Skip to main content
Log in

The tissue dynamics of heart morphogenesis I. The phenomena of cell death

A. Identification and morphology

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

Summary

  1. 1.

    The morphology and some histochemical aspects of spontaneous cell death associated with the development of the chick embryo heart were studied.

  2. 2.

    The degenerative phenomena in the bulbar cushions on the 4th to 5th day of incubation, as based on hematoxylin-eosin staining, were ascertained by means of methyl green-pyronine staining, PAS, Feulgen and acid phosphatase reactions, supravital Nile blue sulphate and neutral red stainings as well as electron microscopy.

  3. 3.

    The degenerating, dying or dead cells were found to be Feulgen-positive. Some were PAS-positive. The staining pattern with methyl green-pyronine indicated DNA and RNA materials.

  4. 4.

    The macrophages appearing on the 5th day of incubation in bulbar cushions stained supravitally with Nile blue sulphate and neutral red, and large quantities of acid phosphatase could be demonstrated.

  5. 5.

    The electron microscope studies confirmed increased autophagic activity at the begining of degeneration and the appearance of macrophages in the later stages.

  6. 6.

    With increasing embryonal age large pycnotic figures became rare and fine degeneration granules prevailed.

  7. 7.

    Until the 6th day of incubation the degenerating and/or dead cells were lysed in situ if isolated, or phagocytized by neighbouring mesenchymal cells if present in greater quantities. They could also be expelled to different tissue boundaries.

  8. 8.

    As from the 8th day of incubation, some of the degenerating and dead cells were concentrated around blood vessels. They were also seen in heart cavities and in blood vessel lumina.

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

  • Ballard, K.J., Holt, S.J.: Cytological and cytochemical studies on cell death and digestion on the foetal rat foot: the role of macrophages and hydrolytic enzymes. J. Cell Sci. 3, 245–262 (1968).

    Google Scholar 

  • Barka, T., Anderson, P.J.: Histochemistry. Theory, practice and bibliography. New York: Harpers & Row 1963.

    Google Scholar 

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

    Google Scholar 

  • Bengmark, S., Forsberg, J.G.: Some remarks on degeneration granules in the genital sphere. Z. Zellforsch. 49, 694–698 (1959).

    Google Scholar 

  • Center, E.M.: Changes in the distribution of acid phosphatase in limbs of syndactyly (jt) mice and of alkaline phosphatase in limbs of luxoid (lu) mice. Abstract. Anat. Rec. 163, 170 (1970).

    Google Scholar 

  • Chang, T.K.: Cellular inclusions and phagocytosis in normal development of mouse embryos. Peking. Nat. Hist. Bull. 14, 159–169 (1939).

    Google Scholar 

  • David, H.: Sterben und Tod der Zelle. Mber. Dtsch. Akad. Wiss. 7, 452–463 (1965).

    Google Scholar 

  • Deleanu, M.: Leg differentiation and experimental syndactyly in chick embryo. I. Degenerative phenomena during toes differentiation in chick embryo. Rev. roum. Embryol. Cytol. SĂ©r. Embryol. 1, 61–69 (1964).

    Google Scholar 

  • Ernst, M.: Ăśber Untergang von Zellen während der normalen Entwicklung bei Wirbeltieren. Z. Anat. Entwickl.-Gesch. 79, 228–262 (1926).

    Google Scholar 

  • Fallon, J. F., Saunders, J. W., Jr.: In vitro analysis of the control of cell death in a zone of prospective necrosis from the chick embryo wing bud. Develop. Biol. 18, 553–570 (1968).

    Google Scholar 

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

    Google Scholar 

  • Fell, H. B., Andrews, J. A.: A cytological study of cultures in vitro of Jensen rat sarcoma. Brit. J. exp. Path. 8, 413–428 (1927).

    Google Scholar 

  • Florez-Cossio, T. J.: Wachstum als entwicklungsphysiologisches Problem. Med. Welt 20, 1379–1381 (1969).

    Google Scholar 

  • Forsberg, J. G.: On the development of the cloaca and the perineum and the formation of the urethral plate in female rat embryos. J. Anat. (Lond.) 95, 423–436 (1961).

    Google Scholar 

  • Forsberg, J. G.: Derivation and differentiation of the vaginal epithelium. Thesis. Lund: Hakan Olssons Boktryckeri 1963.

    Google Scholar 

  • Forsberg, J. G.: Studies on the cell degeneration rate during the differentiation of the epithelium in the uterine cervix and MĂĽllerian vagina of mouse. J. Embryol. exp. Morph. 17, 433–440 (1967).

    Google Scholar 

  • Forsberg, J. G., KällĂ©n, B.: Cell death during embryogenesis. Rev. roum. Embryol. Cytol. SĂ©r. Embryol. 5, 91–102 (1968).

    Google Scholar 

  • Forsberg, J. G., Olivecrona, H.: Degeneration process during the development of the MĂĽllerian ducts in alligator and female chicken embryo. Z. Anat. Entwickl.-Gesch. 124, 83–96 (1963).

    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 

  • Ghidoni, J., Campbell, M.: Karyolytic bodies. Arch. Path. 88, 480–488 (1969).

    Google Scholar 

  • GlĂĽcksmann, A.: Ăśber die Bedeutung von Zellvorgängen fĂĽr die Formbildung epithelialer Organe. Z. Anat. Entwickl.-Gesch. 93, 35–92 (1930).

    Google Scholar 

  • GlĂĽcksmann, A.: Cell deaths in normal vertebrate ontogeny. Biol. Rev. 25, 59–86 (1951).

    Google Scholar 

  • GlĂĽcksmann, A., Tansley, K.: Some effects of gamma irradiation on the developing rat retina. Brit. J. Ophthal. 20, 497–509 (1936).

    Google Scholar 

  • Goerttler, Kl.: Die Stoffwechseltopographie des embryonalen HĂĽhnerherzens und ihre Bedeutung fĂĽr die Entstehung angeborener Herzfehler. Verh. dtsch. Ges. Path. 40, 181–185 (1956).

    Google Scholar 

  • Goerttler, Kl.: Der pränatale Organismus als reagierendes Subjekt. Bull. schweiz. Akad. med. Wiss. 20, 336–359 (1964).

    Google Scholar 

  • Hamburger, V.: Regression versus peripheral control of differentiation in motor hypoplasia. Amer. J. Anat. 102, 365–410 (1958).

    Google Scholar 

  • Hammar, S. P., Mottet, S. P.: Tetrazolium salt and electron microscopic studies of cellular degeneration and necrosis in the interdigital areas of the developing chick limb. J. Cell Sci. 8, 229–251 (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 

  • Hourdry, J.: Remaniements ultrastructuraux de l'Ă©pithĂ©lium intestinal chez la larve d'un amphibien anoure en mĂ©tamorphose, Alytes obstetricans Laur. I. PhĂ©nomènes histolytiques. Z. Zellforsch. 101, 527–554 (1969).

    Google Scholar 

  • Hourdry, J.: Etude histochimique de quelques hydrolases lysosomiques de l'Ă©pithĂ©lium intestinal, au cours du dĂ©veloppement de la larve de Discoglossus pictus Otth, amphibien anoure. I. Observations au microscope photonique. Histochimie 26, 126–141 (1971a).

    Google Scholar 

  • Hourdry, J.: Etude histochimique de quelques hydrolases lysosomiques de l'Ă©pithĂ©lium intestinal, au cours du dĂ©veloppement de la larve de Discoglossus pictus Otth, amphibien anoure. II. Observations au microscope Ă©lectronique. Histochimie 26, 266–287 (1971b).

    Google Scholar 

  • Houdry, J.: Evolution des processus lytiques dans l'Ă©pithĂ©lium intestinal de Discoglossus pictus Otth (amphibien anoure) au cours de sa mĂ©tamorphose. J. Microscopie 10, 41–58 (1971c).

    Google Scholar 

  • Hughes, A. F. W.: The histogenesis of arteries in the chick embryo. J. Anat. (Lond.) 77, 266–287 (1948).

    Google Scholar 

  • Illies, A.: La topographie et la dynamique des zones nĂ©crotiques normales chez l'embryon humain. Rev. roum. Embryol. Cytol. SĂ©r. Embryol. 4, 57–85 (1967).

    Google Scholar 

  • KällĂ©n, B.: Degeneration and regeneration in the vertebrate central nervous system during embryogenesis. Progr. Brain Res. 14, 77–96 (1965).

    Google Scholar 

  • Kelley, R. O.: An electron microscopic study of mesenchyme during development of interdigital spaces in man. Anat. Rec. 168, 43–54 (1970).

    Google Scholar 

  • Kieny, M., Pautou, M. P.: Sur le mĂ©canisme de la nĂ©crose morphogène dans le pied de l'embryon de poulet. C. R. Acad. Sci. (Paris), Ser. D. 270, 3091–3094 (1970).

    Google Scholar 

  • Krstić, R., Pexieder, T.: Elektronenmikroskopische Darstellung des Zellunterganges in den HerzbulbuswĂĽlsten des HĂĽhnerembryos. Abstract. Verh. Anat. Schweiz. Hochschulen, Bern, 1971. Acta anat. (Basel). In press.

  • Leuchtenberger, C.: A cytochemical study of pycnotic nuclear degeneration. Chromosoma (Berl.) 3, 449–473 (1947).

    Google Scholar 

  • Littau, V. C., Alfrey, V. G., Frenster, J. K., Mirsky, A. E.: Active and inactive regions of chromatin as revealed by electron microscopy and autoradiography. Proc. nat. Acad. Sci. (Wash.) 52, 93–100 (1964).

    Google Scholar 

  • Love, R., Studzinski, G. P., Walsh, R. J.: Nuclear, nucleolinar and cytoplasmic acid phosphatase in cultured mammalian cells. Exp. Cell Res. 58, 62–72 (1969).

    Google Scholar 

  • Manasek, F. J.: Myocardial cell death in the embryonic chick ventricle. J. Embryol. exp. Morph. 22, 333–348 (1969).

    Google Scholar 

  • Mato, M., Aikawa, E.: Some observations on the obliteration of the ductus arteriosus Botalli. Z. Anat. Entwickl.-Gesch. 127, 327–349 (1968).

    Google Scholar 

  • Mato, M., Aikawa, E., Uchiyama, Y.: Radioautographic study on the obliteration of the ductus arteriosus Botalli. Virchows. Arch. path. Anat. 349, 10–20 (1969).

    Google Scholar 

  • Menkes, B., Alexandru, C., Pavkov, A., Mircova, O.: Researches on the formation and the elastic structure of the aortopulmonary septum in the chick embryo. Rev. roum. Embryol. Cytol. SĂ©r. Embryol. 2, 79–91 (1965).

    Google Scholar 

  • Menkes, B., Deleanu, M., Illies, A.: Comparative studies of some areas of physiological necrosis at the embryo of man, some laboratory animals and fowl. Rev. roum. Embryol. Cytol. SĂ©r. Embryol. 2, 161–172 (1965).

    Google Scholar 

  • Menkes, B, Litvac, B.: Researches at phase contrast and electron microscopy on the necrobiotic processes of the neuroblasts, brought about by intraependymary injection of Janus green in the chick embryo. Rev. roum. Embryol. Cytol. SĂ©r. Embryol. 1, 193–199 (1964).

    Google Scholar 

  • Menkes, B., Litvac, B., Illies, A.: Spontaneous and induced cell degenerescence in relation to teratogenesis. Rev. roum. Embryol. Cytol. SĂ©r. Embryol. 1, 1–60 (1964).

    Google Scholar 

  • Menkes, B., Sandor, S., Illies, A.: Cell death in teratogenesis. In Advances in teratogenesis (ed. D. H. M. Woollam), vol. 4, p. 170–215. Oxford: Logos Press 1970.

    Google Scholar 

  • Mizejewski, G. J., Ramm, G. M.: Phagocytosis as related to the reticuloendothelial system in the developing chick. Growth 33, 47–56 (1969).

    Google Scholar 

  • Paufou, M. P., Kieny, M.: Sur les mĂ©canismes histologiques et cytologiques de la nĂ©crose morphogène interdigitale chez l'embryon de poulet. C. R. Acad. Sci., (Paris) Ser. D 272, 2025–2028 (1971).

    Google Scholar 

  • Pearse, A. G. E.: Histochemistry. Theoretical and applied. London: Churchill 1960.

    Google Scholar 

  • Pexieder, T.: Cell death in the development of the chick embryo heart. Abstract. Proc. XII. Congr. czech. morphol. with internat. particip. Praha, October, 1969.

  • Pexieder, T.: Zelltod als Faktor bei der Herzentwicklung des HĂĽhnerembryos. Abstract. Acta anat. (Basel) 78, 150 (1971a).

    Google Scholar 

  • Pexieder, T.: Zelluntergang im Herz von HĂĽhnerembryonen zwischen dem 2. und 8. Tag der Entwicklung (Demonstration). Abstract. Acta anat. (Basel) 78, 159 (1971b).

    Google Scholar 

  • Pexieder, T.: Zur quantitativen Auswertung der Gewebedynamik in der Herzorganogenese (mit besonderer BerĂĽcksichtigung des Zelltodes) (Demonstration). Abstract. Acta anat. (Basel) 79, 156–157 (1971c).

    Google Scholar 

  • Pexieder, T.: Die quantitativer Karte des Zellunterganges in der Herzentwicklung der HĂĽhnerembryonen zwischen dem 2. und 8. Tag der Inkubation. Anat. Anz. 128, Erg.-H., 295–300 (1971d).

    Google Scholar 

  • Pexieder, T.: Beobachtungen ĂĽber den lokalen Zelltod während der Herzbulbunsseptierung des HĂĽhnerembryos. Verh. Anat. Ges. Zagreb, 1971. Anat. Anz. In press (1971 e).

  • Pexieder, T.: Ăśber die Wirkung der Hämodynamik auf den Zelluntergang in den HerzbulbuswĂĽlsten des HĂĽhnerembryos. Verh. Anat. Schweiz. Hochschulen, Bern, 1971, Abstract. Acta anat (Basel). In press. (1971f).

  • Politzer, G.: Ăśber einen menschlichen Embryo mit 18 Ursegmentpaaren. Z. Anat. Entwickl.-Gesch. 87, 674–727 (1933).

    Google Scholar 

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

    Google Scholar 

  • Rychter, Z.: The vascular system of the chick embryo. III. On the problem of septation of the heart bulb and trunc in chick embryos. [In Czech, with english summary.]. ÄŚs. Morfol. 7, 1–20 (1959).

    Google Scholar 

  • Rychter, Z., Ošťádal, B.: Periodisation of the blood supply development of the myocardium in chick embryos. Abstract: Physiol. bohemoslov. 17, 485 (1968).

    Google Scholar 

  • Salzgeber, B., Weber, R.: La rĂ©gression du mĂ©sonĂ©phros chez l'embryon de poulet. Etude des activitĂ©s de la phosphatase acide et des cathĂ©psines. Analyse biochimique, histochimique et les observation au microscope Ă©lectronique. J. Embryol. exp. Morph., 15, 379–419 (1966).

    Google Scholar 

  • Salzmann, R., Weber, R.: Histochemical localization of acid phosphatases and cathepsinlike activities in regressing tails of Xenopus larvae at metamorphosis.Experientia (Basel) 19, 352–354 (1963).

    Google Scholar 

  • Sandor, S., Elias, S.: Evolution of circumscribed necrotic areas in the axis of the chick embryo induced by irradiation with ultraviolet rays. Rev roum. Embryol. Cytol. SĂ©r. Embryol. 5, 173–180 (1968).

    Google Scholar 

  • Saunders, J. W., Jr.: Cell death in embryonic systems. Science 154, 604–612 (1966).

    Google Scholar 

  • Saunders, J. W., Jr., Fallon, J. F.: Cell death in morphogenesis. In: Major problems of developmental biology (ed. M. Locke), p. 289–314. New York: Academic Press 1966.

    Google Scholar 

  • Saunders, J. W., Jr., Gasseling, M. T., Saunders, L.: Cellular death in the morphogenesis of the avian wing. Develop. Biol. 5, 147–178 (1962).

    Google Scholar 

  • Scheib, D.: Sur la rĂ©gression du canal de MĂĽller mâle de l'embryon de poulet: localisation de la phosphatase acide au microscope Ă©lectronique. C. R. Acad. Sci. (Paris), Ser. D 261, 5219–5221 (1965).

    Google Scholar 

  • Spear, F. G., GlĂĽcksmann, A.: The effect of gamma irradiation on cells in vivo. Brit. J. Radiol. 11, 533–553 (1938).

    Google Scholar 

  • Strangeways, T. S. P., Oakley, H. E. H.: The immediate changes in tissue cells after exposure to soft X-rays while growing in vitro. Proc. roy. Soc. B 95, 373–381 (1923).

    Google Scholar 

  • Sweney, L. R., Shapiro, B. L.: Histogenesis of Swiss white mouse secondary palate from nine and one half 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, 481–487 (1964).

    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 

  • Wendler, D.: Embryogenese und Degeneration. Morph. Jb. 111, 416–422 (1967).

    Google Scholar 

  • Whitten, J. M.: Cell death during early morphogenesis. Paralleles between insect limb and vertebrate limb development. Science 163, 1456–1457 (1969).

    Google Scholar 

  • Wolf, J.: Microscopic techniques. Praha: SZdN 1952 [In Czech].

    Google Scholar 

  • Zwilling, G.: Controlled degeneration during development.In CIBA Foundation Symposium on Cellular Injury (eds. A. V. S. Reuck, J. Knight), p. 352–361. London: Churchill 1964.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pexieder, T. The tissue dynamics of heart morphogenesis I. The phenomena of cell death. Z. Anat. Entwickl. Gesch. 137, 270–284 (1972). https://doi.org/10.1007/BF00519097

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00519097

Key words

Navigation