Skip to main content
Log in

Centriole replication during ciliogenesis in the chick tracheal epithelium

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

Summary

Morphological aspects of centriole replication as displayed in tracheal epithelial cells of 15 to 19-day-old chick embryos during ciliogenesis were examined by electron microscopy. It was found that centriole replication and development take place in a finely fibrous region around the two mature centrioles of the diplosome. Procentrioles in early stages of development are observed in clusters. The core of each cluster is occupied by one or more cylindrical structures which gradually disappear as the procentrioles mature. Some of the procentriolar clusters are attached directly to the walls of the diplosomal centrioles by the cylindrical cores. This observation suggests that all of the clusters may form initially in close association with the diplosomal centrioles.

The earliest recognizable procentrioles are short, cylindrical structures that have no microtubules. Later microtubules appear, first as singlets, then doublets and finally as triplets. The singlet becomes the innermost microtubule of the triplet. Following the assembly of the nine triplets, the procentrioles separate from the clusters, elongate to their mature length and acquire rootlets, ciliary vesicles and cilia. The observation that all the procentrioles in each cell are in the same stage of development indicates that all the centrioles or presumptive basal bodies required by this cell are produced at the same time.

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

  • Allen, R. D.: The morphogenesis of basal bodies and accessory structures of the cortex of the ciliated protozoan Tetrahymena pyriformis. J. Cell Biol. 40, 716–733 (1969).

    Google Scholar 

  • Bernhard, W., et E. de Harven: L'ultrastructure du centriole et d'autres éléments de l'appareil achromatique. Proc. Fourth Intern. Conf. Electron Microscopy, vol. 2, p. 217–227. Berlin-Göttingen-Heidelberg: Springer 1960.

    Google Scholar 

  • Dippel, R. V.: How ciliary basal bodies develop. Science 158, 527 (1967).

    Google Scholar 

  • Dirksen, E. R.: The presence of centrioles in artificially activated sea urchin eggs. J. biophys. biochem. Cytol. 11, 244–247 (1961).

    Google Scholar 

  • —, and T. T. Crocker: Centriole replication in differentiating ciliated cells of mammalian respiratory epithelium. An electron microscopy study. J. Microscopie 5, 629–644 (1966).

    Google Scholar 

  • Frasca, J. M., O. Auerbach, V. R. Parks, and W. Stoeckenius: Electron microscopic observations of bronchial epithelium. II. Filosomes. Exp. molec. Path. 8, 92–104 (1967).

    Google Scholar 

  • Gall, J. G.: Centriole replication. A study of spermatogenesis in the snail Viviparus. J. biochem. and biophys. Cytol. 10, 163–209 (1961).

    Google Scholar 

  • Johnson, U. G., and K. R. Porter: Fine structure of cell division in Chlamydomonas Reinhardi. Basal bodies and microtubules. J. Cell Biol. 38, 403–425 (1968).

    Google Scholar 

  • Kalnins, V. I.: Ultrastructural observations on the development of cilia in the trochophore of Nereis limbata. Biol. Bull. 133, 472 (1967).

    Google Scholar 

  • Lucas, A.M.: Ciliated epithelium. In: Special Cytology. E.V. Cowdry, ed., 2nd ed. New York: Paul B. Hoeber, Inc. 1932.

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  • Lwoff, A.: Problems of morphogenesis in ciliates. New York: J. Wiley & Sons, Inc. 1950.

    Google Scholar 

  • Martínez Martínez, P. et W. T. Daems: Les phases précoces de la formation des cils et le problème de l'origine du corpuscule basal. Z. Zellforsch. 87, 46–68 (1968).

    Google Scholar 

  • Massover, W. H.: Cytoplasmic cylinders in bullfrog oocytes. J. Ultrastruct. Res. 22, 159–167 (1968).

    Google Scholar 

  • Mizukami, I., and J. Gall: Centriole replication. II. Sperm formation in the fern Marsilea and the cycad Zamia. J. Cell Biol. 29, 97–111 (1966).

    Google Scholar 

  • Porter, K. R.: Cytoplasmic microtubules and their functions. In: Ciba Foundation Symposium. Principles of biomolecula rorganization (G.E.W. Wolstenholme and M. O'Connor, eds.). J. & A. Churchill Ltd. London 1966.

    Google Scholar 

  • Renaud, F. L., and H. Swift: The development of basal bodies and flagella in Allomyces arbusculus. J. Cell Biol. 23, 339–354 (1964).

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Robinow, C., and J. Marak: A fiber apparatus in the nucleus of the yeast cell. J. Cell Biol. 29, 129–151 (1966).

    Google Scholar 

  • Sabatini, D. D., K. Bensch, and R. J. Barrnett: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963).

    Google Scholar 

  • Schreiner, A., u. K. Schreiner: Über die Entwicklung der männlichen Geschlechtszellen von Myxine glutinosa (L.) II. Die Centriolen und ihre Vermehrungsweise. Arch. Biol. (Liège) 21, 315–355 (1905).

    Google Scholar 

  • Schuster, F. L.: An electron microscope study of the amoebo-flagellate, Naegleria gruberi (Schardinger). I. The amoeboid and flagellate stages. J. Protozool. 10, 297–313 (1963).

    Google Scholar 

  • Sorokin, S. P.: Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15, 363–377 (1962).

    Google Scholar 

  • —: Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 3, 207–233 (1968).

    Google Scholar 

  • Steinman, R. M.: An electron microscopic study of ciliogenesis in developing epidermis and trachea in the embryo of Xenopus laevis. Amer. J. Anat. 122, 19–56 (1968).

    Google Scholar 

  • Stockinger, L., u. E. Cireli: Eine bisher unbekannte Art der Zentriolenvermehrung. Z. Zellforsch. 68, 733–740 (1965).

    Google Scholar 

  • Watson, M. L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This investigation was supported by a post-doctoral fellowship from the National Research Council of Canada and by Medical Research Council of Canada grant MA-3302 to V. I. Kalnins and by a training grant from the USPHS (5 T01 GM00707) to K. R. Porter. We wish to thank Mrs. Helen Lyman for the drawing in this paper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kalnins, V.I., Porter, K.R. Centriole replication during ciliogenesis in the chick tracheal epithelium. Z. Zellforsch. 100, 1–30 (1969). https://doi.org/10.1007/BF00343818

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00343818

Keywords

Navigation