Skip to main content
Log in

Ultrastructural study on nuclear-cytoplasmic relationships in oocytes of the African lungfish, Protopterus aethiopicus

I. Nucleolo-cytoplasmic pathways

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

Growing oocytes of Protopterus, like those of some amphibians and teleosts, show an impressive development of the nucleolar apparatus. Numerous nucleolus-like bodies establish close spatial relationships with the nuclear envelope by extending pedicels and streams of finely dispersed material towards the inner membrane.

At such contact points, gaps in the perinuclear cistern are more frequent than elsewhere along the nuclear boundary. Expansion of the outer nuclear membrane gives rise to blebs, with or without visible content, and these become pinched off to form small vesicles in the perinuclear cytoplasm.

Small, electron dense aggregates, indistinguishable from nucleolar material occur on both sides of the nuclear envelope opposite to each other, some being connected by a slender portion of the same material within a nuclear pore. Such accumulations are interpreted as detached parts of nucleolar bodies in transit to cytoplasmic sites where they presumably participate in the biogenesis of ribosomes. At the height of nucleolar emission, nucleoplasm and perinuclear cytoplasm are so rich in small electron dense particles that they are almost indistinguishable from each other.

At this stage of massive transport, the route provided by the nuclear pores seems to be insufficient and another, more spacious, gateway may be in operation. The latter involves direct passage of material across the nuclear membranes preferentially where these form blebs.

This view is supported not only by the overt spatial relationships between nucleolar pedicels and blebs, but by the occurrence within perinuclear lacunae and blebs of particles that seem to be derived from nucleolar bodies. Furthermore, frequent interruptions in the nuclear membranes preferentially located where they expand into outpocketings suggest that at these sites temporary gateways may exist in the living cell that permit easy access of intranuclear components to the cytoplasm.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson, E., and H. W. Beams: Evidence from electron micrographs for the passage of material through pores of the nuclear membrane. J. biophys. biochem. Cytol., 2, Suppl. (Arden House Conference) 439–443 (1956).

    Google Scholar 

  • Arndt, E. A.: Die Aufgaben des Kerns während der Oogenese der Teleosteer. Z. Zellforsch. 51, 356–378 (1960).

    Google Scholar 

  • Beermann, W.: Control of differentiation at the chromosomal level. J. exp. Zool. 157, 49–61 (1964).

    Google Scholar 

  • Bernhard, W.: Ultrastructural aspects of the normal and pathological nucleolus in mammalian cells. Nat. Cancer Inst. Monogr. 23, 13–38 (1966).

    Google Scholar 

  • —, and N. Granboulan: Electron microscopy of the nucleolus in vertebrate cells. In: The nucleus, ed. by A. J. Dalton and F. Haguenau, p. 81–149. New York and London: Acad. Press 1968.

    Google Scholar 

  • Bertolini, B., e E. Urbani: Le cellule nutrici dell' oocite di Dytiscus marginalis L.: Osservazioni al microscopio elettronico. Rend. Accad. naz. Lincei (8) 36, 240–242 (1964).

    Google Scholar 

  • Brown, D. D.: The genes for ribosomal RNA and their transcription during amphibian development. Curr. Topics in develop. Biol. 2, 47–73 (1967).

    Google Scholar 

  • —, and I. B. Dawid: Specific gene amplification in oocytes. Science 160, 272–280 (1968).

    Google Scholar 

  • Darnell, J. E.: Ribonucleic acids from animal cells. Bact. Rev. 32, 262–290 (1968).

    Google Scholar 

  • Feldherr, C. M.: The effect of the electron-opaque pore material on exchanges through the nuclear annuli. J. Cell Biol. 25, 43–53 (1965).

    Google Scholar 

  • Follett, B. K., and H. Heller: The neurohypophysial hormones of lungfishes and amphibians. J. Physiol. (Lond.) 172, 92–106 (1964).

    Google Scholar 

  • Haggis, G. H.: The electron microscope in molecular biology. New York: John Wiley & Sons 1966.

    Google Scholar 

  • Hay, E. D.: Structure and function of the nucleolus in developing cells. In: The nucleus, ed. by A. J. Dalton and F. Haguenau, p. 1–79. New York and London: Academic Press 1968.

    Google Scholar 

  • Kessel, R. G.: An electron microscope study of nuclear-cytoplasmic exchange in oocytes of Ciona intestinalis. J. Ultrastruct. Res. 15, 181–196 (1966a).

    Google Scholar 

  • —: Some observations on the ultrastructure of the oocyte of Thyone briareus with special reference to the relationship of the Golgi complex and endoplasmic reticulum in the formation of yolk. J. Ultrastruct. Res. 16, 305–319 (1966b).

    Google Scholar 

  • —: Mechanisms of protein yolk synthesis and deposition in crustacean oocytes. Z. Zellforsch. 89, 17–38 (1968).

    Google Scholar 

  • Loewenstein, W.: Permeability of the nuclear membrane as determined with electrical methods. Protoplasmatologia 5 (2), 26–34 (1964).

    Google Scholar 

  • Miller, O. L.: Studies on the ultrastructure and metabolism of nucleoli in amphibian oocytes. Vth Intern. Congr. El. micr. 2, NN-8 (S. S. Breese, edit.). New York and London: Acad. Press 1962.

    Google Scholar 

  • —: Structure and composition of peripheral nucleoli of salamander oocytes. Nat. Cancer Inst. Monogr. 23, 53–66 (1966).

    Google Scholar 

  • Nørrevang, A.: Oogenesis in Priapulus caudatus Lamarck. Vidensk. Medd. Dansk Naturh. Foren. 128, 1–84 (1965).

    Google Scholar 

  • —: Electron microscopic morphology of oogenesis. Int. Rev. Cytol. 2, 113–186 (1968).

    Google Scholar 

  • Raven, C. P.: Oogenesis: The storage of developmental information. New York-Oxford-London-Paris: Pergamon Press (Intern. Ser. Monogr. Biol., vol. 10) 1961.

    Google Scholar 

  • Rogers, M. E.: Ribonucleoprotein particles in the amphibian oocyte nucleus. J. Cell Biol. 36, 421–432 (1968).

    Google Scholar 

  • Scharrer, B., and S. Wurzelmann: Ultrastructural study of nucleolar activity in oocytes of the lungfish, Protopterus aethiopicus. Anat. Rec. 157, 316 (1967).

    Google Scholar 

  • —— Ultrastructural study on nuclear-cytoplasmic relationships in oocytes of the African lungfish, Protopterus aethiopicus. II. The microtubular apparatus of the nuclear envelope. Z. Zellforsch. (in press) (1969).

  • Stevens, B. J., and H. Swift: RNA transport from nucleus to cytoplasm in Chironomus salivary glands. J. Cell Biol. 31, 55–77 (1966).

    Google Scholar 

  • Szollosi, D.: Extrusion of nucleoli from pronuclei of the rat. J. Cell Biol. 25, 545–562 (1965).

    Google Scholar 

  • Vincent, W. S., and O. L. Miller (eds.): Proceedgs. Internat. Sympos. on the Nucleolus (Montevideo, Uruguay, Dec. 1965). Nat. Cancer Inst. Monogr. 23 (Washington, D.C., 630 pp.) (1967).

  • Wessing, A.: Der Nucleolus und seine Beziehungen zu den Ribosomen des Cytoplasmas. Eine Untersuchung an den Malpighischen Gefäßen von Drosophila melanogaster. Z. Zellforsch. 65, 445–480 (1965).

    Google Scholar 

  • Weston, J. C.: Ribosome-like granules within areas of the perinuclear space in cells of 13–14 somite chick embryos. Z. Zellforsch. 87, 199–209 (1968).

    Google Scholar 

  • Wiener, J., D. Spiro, and W. R. Loewenstein: Ultrastructure and permeability of nuclear membranes. J. Cell Biol. 27, 107–117 (1965).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by grants AM-3984, NB-00840, and NB-05219 from the U.S.P.H.S.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scharrer, B., Wurzelmann, S. Ultrastructural study on nuclear-cytoplasmic relationships in oocytes of the African lungfish, Protopterus aethiopicus . Z. Zellforsch. 96, 325–343 (1969). https://doi.org/10.1007/BF00335212

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00335212

Keywords

Navigation