Amores, A. et al. Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711–1714 (1998).

    CAS  PubMed  Google Scholar 

  68. Postlethwait, J. H. et al. Vertebrate genome evolution and the zebrafish gene map. Nature Genet. 18, 345–349 (1998).

    CAS  PubMed  Google Scholar 

  69. Peled, A. et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283, 845–848 (1999).

    CAS  PubMed  Google Scholar 

  70. Petit, I. et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nature Immunol. 3, 687–694 (2002).

    CAS  Google Scholar 

  71. Aiuti, A., Webb, I., Bleul, C., Springer, T. & Gutierrez-Ramos, J. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J. Exp. Med. 185, 111–120 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Bleul, C., Fuhlbrigge, R., Casasnovas, J., Aiuti, A. & Springer, T. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J. Exp. Med. 184, 1101–1109 (1996).

    CAS  PubMed  Google Scholar 

  73. Zou, Y. R., Kottmann, A. H., Kuroda, M., Taniuchi, I. & Littman, D. R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595–599 (1998).

    CAS  PubMed  Google Scholar 

  74. Xiang, Y. et al. Nerve growth cone guidance mediated by G protein coupled receptors. Nature Neurosci. 5, 843–848 (2002).

    CAS  PubMed  Google Scholar 

  75. Muller, A. et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 410, 50–56 (2001).

    CAS  PubMed  Google Scholar 

  76. David, N. B. et al. Molecular basis of cell migration in the fish lateral line: role of the chemokine receptor CXCR4 and of its ligand, SDF1. Proc. Natl Acad. Sci. USA 99, 16297–16302 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Starz-Gaiano, M. Molecular Guidance Cues and Intracellular Signaling in Drosophila Germ Cell Migration. Thesis, New York Univ. (2002).

    Google Scholar 

  78. Ara, T. et al. Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc. Natl Acad. Sci. USA 100, 5319–5323 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Molyneaux, K. et al. The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development (in the press). Together with reference 78, these papers show a role for Sdf-1/Cxcl12 in PGC migration towards the gonad. As well as this role, which is similar to that described for the zebrafish Sdf1, the mouse Sdf-1 is also essential for PGC survival.

  80. Braat, A. K., van de Water, S., Korving, J. & Zivkovic, D. A zebrafish vasa morphant abolishes vasa protein but does not affect the establishment of the germline. Genesis 30, 183–185 (2001).

    CAS  PubMed  Google Scholar 

  81. Styhler, S., Nakamura, A., Swan, A., Suter, B. & Lasko, P. vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125, 1569–1578 (1998).

    CAS  PubMed  Google Scholar 

  82. Tomancak, P., Guichet, A., Zavorszky, P. & Ephrussi, A. Oocyte polarity depends on regulation of gurken by Vasa. Development 125, 1723–1732 (1998).

    CAS  PubMed  Google Scholar 

  83. Kuznicki, K. et al. Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C. elegans. Development 127, 2907–2916 (2000).

    CAS  PubMed  Google Scholar 

  84. Gruidl, M. et al. Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 93, 13837–13842 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Komiya, T., Itoh, K., Ikenishi, K. & Furusawa, M. Isolation and characterization of a novel gene of the DEAD box protein family which is specifically expressed in germ cells of Xenopus laevis. Dev. Biol. 162, 354–363 (1994).

    CAS  PubMed  Google Scholar 

  86. Ikenishi, K., Tanaka, T. & Komiya, T. Spatio-temporal distribution of the protein of the Xenopus vasa homologue (Xenopus vasa-like gene 1, XVLG1) in embryos. Dev. Growth Differ. 38, 527–535 (1996).

    CAS  Google Scholar 

  87. Ikenishi, K. & Tanaka, T. Involvement of the protein of Xenopus vasa homolog (Xenopus vasa-like gene 1, XVLG1) in the differentiation of primordial germ cells. Dev. Growth Differ. 39, 625–633 (1997).

    CAS  PubMed  Google Scholar 

  88. Ikenishi, K. & Tanaka, T. Spatio-temporal expression of Xenopus vasa homolog, XVLG1, in oocytes and embryos: the presence of XVLG1 RNA in somatic cells as well as germline cells. Dev. Growth Differ. 42, 95–103 (2000).

    CAS  PubMed  Google Scholar 

  89. Fujiwara, Y. et al. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc. Natl Acad. Sci. USA 91, 12258–12262 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Tanaka, S. S. et al. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14, 841–853 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Noce, T., Okamoto-Ito, S. & Tsunekawa, N. Vasa homolog genes in mammalian germ cell development. Cell Struct. Funct. 26, 131–136 (2001).

    CAS  PubMed  Google Scholar 

  92. Zeeman, A. M. et al. VASA is a specific marker for both normal and malignant human germ cells. Lab. Invest. 82, 159–166 (2002).

    CAS  PubMed  Google Scholar 

  93. Castrillon, D. H., Quade, B. J., Wang, T. Y., Quigley, C. & Crum, C. P. The human VASA gene is specifically expressed in the germ cell lineage. Proc. Natl Acad. Sci. USA 97, 9585–9590 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Wang, C. & Lehmann, R. Nanos is the localized posterior determinant in Drosophila. Cell 66, 637–647 (1991).

    CAS  PubMed  Google Scholar 

  95. Gavis, E. R. & Lehmann, R. Translational regulation of nanos by RNA localization. Nature 369, 315–318 (1994).

    CAS  PubMed  Google Scholar 

  96. Mosquera, L., Forristall, C., Zhou, Y. & King, M. L. A mRNA localized to the vegetal cortex of Xenopus oocytes encodes a protein with a nanos-like zinc finger domain. Development 117, 377–386 (1993).

    CAS  PubMed  Google Scholar 

  97. Jaruzelska, J. et al. Conservation of a Pumilio–Nanos complex from Drosophila germ plasm to human germ cells. Dev. Genes Evol. 213, 120–126 (2003).

    CAS  PubMed  Google Scholar 

  98. Maegawa, S., Yasuda, K. & Inoue, K. Maternal mRNA localization of zebrafish DAZ-like gene. Mech. Dev. 81, 223–226 (1999).

    CAS  PubMed  Google Scholar 

  99. Xu, E. Y., Moore, F. L. & Pera, R. A. A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in metazoans. Proc. Natl Acad. Sci. USA 98, 7414–7419 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Cheng, M. H., Maines, J. Z. & Wasserman, S. A. Biphasic subcellular localization of the DAZL-related protein boule in Drosophila spermatogenesis. Dev. Biol. 204, 567–576 (1998).

    CAS  PubMed  Google Scholar 

  101. Maines, J. Z. & Wasserman, S. A. Post-transcriptional regulation of the meiotic Cdc25 protein Twine by the Dazl orthologue Boule. Nature Cell Biol. 1, 171–174 (1999).

    CAS  PubMed  Google Scholar 

  102. Karashima, T., Sugimoto, A. & Yamamoto, M. Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127, 1069–1079 (2000).

    CAS  PubMed  Google Scholar 

  103. Houston, D. W. & King, M. L. A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127, 447–456 (2000).

    CAS  PubMed  Google Scholar 

  104. Houston, D. W., Zhang, J., Maines, J. Z., Wasserman, S. A. & King, M. L. A Xenopus DAZ-like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. Development 125, 171–180 (1998).

    CAS  PubMed  Google Scholar 

  105. Mita, K. & Yamashita, M. Expression of Xenopus Daz-like protein during gametogenesis and embryogenesis. Mech. Dev. 94, 251–255 (2000).

    CAS  PubMed  Google Scholar 

  106. Ruggiu, M. et al. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389, 73–77 (1997).

    CAS  PubMed  Google Scholar 

  107. Reijo, R. et al. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nature Genet. 10, 383–393 (1995).

    CAS  PubMed  Google Scholar 

  108. Moepps, B. et al. Characterization of a Xenopus laevis CXC chemokine receptor 4: implications for hematopoietic cell development in the vertebrate embryo. Eur. J. Immunol. 30, 2924–2934 (2000).

    CAS  PubMed  Google Scholar 

  109. Braun, M. et al. Xenopus laevis stromal cell-derived factor 1: conservation of structure and function during vertebrate development. J. Immunol. 168, 2340–2347 (2002).

    CAS  PubMed  Google Scholar 

  110. Tan, C. H. et al. Ziwi, the zebrafish homologue of the Drosophila piwi: co-localization with vasa at the embryonic genital ridge and gonad-specific expression in the adults. Gene Expr. Patterns 2, 257–260 (2002).

    CAS  PubMed  Google Scholar 

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Acknowledgements

I thank Michal Reichman-Fried for her critical reading of the manuscript and members of the Raz laboratory for their helpful discussions. E.R. is funded by the Deutsche Forschungsgemeinschaft and Volkswagen-Stiftung.

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Authors and Affiliations

  1. Germ Cell Development, Max-Planck-Institute for Biophysical Chemistry, Am Fassberg 11, Goettingen, 37070, Germany

    Erez Raz

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  1. Erez Raz
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DATABASES

FlyBase

Hmgcr

slam

wun

wun 2

LocusLink

Cxcl12

Cxcr4

SwissProt

Cxcr4b

GFP

Sdf1a

ZFIN

albino

cxcl12a

cxcl12b

cxcr4a

cxcr4b

floating head

golden

knypek

nanos-1

nebel

no tail

spadetail

vasa

FURTHER INFORMATION

Erez Raz's laboratory

Glossary

PRIMORDIAL GERM CELLS

Germline cells at all stages of development from the time when this lineage is formed until they arrive at the gonad and start differentiating into gametes.

OOGONIA STAGE

A stage in oogenesis that occurs after the primordial germ cells colonize the gonad and before they undergo meiosis.

SPERMATOGONIA STAGE

A stage in spermatogenesis that occurs after the primordial germ cells colonize the gonad and before they undergo meiosis.

URODELE

An order of amphibians that includes the newts and salamanders, which have elongated bodies, short limbs and a tail.

GASTRULATION

A process of cell and tissue movements whereby the cells of the blastula are rearranged to form a three-layered body plan, which consists of the outer ectoderm, inner ectoderm and interstitial mesoderm.

DEAD BOX

A highly conserved motif in a family of putative RNA helicases, which is named after the single-letter code for the amino-acid sequence involved (Asp-Glu-Ala-Asp).

CENTRIOLES

A pair of cylinder-like structures that are embedded in the centrosome (the microtubule-organizing centre in most animal cells). They replicate during interphase. As mitosis begins, the centrioles migrate to the two poles, where they organize microtubules for proper chromosome alignment and separation.

MODIFIED ANTISENSE OLIGONUCLEOTIDES

(morpholinos). Oligomers that normally consist of 25 morpholino subunits, each of which contains one of the four genetic bases linked to a morpholine ring. The oligomers can bind and inactivate selected RNA sequences on the basis of base pairing and steric interference.

PARAXIAL MESODERM

A region of the mesoderm that gives rise to somites, blocks of mesodermal cells on both sides of the neural tube.

NOTOCHORD

A rod of dorsal-most mesoderm that separates the embryo into right and left halves.

GLYPICANS

A family of cell-surface heparan sulphate proteoglycans. Each glypican is composed of a membrane-associated protein core and a variable number of heparan sulphate chains.

HMG-COA REDUCTASE

(NADP). An important regulatory enzyme in pathways for the synthesis of cholesterol and other sterols.

PENETRANCE

The proportion of individuals with a specific genotype who manifest the genotype at the phenotypic level.

SLICE CULTURE

A slice of live tissue (200μm thick) in which microscopic analysis of primordial-germ-cell migration can be carried out under organ culture conditions.

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Raz, E. Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet 4, 690–700 (2003). https://doi.org/10.1038/nrg1154

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