Skip to main content
Log in

Ultrastructure of cell death in bulbar cushions of chick embryo heart

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

Summary

The ultrastructure of the “physiological” cell death was studied in distal ventral bulbar cushions of 15 chick embryo hearts on the 4th and 5th day of incubation. Microperfusion fixation was performed. The ultracytochemistry of a lysosomal hydrolytic enzyme acid phosphatase was also investigated in another 15 embryonic hearts.

In the course of the cell degeneration an increase in cellulr autophagy was observed without previous cytoplasmic or nuclear changes or phagocyte ingestion. A cytoplasmic diffusion of acid phosphatase outside of lysosomes was observed.

Besides the cell death with the marked participation of the lysosomal system, another kind of dying cells was found, characterized by their nuclear pycnosis and cytoplasmic condensation. Starting from the 5th day of incubation the dying and dead cells were found phagocytized by some of their neighbouring viable mesenchymal cells. A formation of ribosomal crystals was not observed.

The formation and fate of cytolysomes as well as the fate of phagocytes are discussed. The presence of pre-necrotic cells with important autophagy and of necrotic cells with nuclear changes was related to the possibility of a dual cause of the cell death. In the case of pre-necrotic cells the epigenetic factors like the biomechanic action of hemodynamics were considered, while the necrotic cells seem to be programmed to death by their genome.

Finally the uniformity of cell death ultrastructure in different organs and species was noticed.

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

  • Allenspach, A. L.: Ultrastructural observations of oesophageal organogenesis in the chick embryo. Abstract. J. Cell Biol. 43, 5a (1969).

    Google Scholar 

  • Ballard, K. J.: Studies on the participation of hydrolytic enzymes in physiological autolysis in degenerating regions of the rat foetus. Ph. D. Thesis, University of London (1965).

  • Behnke, O.: Demonstration of acid phophatase containing granules and cytoplasmic bodies in the epithelium of foetal rat duodenum during certain stages of differentiation. J. Cell Biol. 18, 251–265 (1963).

    Google Scholar 

  • Bellairs, R.: Cell death in chick embryos as studied by electron microscope. J. Anat. (Lond.) 95, 54–60 (1961).

    Google Scholar 

  • Birks, R. I., Weldon, P. R.: Formation of crystalline ribosomal arrays in cultured chick embryo dorsal root ganglia. J. Anat. (Lond.) 109, 143–156 (1971).

    Google Scholar 

  • Brusati, R., Miani, C.: Ultrastructural features of the involution of the epithelial sheet of the secondary palate in rats. L'Ateneo Parmense Acta Biomed. 39, 1–11 (1968).

    Google Scholar 

  • Byers, B.: Structure and formation of ribosome crystals in hypothermic chick embryo cells. J. molec. Biol. 26, 155–167 (1967).

    Google Scholar 

  • Coleman, R., Evennett, P. J., Dodd, J. M.: The ultrastructural localization of acid phosphatase, alkaline phosphatase and adenosine triphosphatase in induced goitres of Xenopus laevis Daudin tadpoles. Histochemie 10, 33–43 (1967).

    Google Scholar 

  • Dawd, D. S.: Studies on the “opaque patch” of cell death in the mesenchyme of the developing chick limb. Ph. D. Thesis, University College of Wales, Aberystwyth (1969).

    Google Scholar 

  • Dawd, D. S., Hinchliffe, J. R.: Cell death in the “opaque patch” in the central mesenchyme of the developing chick limb: a cytological, cytochemical and electron microscopic analysis. J. Embryol. exp. Morph. 26, 401–424 (1971).

    Google Scholar 

  • Duve, C. de: The lysosomes concept. In: Lysosomes. Ciba Found. Symp. (eds. A. V. S. de Reuck and J. Knight), p. 1–31. London: Churchill 1963.

    Google Scholar 

  • Duve, C. de, Wattiaux, R.: Functions of lysosomes. Ann. Rev. Physiol. 28, 435–492 (1966).

    Google Scholar 

  • Farbman, A. I.: Electron microscope study of palate fusion in mouse embryos. Develop. Biol. 18, 93–116 (1968).

    Google Scholar 

  • Fox, H.: Tissue degeneration: an electron microscopic study of the pronephros of Rana temporaria. J. Embryol. exp. Morph. 24, 139–157 (1970).

    Google Scholar 

  • Franchi, L. L., Mandl, A. M.: The ultrastructure of oogonia and oocytes in the foetal and neonatal rat. Proc. roy. Soc. B. 157, 99–114 (1962).

    Google Scholar 

  • Hammar, S. P., Mottet, N. K.: Tetrazolium salt and electron microscopic studies of cellular degeneration and necrosis in the interdigital areas of the developing chick limb. J. Cell Sci. 8, 229–252 (1971).

    Google Scholar 

  • Hayward, A. F.: The ultrastructural appearance of cell death in developing tissues. Abstract. J. Anat. (Lond.) 103, 580–581 (1968).

    Google Scholar 

  • Heidekrüger, R., Merker, H. J.: Elektronenmikroskopische Untersuchung der Linsenentwicklung bei Rattenembryonen. Z. Anat. Entwickl.-Gesch. 136, 115–124 (1972).

    Google Scholar 

  • Hourdry, J.: Remaniements ultrastructuraux de l'épithélium intestinal chez la larve d'un amphibien anoure en métamorphose, Alytes obstetricans Laur. I. Phénomènes histolytiques. Z. Zellforsch. 101, 527–554 (1969).

    Google Scholar 

  • Hourdry, J.: Evolution des processus lytiques dans l'épithélium intestinal de Discoglossus pictus Otth (amphibien anoure) au cours de sa métamorphose. J. Microscopie (Paris) 10, 41–58 (1971).

    Google Scholar 

  • Johnson, B.: Studies on the degeneration of flight muscles in alate aphids. II. Histology and control of muscle breakdown. J. Insect Physiol. 3, 367–377 (1959).

    Google Scholar 

  • Jokelainen, P., Jokelainen, G.: Ultrastructural study of cell death in early metanephric nephron unit. Abstract. Anat. Rec. 157, 266–267 (1967).

    Google Scholar 

  • Jurand, A.: Ultrastructural aspects of early development of the forelimb buds in the chick and mouse. Proc. roy. Soc. B 162, 387–405 (1965).

    Google Scholar 

  • Kerr, J. F. R.: Liver cell defaecation: an electron microscope study of the discharge oflysosomal residual bodies into the intercellular space. J. Path. Bact. 100, 99–103 (1970).

    Google Scholar 

  • Kerr, J. F. R.: Shrinkage necrosis: a distinct mode of cellular death. J. Path. Bact. 105, 13–20 (1971).

    Google Scholar 

  • Korfsmeier, K.-H.: Über den Abbau von Zellorganellen in der Gewebekultur. Verh. Anat. Ges. Köln 1972. Anat. Anz., Erg.-H. (1973) (im Druck).

  • Krstić, R., Pexieder, T.: Elektronenmikroskopische Darstellung des Zelluntergangs in den Herzbulbuswülsten des Hühnerembryos. Abstract. Acta anat. (Basel) 82, 470 (1972).

    Google Scholar 

  • Krstić, R., Pexieder, T.: Elektronenmikroskopische Beobachtungen der Kulminationsphase des Zelluntergangs in den Herzbulbuswülsten des Hühnerembryos. Demonstration. Verh. Anat. Ges. Köln 1972. Anat. Anz., Erg.-H. (1973) (im Druck).

  • Manasek, F. J.: Myocardial cell death in the embryonic chick ventricle. J. Embryol. exp. Morph. 21, 271–284 (1969).

    Google Scholar 

  • Maraldi, N. M., Barbieri, M.: Ribosome crystallization during chick embryo development. J. submier. Cytol. 1, 159–170 (1969).

    Google Scholar 

  • Mathiessen, M., Andersen, H.: Disintegration of the junctional epithelium of human fetal hard palate. Z. Anat. Entwickl.-Gesch. 137, 153–169 (1972).

    Google Scholar 

  • Mato, M., Aikawa, E.: Some observations on the obliteration of ductus arteriosus Botalli using the electron microscope. Z. Anat. Entwickl.-Gesch. 127, 327–345 (1968).

    Google Scholar 

  • Mato, M., Aikawa, E., Katahira, M.: Appearance of various types of lysosomes in the epithelium covering lateral palatal shelves during a secondary palate formation. Gunma J. med. Sci. 15, 46–56 (1967).

    Google Scholar 

  • Mato, M., Aikawa, E., Katahira, M.: Alteration of the fine structure of the epithelium on the lateral palatine shelf during the secondary palate formation. Gunma J. med. Sci. 16, 79–99 (1968).

    Google Scholar 

  • Michaels, J. E., Albright, J. T., Patt, D. I.: Fine structural observations on cell death in the epidermis of the external gills of the larval frog, Rana pipiens. Amer. J. Anat. 132, 301–318 (1971).

    Google Scholar 

  • Mottet, N. K., Hammar, S. P.: Ribosome crystals in necrotizing cells from the posterior necrotic zone of the developing chick limb. J. Cell Sci. 11, 403–414 (1972).

    Google Scholar 

  • Neubert-Kirfel, D.: Die Wirkung subletaler Röntgendosen auf das Verdauungssystem kultivierter Hühnerherzmyoblasten. Protoplasma (Wien) 70, 389–404 (1970).

    Google Scholar 

  • Pautou, M., Kieny, M.: Sur les mécanismes histologiques et cytologiques de la nécrose morphogène interdigitale chez l'embryon de poulet. C. R. Acad. Sci. (Paris), Ser. D 272, 2025–2028 (1971).

    Google Scholar 

  • Pexieder, T.: The tissue dynamics of heart morphogenesis. I. Cell death phenomena. B. Topography. Z. Anat. Entwickl.-Gesch. 138, 241–253 (1972a).

    Google Scholar 

  • Pexieder, T.: Becbachtungen über den lokalen Zelltod während der Herzbulbusseptierung des Hühnerembryos. Anat. Anz. 130, Erg.-H., 279–286 (1972b).

    Google Scholar 

  • Pexieder, T.: Über die Wirkung der Haemodynamik auf den Zelluntergang in den Herzbulbuswülsten des Hünnerembryos. Abstract. Acta anat. (Basel) 82, 459–460 (1972c).

    Google Scholar 

  • Pexieder, T.: The tissue dynamics of heart morphogenesis. II. Quantitative investigations. A. Method and Background values. Develop. Biol. (1973a) (in press).

  • Pexieder, T.: The tissue dynamics of heart morphogenesis. II. Quantitative investigations. B. Cell death foci values. Develop. Biol. (1973b) (in press).

  • Pexieder, T.: Über die primären Ursachen des Zelltodes in den Herzbulbuswülsten des Hühnerembryos. Verh. Anat. Ges. Köln 1972. Anat. Anz., Erg.-H. (1973c) (im Druck).

  • Pipan, N., Marin, M.: Autophagie und Glykogenverteilung im Magenepithel der Maus während der Differenzierung. Z. mikr.-anat. Forsch. 85, 421–437 (1972).

    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 

  • Richardson, K. C., Jarett, L., Finke, E. H.: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).

    Google Scholar 

  • Salzgeber, B., Weber, R.: La régression du mésonéphros chez l'embryon de poulet. Etude des activités de la phosphatase acide et des cathepsines. Analyse biochimique, histochemique et les observations au microscope électronique. J. Embryol. exp. Morph. 15, 397–419 (1966).

    Google Scholar 

  • Saunders, J. W. jr.: Death im embryonic systems. Science 154, 604–612 (1966).

    Google Scholar 

  • Saunders, J. W. jr., Fallon, J. F.: Cell death in morphogenesis. Symp. Soc. Develop. Biol. 25, 289–314 (1966).

    Google Scholar 

  • Schäfer, D.: Autophagosomen in gezüchteten Hühnerherzzellen. Z. Zellforsch. 133, 201–210 (1972).

    Google Scholar 

  • Scharrer, B.: Ultrastructural study of the regressing prothoracic glands of blattarian insects. Z. Zellforsch. 69, 1–21 (1966).

    Google Scholar 

  • Scheib, D.: Sur la régression du canal de Müller mâle de l'embryon de poulet: localisation de la phosphatase acide au microscope électronique. C. R. Acad. Sci. (Paris), Ser. D 261, 5219–5221 (1965).

    Google Scholar 

  • Schwarz, W.: Elektronenmikroskopische Untersuchungen an Lysosomen im Blastem der Extremitätenknospe der Ratte. Z. Zellforsch. 73, 27–36 (1966).

    Google Scholar 

  • Schweichel, J. U.: Morphological studies on the problem of physiological cell death during embryonic development. In symposium: Metabolic pathways in mammalian embryos during organogenesis and its modification by drugs. Berlin: Symposium des SFB 29, 1970.

  • Schweichel, J. U.: Das elektronenmikroskopische Bild des Abbaues der epithelialen Scheitelleiste während der Extremitätenentwicklung bei Rattenfeten. Z. Anat. Entwickl.-Gesch. 136, 192–203 (1972).

    Google Scholar 

  • Shapiro, B. L., Sweney, L.: Electron microscopic and histochemical examination of oral epithelial-mesenchymal interaction (programmed cell death). J. dent. Res. 48, 652–660 (1969).

    Google Scholar 

  • Smiley, G. R., Dixon, A. D.: Fine structure of midline epithelium in developing palate of the mouse. Anat. Rec. 161, 293–310 (1968).

    Google Scholar 

  • Sweney, L. R., Shapiro, B. L.: Histogenesis of Swiss white mouse secondary palate from nine and one-half days to fifteen and one-half days in utero. I. Epithelial-mesenchymal relationships. Light and electron microscopy. J. Morph. 130, 435–450 (1970).

    Google Scholar 

  • Weber, R.: Ultrastructural changes in regressing tail muscles of Xenopus larvae at metamorphosis. J. Cell Biol. 22, 481–485 (1964).

    Google Scholar 

  • Weber, R.: Tissue involution and lysosomal enzymes during anuran metamorphosis. In: Lysosomes in biology and pathology (eds. I. T. Dingle and H. B. Fell), vol. 2, p. 437–461. Amsterdam: North Holland Publ. Co. 1969.

    Google Scholar 

  • Webster, D. A., Gross, J.: Studies on possible mechanisms of programmed cell death in the chick embryo. Develop. Biol. 22, 157–184 (1970).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krstić, R., Pexieder, T. Ultrastructure of cell death in bulbar cushions of chick embryo heart. Z. Anat. Entwickl. Gesch. 140, 337–350 (1973). https://doi.org/10.1007/BF00525060

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00525060

Key words

Navigation