Karyomeres in early cleavage embryos of ophryotrocha labronica lagreca and bacci

  • Hadar Emanuelsson


Karyomeres or chromosome vesicles occur regularly at all cell divisions in cleavage embryos ofOphryotrocha labronica up to the 16-cell stage. They are formed as separate units, containing one or several nucleolus-like bodies (NLB) as well as intranuclear annulate lamellae (IAL), but coalesce later into a compound nucleus, in connection with copious blebbing and simultaneous appearance of cytoplasmic annulate lamellae (CAL). Labelling of the early embryos with3H-thymidine revealed marked localization of the synthesized DNA to the karyomere envelope region, whereas3H-uridine incorporation, indicating RNA synthesis, was sparse and notably absent in the NLB. On the other hand the latter structure like the envelopes preferentially incorporated3H-myoinositol, and displayed considerable labelling with3H-leucine. The mechanism and general significance of karyomere formation is discussed with particular attention to the NLB and their possible involvement in nuclear membrane formation.

Key words

Karyomere Nuclear envelope Nucleolus-like body Annulate lamellae DNA synthesis 


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  1. Alfert, M., Das, N. K.: Evidence for control of the rate of nuclear DNA synthesis by the nuclear membrane in eukaryotic cells. Proc. nat. Acad. Sci. (Wash.)63, 123–128 (1969).Google Scholar
  2. Bernhard, W.: Ultrastructure of the cancer cell. In: Handbook of molecular cytology (ed. A. Lima-De-Faria), p. 687–715. Amsterdam: North-Holland 1969.Google Scholar
  3. Calarco, P. G., Donahue, R. P., Szollosi, D.: Germinal vesicle breakdown in the mouse oocyte. J. Cell Sci.10, 369–385 (1972).Google Scholar
  4. Comings, D. E., Kakefuda, T.: Initiation of deoxyribonuoleic acid replication at the nuclear membrane in human cells. J. molec. Biol.33, 225–229 (1968).Google Scholar
  5. Comings, D. E., Okada, T. A.: Association of chromatin fibers with the annuli of the nuclear membrane. Exp. Cell Res.62, 293–302 (1970a)Google Scholar
  6. Comings, D. E., Okada, T. A.: Association of nuclear membrane fragments with metaphase and anaphase chromosomes as observed by whole mount electron microscopy. Exp. Cell Res.63, 62–68 (1970b).Google Scholar
  7. Conklin, E. G.: Karyokinesis and cytokinesis in the maturation, fertilization and cleavage of Crepidula and other gastropods. J. Acad. Nat. Sci. Phila.12, 5–121 (1902).Google Scholar
  8. Dhainaut, A.: Présence de membranes annelées extra- et intra-micléaires au cours de l'ovogenèse naturelle et expérimentale chez Nereis pelagica L. (Annélide Polychète). C. R. Soc. Biol. (Paris)160 749–752 (1966).Google Scholar
  9. Deumling, B., Franke, W. W.: Nuclear membranes from mammalian liver. V. Hoppe-Seylers Z. physiol. Chem.353, 287–297 (1972).Google Scholar
  10. Emanuelsson, H.: Cell multiplication in the chick blastoderm up to the time of laying. Exp. Cell Res.39, 386–399 (1965).Google Scholar
  11. Everingham, J. W.: Attachment of intranuclear annulate lamellae to the nuclear envelope. J. Cell Biol.37, 540–550 (1968a).Google Scholar
  12. Everingham, J. W.: Intranuclear annulate lamellae in ascidian embryos. J. Cell Biol.37, 551–554 (1968b).Google Scholar
  13. Folliot, R.: Les lamelles annelées intranucléaires des cellules du tissu germinal mâle avant la méiose chez Philaenus spumarius L. (Insecte Homoptère). Z. Zellforsch.92, 115–129 (1968).Google Scholar
  14. Franke, W. W., Scheer, U.: Some structural differentiations in the HeLa cell: heavy bodies, annulate lamellae, and cotte de maillet endoplasmic reticulum. Cytobiol.4, 317–329 (1971).Google Scholar
  15. Franke, W. W., Scheer, U., Fritsch, H.: Intranuclear and cytoplasmic annulate lamellae in plant cells. J. Cell Biol.53, 823–827 (1972).Google Scholar
  16. Fry, H. J.: Studies of the mitotic figure. V. The time schedule of mitotic changes in developing Arbacia eggs. Biol. Bull.70, 89–99 (1936).Google Scholar
  17. Graham, C. F., Morgan, R. W.: Changes in the cell cycle during early amphibian development. Develop. Biol.14, 439–460 (1966).Google Scholar
  18. Harris, P.: Electron microscope study of mitosis in sea urchin blastomeres. J. biophys. biochem. Cytol.11, 419–431 (1961).Google Scholar
  19. Hay, E. D., Gurdon, J. B.: Fine structure of the nucleolus in normal and mutant Xenopus embryos. J. Cell Sci.2, 151–162 (1967).Google Scholar
  20. Hillman, N., Tasca, R. J.: Ultrastructural and autoradiographic studies of mouse cleavage Amer. J. Anat.126, 151–174 (1969).Google Scholar
  21. Hinegardner, R. T., Rao, B., Feldman, D. E.: The DNA synthetis period during the early development of the sea urchin egg. Exp. Cell Res.36, 53–61 (1964).Google Scholar
  22. Hokin, L. E., Huebner, D.: Radioautographic localization of the increased synthesis of phosphatidylinositol in response to panereozymin or acetylcholine in guinea pig pancreas slices. J. Cell Biol.33, 521–530 (1967).Google Scholar
  23. Hsu, W. S.: The origin of annulate lamellae in the ovocyte of the ascidian Boltenia villosa Stimpson. Z. Zellforsch.82, 376–390 (1967).Google Scholar
  24. Jollie, W. P.: Nuclear and cytoplasmic annulate lamellae in trophoblast giant cells of rat placenta. Anat. Rec.165, 1–14 (1969).Google Scholar
  25. Karasaki, S.: Electron microscopic examination of the sites of nuclear RNA synthesis during amphibian embryogenesis. J. Cell Biol.26, 937–958 (1965).Google Scholar
  26. Karasaki. S.: The ultrastructure and RNA metabolism of nucleoli in early sea urchin embryos. Exp. Cell Res.52, 13–26 (1968).Google Scholar
  27. Kay, R. R., Haines, M. E., Johnston, I. R.: Late replication of the DNA associated with the nuclear membrane. Febs lettres16, 233–236 (1971).Google Scholar
  28. Kessel, R. G.: Electron microscope studies on the origin of annulate lamellae in oocytes of Necturus. J. Cell Biol.19, 391–414 (1963).Google Scholar
  29. Kessel, R. G.: Intranuclear annulate lamellae in ovocytes of the tunicate, Styela partita. Z. Zellforsch.63, 37–51 (1964).Google Scholar
  30. Kessel, R. G.: Annulate lamellae. J. Ultrastruct. Res., Suppl.10, 1–82 (1968).Google Scholar
  31. Kezer, J., Macgregor, H. C., Sohabtach, E.: Observations on the membraneous components of amphibian oocyte nucleoli. J. Cell Sci.8, 1–17 (1971).Google Scholar
  32. LaCour, LF., Chayen, J., Gahan, P. S.: Evidence for lipid material in chromosomes. Exp. Cell Bes.14, 469–485 (1958).Google Scholar
  33. Lewis, W. H.: Interphase (resting) nuclei, chromosomal vesicles and amitosis, Anat. Rec.97, 433–445 (1947).Google Scholar
  34. Mazia, D.: Mitosis and the physiology of cell division. In: The cell (eds. Brachet, J. and A. E. Mirsky), vol. III., p. 77–412. New York: Academic Press Inc. 1961.Google Scholar
  35. Mizuno, N. S., Stoops, C. E., Pfeiffer, R. L., Jr.: Nature of the DNA associated with the nuclear envelope of regenerating liver. J. molec. Biol.59, 517–525 (1971).Google Scholar
  36. O'Brien, R. L., Sanyal, A. B., Stanton, R. H.: Association of DNA replication with the nuclear membrane of HeLa cells. Exp. Cell Res.70, 106–112 (1972).Google Scholar
  37. Ollerich, D. A., Carlson, E. C.: Ultrastructure of intranuclear annulate lamellae in giant cells of rat placenta. J. Ultrastruct. Res.30, 411–422 (1970).Google Scholar
  38. Panel on ribosome biogenesis. Nat. Cancer Inst. Monogr.23, 547–562 (1966).Google Scholar
  39. Phillips, S. G.: Repopulation of the postmitotic nucleolus by preformed RNA. J. Cell Biol.53, 611–623 (1972).Google Scholar
  40. Rouser, G., Nelson, G. I., Fleischer, S., Simon, G.: Lipid composition of animal cell membranes, organelles and organs. In: Biological membranes (ed. D. Chapman), p. 5–70. New York: Academic Press Inc. 1968.Google Scholar
  41. Solomon, J. B.: Increase of deoxyribonucleic acid and cell number during morphogenesis of the early chick embryo. Biochim. biophys. Acta (Amst.)23, 24–27 (1957)Google Scholar
  42. Stevens, B. J., André, J.: The nuclear envelope. In: Handbook of molecular cytology (ed. A. Lima-De-Faria), p. 839–871. Amsterdam: North-Holland 1969.Google Scholar
  43. Thomas, C.: Correlation between ultrastructural aspect of nucleoli and inhibition of ribosomal RNA synthesis in Xenopus laevis oocytes. Exp. Cell Res.74, 547–551 (1972).Google Scholar
  44. Wilson, E. B.: The cell in development and heredity. Fifth printing. New York: Macmillan Co. 1953.Google Scholar
  45. Wischnitzer, S.: The annulate lamellae. Int. Rev. Cytol.27, 65–100 (1970).Google Scholar
  46. Yoshida, S., Modak, M. J., Yagi, K.: DNA polymerase associated with nuclear membrane of calf thymus. Biochem. biophys Res. Commun.43, 1408–1414 (1971).Google Scholar
  47. Yoshikawa-Fukada, M., Ebert, J. D.: DNA synthesis by an insoluble chromatin fraction. Biochem. biophys. Res. Commun.43, 133–141 (1971).Google Scholar

Copyright information

© Springer-Verlag 1973

Authors and Affiliations

  • Hadar Emanuelsson
    • 1
  1. 1.Zoophysiological InstituteUniversity of LundSweden

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