Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification

Journal of Cell Biology

Volumn 149, Issue 4, 2000, Pages 875-888

  Knaut, Holger ^a   Pelegri, Francisco ^a,c   Bohmann, Kerstin ^a   Schwarz, Heinz ^b   Nüsslein Volhard, Christiane ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b Elektronenmikroskopie Labor   (Germany)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Asymmetric segregation; Danio rerio; Nebel; Primordial germ cells; RNA localization

Indexed keywords

GENE PRODUCT; MESSENGER RNA;

ACTIN POLYMERIZATION; ARTICLE; BLASTULA; DNA REPLICATION; GENE EXPRESSION; GENE LOCATION; GENE LOSS; GENE SEGREGATION; GENE TRANSLOCATION; GERM CELL; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION INITIATION; ZEBRA FISH;

ACTINS; ANIMALS; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL DIFFERENTIATION; CELL NUCLEUS; CELL POLARITY; DEAD-BOX RNA HELICASES; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GENE SILENCING; GERM CELLS; MICROTUBULES; OOGENESIS; ORGANELLES; RNA HELICASES; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS; ZYGOTE;

DANIO; DANIO RERIO; VERTEBRATA;

EID: 0034657873     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.4.875     Document Type: Article

References (83)

1. Andre, J., and C. Rouiller 1957. Electron Microscopy. Proc. Stockholm Conf., 1956, 162-164.
2. Asaoka, M., H. Sano, Y. Obara, and S. Kobayashi. 1998. Maternal Nanos regulates zygotic gene expression in germline progenitors of Drosophila melanogaster. Mech. Dev. 78: 53-158.
3. Bobola, N., R.P. Jansen, T.H. Shin, and K. Nasmyth. 1996. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell. 84:699-709.
4. Braat, A.K., T. Zandbergen, S. Van de Water, H.J.T. Goos, and D. Zivkovic. 1999. Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev. Dynamics. 216:153-167.
5. Bregman, D.B., L. Du, S. van der Zee, and S.L. Warren. 1995. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129:287-298.
6. Dahm, R., C. Gribbon, R.A. Quinlan, and A.R. Prescott. 1998. Changes in the nucleolar and coiled body compartments precede lamina and chromatin reorganization during fibre cell denucleation in the bovine lens. Eur. J. Cell Biol. 75:237-246.
7. Eddy, E. 1975. Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43:229-280.
8. Ephrussi, A., and R. Lehmann. 1992. Induction of germ cell formation by oskar. Nature. 358:387-392.
9. Ephrussi, A., L.K. Dickinson, and R. Lehmann. 1991. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell. 66: 37-50.
10. Erdelyi, M., A.M. Michon, A. Guichet, J.B. Glotzer, and A. Ephrussi. 1995. Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization. Nature. 377:524-527.
11. Fujiwara, Y., T. Komiya, H. Kawabata, M Sato, H. Fujimoto, M. Furusawa, and T. Noce. 1994. 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.
12. Gevers, P., J. Dulos, H. Schipper, and L.P. Timmermans. 1992. Origin of primordial germ cells, as characterized by the presence of nuage, in embryos of the teleost fish Barbus conchonius. Eur. J. Morphol. 30:195-204.
13. Gruidl, M.E., P.A. Smith, K.A. Kuznicki, J.S. McCrone, J. Kirchner, D.L. Roussell, S. Strome, and K.L. Bennett. 1996. 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.
14. Haffter, P., M. Granato, M. Brand, M.C. Mullins, M. Hammerschmidt, D.A. Kane, J. Odenthal, F.J. van Eeden, Y.I. Jiang, C.P. Heisenberg, et al. 1996. The identification of genes with unique and essential functions in the development of the zebrafish. Danio rerio. Development. 123:1-36.
15. Hamaguchi, S. 1982. A light- and electron-microscopic study on the migration of primordial germ cells in the teleost. Oryzias latipes. Cell. Tissue Res. 227: 139-151.
16. Hay, B., L. Ackerman, S. Barbel, L.Y. Jan, and Y.N. Jan. 1988a. Identification of a component of Drosophila polar granules. Development. 103:625-640.
17. Hay, B., L. Y. Jan, and Y.N. Jan. 1988b. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell. 55:577-587.
18. Hirata, J., H. Nakagoshi, Y. Nabeshima, and F. Matsuzaki. 1995. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature. 377:627-630.
19. Hopman, A.H., F.C. Ramaekers, and E.J. Speel. 1998. Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for in situ hybridization using CARD amplification. J. Histochem. Cytochem. 46:771-777.
20. Horvitz, H.R., and I. Herskowitz. 1992. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell. 68:237-255.
21. Ikenishi, K., T.S. Tanaka, and T. Komiya. 1996. Spatio-temporal distribution of the protein of Xenopus vasa homologue (Xenopus vasa-like gene 1, XVLG I) in embryos. Dev. Growth Differ. 38:527-535.
22. Illmensee, K., and A.P. Mahowald. 1974. Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc. Natl. Acad. Sci. USA. 71:1016-11120.
23. Jan, Y.N., and L.Y. Jan. 1998. Asymmetric cell division. Nature. 392:775-778.
24. Jan, Y.N., and L.Y. Jan. 1999. Asymmetry across species. Nat. Cell Biol. 1:E42-44.
25. Kane, D.A., and C.B. Kimmel. 1993. The zebrafish midblastula transition. Development. 119:447-456.
26. Kim, E., L. Du, D.B. Bregman, and S.L. Warren. 1997. Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J. Cell Biol. 136:19-28.
27. Kimmel, C.B., W.W. Ballard, S.R. Kimmel, B. Ullmann, and T.F. Schilling. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:253-310.
28. Knoblich, J.A. 1997. Mechanisms of asymmetric cell division during animal development. Curr. Opin. Cell Biol. 9:833-841.
29. Knoblich, J.A., L.Y. Jan, and Y.N. Jan. 1995. Asymmetric segregation of Numb and Prospero during cell division. Nature. 377:624-627.
30. Komiya, T., and Y. Tanigawa. 1995. Cloning of a gene of the DEAD box protein family which is specifically expressed in germ cells in rats. Biochem. Biophys. Res. Commun. 207:405-410.
31. Komiya, T., K. Itoh, K. Ikenishi, and M. Furusawa. 1994. 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.
32. Lantz, V.A., S.E. Clemens, and K.G. Miller. 1999. The actin cytoskeleton is required lor maintenance of posterior pole plasm components in the Drosophila embryo. Mech. Dev. 85:111-122.
33. Lasko, P.F., and M. Ashburner. 1988. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature. 335:611-617.
34. Lasko, P.F., and M. Ashhurner. 1990. Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes. Dev. 4:905-921.
35. Lehmann, R., and C. Nüsslein-Volhard. 1991. The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development. 112:679-691.
36. Long, R.M., R.H. Singer, X. Meng, I. Gonzalez, K. Nasmyth, and R.P. Jansen. 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA Science. 277:383-387.
37. Mahowald, A.P. 1962. Fine structure of pole cells and polar granules in Drosophila melanogaster. J. Exp. Zool. 228:91-97.
38. Mahowald, A.P. 1968. Polar granules of Drosophila. II. Ultrastructural changes during early embryogenesis. J. Exp. Zool. 167:237-261.
39. Mahowald, A.P. 1971. Polar granules of Drosophila. 3. The continuity of polar granules during the life cycle of Drosophila. J. Exp. Zool. 176:329-343.
40. Mullins, M.C., M. Hammerschmidt, P. Haffter, and C. Nüsslein-Volhard. 1994. Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr. Biol. 4:189-202.
41. Nagano, H., S. Hirai, K. Okano, and S. Ikegami. 1981. Achromosomal cleavage of ferlilized starfish eggs in the presence of aphidicolin. Dev. Biol. 85:409-415.
42. Newport, J., and M. Kirschner. 1982. A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage. Cell. 30:675-686.
43. Nieuwkoop, P.D., and L.A. Sutasurya. 1979. Primordial Germ Cells in the Chordates. Cambridge University Press, Cambridge, London/New York/ Melbourne. 81-127.
44. Ober, E.A., and S. Schulte-Merker. 1999. Signals from the yolk cell induce mesoderm, neuroectoderm, the trunk organizer, and the notochord in zebrafish. Dev. Biol. 215:167-181.
45. Okada, M., I.A. Kleinman, and H.A. Schneiderman. 1974. Restoration of fertility in sterilized Drosophila eggs by transplantation of polar cytoplasm. Dev. Biol. 37:43-54.
46. Olsen, L.C., R. Aasland, and A. Fjose. 1997. A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech. Dev. 66:95-105.
47. Patturajan, M., R.J. Schulte, B.M. Sefton. R. Berezney, M. Vincent. O. Bensaude, S.L. Warren, and J.L. Corden. 1998. Growth related changes in phosphorylation of yeast RNA polymerase II. J. Biol. Chem. 273:4689-4694.
48. Pelegri, F., and S. Schulte-Merker. 1999. A gynogenesis-based screen for maternal-effect genes in the zebrafish, Danio rerio. In The Zebrafish: Genetics and Genomics. W. Detrich, L.I. Zon and M. Westerfield, editors. Academic Press Inc., New York. 1-20.
49. Pelegri, F., H. Knaut, H.M. Maischein, S. Schulte-Merker, and C. Nüsslein-Volhard. 1999. A mutation in the zebrafish maternal-effect gene nebel affects furrow formation and vasa RNA localization. Curr. Biol. 9:1431-1440.
50. Pitt, J.N., J.A. Schisa, and J.R. Priess. 2000. P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA. Dev. Biol. 219:315-333.
51. Pokrywka, N.J., and E.C. Stephenson. 1995. Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol. 167: 363-370.
52. Pugh, G.E. P.J. Coates, E.B. Lane, Y. Raymond, and R.A. Quinlan. 1997. Distinct nuclear assembly pathways for lamins A and C lead to their increase during quiescence in Swiss 3T3 cells. J. Cell. Sci. 110:2483-2493.
53. Raff, J.W., and D.M. Glover. 1989. Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell. 57:611-619.
54. Rappaport, R. 1996. Cytokinesis in Animal Cells. Cambridge University Press, Cambridge. 51-95.
55. Ressom, R.E., and K.E. Dixon. 1988 Relocation and reorganization of germ plasm in Xenopus embryos after fertilization. Development. 103:507-518.
56. Rhyu, M.S., and J.A. Knoblich. 1995. Spindle orientation and asymmetric cell fate. Cell. 82:523-526.
57. Rhyu, M.S., L.Y. Jan, and Y.N. Jan. 1994. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell. 76:477-191.
58. Robb, D.L., J. Heasman, J. Raats, and C. Wylic. 1996. A kinesin-like protein is required for germ plasm aggregation in Xenopus. Cell. 87:823-831.
59. Rongo, C., H.T. Broihier, L. Moore, M. Van Doren, A. Forbes, and R. Lehmann. 1997. Germ plasm assembly and germ cell migration in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 62:1-11.
60. Schober, M., M. Schaefer, and J.A. Knoblich. 1999. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature. 402:548-551.
61. Schüpbach, T., and E. Wieschaus. 1986. Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Roux's Arch. Dev. Biol. 195:302-317.
62. Selman, S., R. A. Wallace, A. Sarka, and X. Oi. 1993. Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morphology. 218:203-224.
63. Seydoux, G., and M.A. Dunn. 1997. Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development. 124: 2191-2201.
64. Seydoux, G., and S. Strome. 1999. Launching the germline in Caenorhabditis elegans: regulation of gene expression in early germ cells. Development. 126: 3275-3283.
65. Shen, C.P., J.A. Knoblich, Y.M. Chan, M.M. Jiang, L.Y. Jan, and Y.N. Jan. 1998. Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila. Genes. Dev. 12:1837-1846.
66. Sil, A., and I. Herskowitz. 1996. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell. 84:711-722.
67. Spana, E.P., and C.Q. Doc. 1995. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development. 121:3187-3195.
68. Spana, E.P., C. Kopezynski, C.S. Goodman, and C.Q. Doc. 1995. Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development. 121:3489-3494.
69. Spector, I., N.R. Shochet, Y. Kashman, and A. Groweiss. 1983. Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science: 219:493-495.
70. Styhler, S., A. Nakamura, A. Swan, B. Suter, and P. Lasko. 1998. Vasa is required fur GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development. 125:1569-1578.
71. Takizawa, P.A., A. Sil, J.R. Swedlow, I. Herskowitz, and R.D. Vale. 1997. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast, Nature. 389:90-93.
72. Tanaka, S.S., Y. Toyooka, R. Akasa, Y. Katoh-Fukui, Y. Nakahara, R. Suzuki, M. Yokoyama, and T. Noce. 2000. The mouse homolog of Drosophila vasa is required for the development of male germ cells. Genes Dev. 14:841-853.
73. Tomancak, P., A. Guichet, P. Zavorszky, and A. Ephrussi. 1998. Oocyte polarity depends on regulation of gurken by Vasa. Development. 125:1723-1732.
74. Van Doren, M., A.L. Williamson, and R. Lehmann. 1998. Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol. 8:243-246.
75. Wallace, R.A., and K. Selman. 1990. Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J. Electron Microsc. Tech. 16:175-201.
76. Warren, S.L., A.S. Landolfi, C. Curtis, and J.S. Morrow. 1992. Cytostellin: a novel, highly conserved protein that undergoes continuous redistribution during the cell cycle. J. Cell. Sci. 103:381-388.
77. Weidinger, G., U. Wolke, M. Koprunner, M. Klinger, and E. Raz. 1999. Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development. 126:5295-5307.
78. Whitington, P.M., and K.E. Dixon. 1975. Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis. J. Embryol. Exp. Morphol. 33:57-74.
79. Wodarz, A., A. Ramrath, U. Kuchinke, and E. Knust. 1999. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature. 402:544-547.
80. Wolf, N., J. Priess, and D. Hirsh. 1983. Segregation of germline granules in early embryos of Caenorhabditis elegans: an electron microscopic analysis. J. Embryol. Exp. Morphol. 73:297-306.
81. Wylie, C. 1999. Germ cells. Cell. 96:165-174.
82. Yoon, C., K. Kawakami, and N. Hopkins. 1997. 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.
83. Zalokar, M. 1976. Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev. Biol. 49:425-437.