Development Genes and Evolution

, Volume 214, Issue 12, pp 615–627 | Cite as

Spatio-temporal expression of a DAZ-like gene in the Japanese newt Cynops pyrrhogaster that has no germ plasm

  • Yoichiro Tamori
  • Toshiharu Iwai
  • Koichi Mita
  • Masami Wakahara
Original Article

Abstract

To investigate the germ cell specification in urodeles, we cloned a DAZ-like sequence from the Japanese newt Cynops pyrrhogaster, Cydazl, and raised antibodies specific to Cydazl. Cydazl is a homologue of the human DAZ (deleted in azoospermia), DAZL, and Xenopus dazl genes, which are involved in gametogenesis or germ cell specification. During gametogenesis, expression of Cydazl mRNA and Cydazl protein was detected at first in the small previtellogenic oocytes in females but was not localized as seen in Xenopus and was restricted to secondary spermatogonia prior to meiosis in males. During early embryogenesis, maternal stores of the Cydazl transcript and protein were present in the entire embryos, not localized in any specific region. The zygotic expression was detected in hatching larvae (stage 50) by RT-PCR analysis whereas specific cells expressing Cydazl could not be determined by in situ hybridization at this stage. Strong expression of Cydazl and Cydazl were detected in primordial germ cells (PGCs) that had entered the gonadal rudiment at late stage 59. These results suggest that Cydazl does not function early in development, for the specification of germ cells, but functions later for differentiation of germ cells in the developing gonads during embryogenesis and for meiotic regulation, supporting the previous idea of an intermediate germ cell formation mode in urodeles.

Keywords

DAZ-like Primordial germ cells Gametogenesis Urodele 

Notes

Acknowledgements

This work partly was supported by the Sasakawa Scientific Research Grant from The Japan Science Society.

References

  1. Akita Y, Wakahara M (1985) Cytological analyses of factors which determine the number of primordial germ cells (PGCs) in Xenopus laevis. J Embryol Exp Morphol 90:251–265PubMedGoogle Scholar
  2. Ariizumi T, Moriya N, Uchiyama H, Asashima M (1991a) Concentration-dependent inducing activity of activin A. Roux’s Arch Dev Biol 200:230–233Google Scholar
  3. Ariizumi T, Sawanuma K, Uchiyama H, Asashima M (1991b) Dose and time dependent mesoderm induction and out-growth formation by activin A in Xenopus laevis. Int J Dev Biol 35:407–411PubMedGoogle Scholar
  4. Beetschen JC, Gautier J (1989) Oogenesis. In: Armstrong JB, Malacinski GM (eds) Developmental biology of the axolotl. Oxford University Press, New York, pp 25–35Google Scholar
  5. Cooke HJ, Lee M, Kerr S, Fuggiu M (1996) A murine homologue of the human DAZ gene is autosomal and expressed only in male and female gonads. Hum Mol Genet 5:513–526CrossRefPubMedGoogle Scholar
  6. Czolovska R (1969) Observations on the origin of the ‘germinal cytoplasm’ in Xenopus laevis. J Embryol Exp Morphol 22:229–251PubMedGoogle Scholar
  7. Dixon KE (1994) Evolutionary aspects of primordial germ cell formation. In: Germline development. Ciba Foundation symposium 182. Wylie, Chichester, pp 92–120Google Scholar
  8. Dumont JN (1972) Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol 136:153–179PubMedGoogle Scholar
  9. Eberhart CG, Maines JZ, Wasserman SA (1996) Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature 381:783–785CrossRefPubMedGoogle Scholar
  10. Eddy EM, Hahnal AC (1983) Establishment of the germ cell line in mammals. In: McLaren A, Wylie CC (eds) Current problems in germ cell differentiation. Cambridge University Press, London, pp 41–69Google Scholar
  11. Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884CrossRefPubMedGoogle Scholar
  12. Guan KL, Dixon JE (1991) Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal Biochem 192:262–267PubMedGoogle Scholar
  13. Hall BK (1999) Evolutionary developmental biology, 2nd edn. Kluwer, DordrechtGoogle Scholar
  14. Hamashima N, Kotani M (1977) Ultrastructural observations on the primordial germ cells in the newt, Triturus pyrrhogaster. Zool Mag 86:239–245PubMedGoogle Scholar
  15. Heasmann J, Quarmby J, Wylie CC (1984) The mitochondrial cloud of Xenopus oocytes: the source of germinal granule material. Dev Biol 105:458–469PubMedGoogle Scholar
  16. Hirai T, Yamashita M, Yoshikuni M, Lou YH, Nagahama Y (1992) Cyclin B in fish oocytes: Its cDNA and amino acid sequences, appearance during maturation, and induction of p34cdc2 activation. Mol Reprod Dev 33:131–140PubMedGoogle Scholar
  17. Houston DW, King ML (2000) A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127:447–456PubMedGoogle Scholar
  18. Houston DW, Zhang J, Maines JZ, Wasserman SA, King ML (1998) A Xenopus DAZ-like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. Development 125:171–180PubMedGoogle Scholar
  19. Ikenishi K (1998) Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev Growth Differ 40:1–10CrossRefPubMedGoogle Scholar
  20. Ikenishi K, Kotani M (1975) Ultrastructure of the ‘germinal plasm’ in Xenopus embryos after cleavage. Dev Growth Differ 17:101–110Google Scholar
  21. Ikenishi K, Nieuwkoop PD (1978) Location and ultrastructure of primordial germ cells (PGCs) in Ambystoma mexicanum. Dev Growth Differ 20:1–9Google Scholar
  22. Ikenishi K, Nakazato S, Okuda T (1986) Direct evidence for the presence of germ cell determinant in vegetal pole cytoplasm of Xenopus laevis and in a subcellular fraction of it. Dev Growth Differ 28:563–568Google Scholar
  23. Johnson AD, Bachvarova RF, Drum M, Masi T (2001) Expression of axolotl Dazl RNA, a marker of germ plasm: widespread maternal RNA and onset of expression in germ cells approaching to the gonad. Dev Biol 234:402–415CrossRefPubMedGoogle Scholar
  24. Johnson AD, Drum M, Bachvarova RF, Masi T, White ME, Crother BI (2003) Evolution of predetermined germ cells in vertebrate embryos: implications for macroevolution. Evol Dev 5:414–431CrossRefPubMedGoogle Scholar
  25. Kamimura M, Ikenishi K, Kotani M, Matsuno T (1976) Observation and proliferation of gonocytes in Xenopus laevis. J Embryol Exp Morphol 36:197–207PubMedGoogle Scholar
  26. Karashima T, Sugimoto A, Yamamoto M (2000) Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127:1069–79PubMedGoogle Scholar
  27. King ML (2003) Germ cells and germ plasm. In: Hall BK, Olson WM (eds) Keywords and concepts in evolutionary developmental biology. Harvard University Press, Cambridge, Mass., pp 155–161Google Scholar
  28. Kocher-Becker U, Tiedemann H (1971) Induction of mesodermal and endodermal structures and primordial germ cells in Triturus ectoderm by vegetalizing factor from chick embryos. Nature 233:65–66PubMedGoogle Scholar
  29. Kotani M (1957) On the formation of primordial germ cells from the presumptive ectoderm of Triturus gastrulae. J Inst Polytech Osaka City Univ Ser D 8:145–159Google Scholar
  30. Kotani M (1958) The formation of germ cells after extirpation of the presumptive lateral plate of Triturus gastrulae. J Inst Polytech Osaka City Univ Ser D 9:195–209Google Scholar
  31. Lawson KA, Hage WJ (1994) Clonal analysis of the origin of primordial germ cells in the mouse. In: Germline development. Ciba Foundation symposium 182. Wylie, Chichester, pp 68–91Google Scholar
  32. Lehmann R, Ephrussi A (1994) Germ plasm formation and germ cell determination in Drosophila. In: Germline development. Ciba Foundation symposium 182. Wylie, Chichester, pp 282–300Google Scholar
  33. Lesimple M, Dournon C, Houillon C (1990) Melanin as a natural germ cell marker for intraspecific transplantation experiments in Ambystoma mexicanum (Urodela, Amphibia). Roux’s Arch Dev Biol 198:420–429Google Scholar
  34. Maegawa S, Yasuda K, Inoue K (1999) Maternal mRNA localization of zebrafish DAZ-like gene. Mech Dev 81:223–226CrossRefPubMedGoogle Scholar
  35. Mahowald AP (1968) Polar granules of Drosophila. II. Ultrastructural changes during early embryogenesis. J Exp Zool 167:237–262PubMedGoogle Scholar
  36. Mahowald AP, Boswell RE (1983) Germ plasm and germ cell development in invertebrates. In: McLaren A, Wylie CC (eds) Current problems in germ cell differentiation. Cambridge University Press, London, pp 3–17Google Scholar
  37. Michael P (1984) Are the primordial germ cell (PGCs) in urodela formed by the inductive action of the vegetative yolk mass? Dev Biol 103:109–116PubMedGoogle Scholar
  38. Mita K, Yamashita M (2000) Expression of Xenopus Daz-like protein during gametogenesis and embryogenesis. Mech Dev 94:251–255CrossRefPubMedGoogle Scholar
  39. Moriya N, Uchiyama H, Asashima M (1993) Induction of pronephric tubules by activin and retinoic acid in presumptive ectoderm of Xenopus laevis. Dev Growth Differ 35:123–128Google Scholar
  40. Nieuwkoop PD, Sutasurya LA (1979) Primordial germ cells in the chordates. Cambridge University Press, CambridgeGoogle Scholar
  41. Nieuwkoop PD, Sutasurya LA (1981) Primordial germ cells in the invertebrates. Cambridge University Press, CambridgeGoogle Scholar
  42. Okada Y, Ichikawa M (1947) Normal table of Triturus (Cynops) pyrrhogaster. Jpn J Exp Morphol 3:1–6Google Scholar
  43. Reijo RA, Lee TY, Salo P, Alagappan R, Brown LG, Rosenberg M, Rozen S, Jaffe T, Straus D, Hovatta O et al. (1995) Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein. Nat Genet 10:383–393CrossRefPubMedGoogle Scholar
  44. Ruggiu M, Speed R, Taggart M, Mckay SJ, Kilanowski F, Saunders P, Dorin J, Cooke HJ (1997) The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389:73–77CrossRefPubMedGoogle Scholar
  45. Saxena R, Brown LG, Hawkins T, Alagappan RK, Skaletsky H, Reeve MP, Reijo R, Rozen S, Dinulos MB, Disteche CM, Page DC (1996) The DAZ gene cluster on the human Y chromosome arose from an autosomal gene that was transposed, repeatedly amplified and pruned. Nat Genet 14:292–9CrossRefPubMedGoogle Scholar
  46. Sekizaki H, Takahashi S, Tanegashima K, Onuma Y, Haramoto Y, Asashima M (2004) Tracing of Xenopus tropicalis germ plasm and presumptive primordial germ cells with the Xenopus tropicalis DAZ-like gene. Dev Dyn 229:367–372CrossRefPubMedGoogle Scholar
  47. Smith LD, Michael P, Williams MA (1983) Does a predetermined germ line exist in amphibians?. In: McLaren A, Wylie CC (eds) Current problems in germ cell differentiation. Cambridge University Press, London, pp 19–39Google Scholar
  48. Strome S, Garvin C, Paulsen J, Capowski E, Martin P, Beanan M (1994) Specification and development of the germline in Caenorhabditis elegans. Ciba Foundation symposium 182. Wylie, Chichester, pp 31–51Google Scholar
  49. Sutasurya LA, Nieuwkoop PD (1974) The induction of the primordial germ cells in the urodeles. Wilhelm Roux’ Arch Entwicklungsmech Org 175:199–220Google Scholar
  50. Takabatake T, Takahashi TC, Inoue K, Ogawa M, Takeshima K (1996) Activation of two Cynops genes, fork head and sonic hedgehog, in animal cap explants. Biochem Biophys Res Commun 218:395–401CrossRefPubMedGoogle Scholar
  51. Wakahara M (1977) Partial characterization of ‘primordial germ cell-forming activity’ localized in vegetal cytoplasm in anuran egg. J Embryol Exp Morphol 39:221–233PubMedGoogle Scholar
  52. Wakahara M (1978) Induction of supernumerary primordial germ cells by injecting vegetal pole cytoplasm into Xenopus eggs. J Exp Zool 203:159–164Google Scholar
  53. Wakahara M (1990) Cytoplasmic localization of and organization of germ-cell determinants. In: Malacinski GM (eds) Cytoplasmic organization system. McGraw-Hill, New York, pp 219–242Google Scholar
  54. Wakahara M (1996) Primordial germ cell development: is the urodele pattern closer to mammals than to anurans? Int J Dev Biol 40:653–659PubMedGoogle Scholar
  55. Whitington P, Dixon KE (1975) Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis. J Embryol Exp Morphol 33:57–74PubMedGoogle Scholar
  56. Williams MA, Smith LD (1971) Ultrastructure of the ‘germinal plasm’ during maturation and early cleavage in Rana pipiens. Dev Biol 25:568–580PubMedGoogle Scholar
  57. Xu EY, Moore FL, Reijo RA (2001) A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in metazoans. Proc Natl Acad Sci USA 98:7414–7419CrossRefPubMedGoogle Scholar
  58. Yamashita M, Yoshikuni M, Hirai T, Fukada S, Nagahama Y (1991) A monoclonal antibody against the PSTAIR sequence of p34cdc2, catalytic subunit of maturation-promoting factor and key regulator of the cell cycle. Dev Growth Differ 33:617–624Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Yoichiro Tamori
    • 1
  • Toshiharu Iwai
    • 1
  • Koichi Mita
    • 1
  • Masami Wakahara
    • 1
  1. 1.Division of Biological Sciences, Graduate School of ScienceHokkaido UniversitySapporoJapan

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