Skip to main content
Log in

Expansive growth of the nuclear envelope and formation of mitochondria in ganglionic neuroblasts

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

Zusammenfassung

Während des 4. und 5. Bruttages differenzieren sich im lateroventralen Abschnitt der Spinalganglien des Hühnerembryos viele Neuroblasten. In diesen Neuroblasten nimmt das Chondriom stark zu und man findet gleichzeitig folgende Strukturen: a) Rollen, aus Membranen gebildet, die einen komplizierten, von Fall zu Fall verschiedenen Verlauf aufweisen. Die Rollen setzen sich in die äußere Nuclearmembran fort. Zwischen ihren Membranen liegen elektronenoptisch dichte, den Ribosomen ähnelnde Granula. b) Membranrollen, deren peripherer halbmondförmiger Abschnitt feinkörniges Material enthält. c) Rollen, deren Membranen sich in die Außenmembran und die Cristae umfangreicher, unregelmäßig geformten Mitochondrien fortsetzen. d) Übergangsformen zwischen denen unter b) und c) beschrieben.

Die äußere Nuclearmembran, die Membranen der beschriebenen Rollen und der Mitochondrien weisen die gleiche Dicke auf. Die Membranen, welche eine der unter a) geschilderten Rollen bilden und jene, die sich in einem der umfangreichen Mitochondrien befinden (c), haben Oberflächen von gleicher Größenordnung.

Unter den verschiedenen Hypothesen zur Interpretation der Befunde verdient folgende den Vorzug, da sie eine klare Deutung aller gewonnenen Befunde erlaubt: die äußere Nuclearmembran dehnt sich aus und führt auf diese Weise zur Entstehung einer Membranrolle. In dieser Rolle bildet sich sodann ein körniges Material, den Vorläufer der MitochondrienMatrix. Die Menge des körnigen Materials nimmt zu, gleichzeitig wickeln sich nach und nach die Membranenrollen ab und bilden die Hülle und die Cristae eines umfangreichen Mitochondrions. Letzteres teilt sich endlich in mehrere kleinere Mitochondrien auf. Während der Neuroblastendifferenzierung der Spinalganglien des Hühnerembryos geht also die Bildung von Mitochondrien von der Nuclearhülle aus.

Summary

Many neuroblasts undergo differentiation in the lateroventral region of spinal ganglia in chick embryos at the 4th to 5th incubation day. In these neuroblasts a striking increase in the chondriome has been recorded, and the following structures have been observed. a) Whorls of membranes which are continuous with the outer nuclear membrane: ribosomelike granules lie in the intramembranous spaces of these whorls, b) Membranous whorls with a peripheral portion, crescent-shaped in the sections, containing a minute granular material, c) Membranous whorls which are continuous with the membranes of the envelope, and of the cristae of large, irregular mitochondria. d) Formations which are transitional in structure between the ones mentioned above.

No significant differences were recorded of the thickness of the outer nuclear membrane, of the whorls' membranes, and of the mitochondrial membranes. Beside, the mean values of the total area of the membranes of each whorl of the type listed under a), and of the total area of the membranes of large mitochondria, such as listed under c), are of the same order of magnitude.

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.

References

  • André, J.: Contribution à la connaissance du chondriome. J. Ultrastruct. Res. 3, Suppl., 1–185 (1962).

    Google Scholar 

  • —, et V. Marinozzi: Présence, dans les mitochondries, de particules ressemblant aux ribosomes. J. Microscopie 4, 615–626 (1965).

    Google Scholar 

  • Bade, E. G.: Bildung von Mitochondrien in der regenerierenden Leber der Maus. Z. Zellorsch. 61, 754–768 (1964).

    Google Scholar 

  • Bahr, G. F., and E. Zeitler: Study of mitochondria in rat liver. Quantitative electron microscopy. J. Cell Biol. 15, 489–501 (1962).

    Google Scholar 

  • Balinsky, B. I., and R. J. Devis: Origin and differentiation of cytoplasmic structures in the oocytes of Xenopus laevis. Acta Embryol. Morph. exp. (Palermo) 6, 55–108 (1963).

    Google Scholar 

  • Behnke, O., and H. Moe: An electron microscope study of mature and differentiating Paneth cells in the rat, especially of their endoplasmic reticulum and lysosomes. J. Cell Biol. 22, 633–652 (1964).

    Google Scholar 

  • Bell, P. R., and K. Mühlethaler: The degeneration and reappearance of mitochondria in the egg cells of a plant. J. Cell Biol. 20, 235–248 (1964).

    Google Scholar 

  • Belt, W. D.: The origin of adrenal cortical mitochondria and liposomes. A preliminary report. J. biophys. biochem. Cytol. 4, 337–340 (1958).

    Google Scholar 

  • Berg, W. E., and W. J. Humphreys: Electron microscopy of four-cell stages of the Ascidians Ciona and Styela. Develop. Biol. 2, 42–60 (1960).

    Google Scholar 

  • Berger, E. R.: Mitochondria genesis in the retinal photoreceptor inner segment. J. Ultrastruct. Res. 11, 90–111 (1964).

    Google Scholar 

  • Bernhard, W., F. Haguenau, A. Gautier et C. Oberling: La structure submicroscopique des éléments basophiles cytoplasmiques dans le foie, le pancréas, et les glandes salivaires. Z. Zellforsch. 37, 281–300 (1952).

    Google Scholar 

  • —: Close topographical relationship between mitochondria and ergastoplasma of liver cells in a definite phase of cellular activity. J. biophys. biochem. Cytol. 2, Suppl., 73–78 (1956).

    Google Scholar 

  • Brandt, P. W., and G. D. Pappas: Mitochondria. II. The nuclear-mitochondrial relationship in Pelomyxa carolinensis Wilson. J. biophys. biochem. Cytol. 6, 91–96 (1959).

    Google Scholar 

  • Buvat, R.: Sur la néoformation de mitochondries à partir du phragmoplaste, dans le méristème radiculaire du Blé. C. R. Acad. Sci. (Paris) 248, 1014–1017 (1959).

    Google Scholar 

  • Chèvremont, M.: Etude des chondriosomes par la mioroscopie et la microcinématographie en contraste de phase. Mon. zool. ital. 61, Suppl., 127–130 (1953).

    Google Scholar 

  • —, S. Chèvremont-Comhaire et B. Baeckeland: Action de désoxyribonucléases neutre et acide sur des cellules somatiques vivantes cultivées in vitro. Arch. Biol. (Liège) 70, 811–831 (1959).

    Google Scholar 

  • David, H.: Zur Mitochondrienneubildung in den Leberzellen des Feuersalamanders (Salamandra maculata). Z. Zellforsch. 57, 567–571 (1962).

    Google Scholar 

  • De Robertis, E., and H. Bleichmar: Mitochondriogenesis in nerve fibers of the infrared receptor membrane of pit vipers. Z. Zellforsch. 57, 572–582 (1962).

    Google Scholar 

  • Duvall, A. J., and J. Wersäll: Site of action of streptomycin upon inner ear sensory cells. Acta oto-laryng. (Stockh.) 57, 581–598 (1964).

    Google Scholar 

  • Elliott, A. M., and I. J. Bak: The fate of mitochondria during aging in Tetrahymena pyriformis. J. Cell Biol. 20, 113–129 (1964).

    Google Scholar 

  • Essner, E., and A. B. Novikoff: Acid phosphatase activity in hepatic lysosomes: electron microscopic demonstration of its reaction product. J. Histochem. Cytochem. 8, 318–318 (1960).

    Google Scholar 

  • —: Localization of acid phosphatase activity in hepatic lysosomes by means of electron microscopy. J. biophys. biochem. Cytol. 9, 773–784 (1961).

    Google Scholar 

  • Fawcett, D.: Observations on the cytology and electron microscopy of hepatic cells. J. nat. Cancer Inst. 15, Suppl., 1475–1502 (1955).

    Google Scholar 

  • Ferreira, J. F. D.: A diferenciação do condrioma aparelho de Golgi e ergastoplasma. Dissertaçao de candidatura ao grau de Doctor. Lisboa: Ramos, Alfonso e Moita, LDA, 1959.

    Google Scholar 

  • Fletcher, M. J., and D. R. Sanadi: Turnover of rat liver mitochondria. Biochim. biophys. Acta (Amst.) 51, 356–360 (1961).

    Google Scholar 

  • Frederic, J.: Recherches cytologiques sur le chondriome normal ou soumis à l'expérimentation dans des cellules vivantes cultivées in vitro. Arch. Biol. (Liège) 69, 167–349 (1958).

    Google Scholar 

  • Furieri, P.: Osservazioni ultrastrutturali sullo spermio di Testudo Hermanni Gmelin. Boll. Soc. ital. Biol. sper. 41, 144–145 (1965).

    Google Scholar 

  • Galey, F.: A mechanical technique for trimming tissue blocks in electron microscopy. J. Ultrastruct. Res. 9, 139–142 (1963).

    Google Scholar 

  • Geren, B. B., and F. O. Schmitt: The structure of the Schwann cell and its relation to the axon in certain invertebrate nerve fibers. Proc. nat. Acad. Sci. (Wash.) 40, 863–870 (1954).

    Google Scholar 

  • Gey, G. O., P. Shapras, F. B. Bang, and M. K. Gey: Some relations of inclusion droplets (pinocytosis, Lewis) and mitochondrial behavior in normal and malignant cells. In: Fine structure of cells, p. 38–54. Groningen: P. Noordhoff 1955.

    Google Scholar 

  • Gross, P. R., D. E. Philpott, and S. Nass: Electron microscopy of the centrifuged sea urchin egg, with a note on the structure of the ground cytoplasm. J. biophys. biochem. Cytol. 7, 135–142 (1960).

    Google Scholar 

  • Hamburger, V.: The effects of wing bud extirpation on the development of the central nervous system in chick embryos. J. exp. Zool. 68, 449–494 (1934).

    Google Scholar 

  • Harvey, E. B.: Structure and development of the clear quarter of the Arbacia punctulata egg. J. exp. Zool. 102, 253–275 (1946).

    Google Scholar 

  • Hoffman, H., and G. W. Grigg: An electron microscopic study of mitochondria formation. Exp. Cell Res. 15, 118–131 (1958).

    Google Scholar 

  • Hudson, G., and J. F. Hartmann: The relationship between dense bodies and mitochondria in motor neurones. Z. Zellforsch. 54, 147–157 (1961).

    Google Scholar 

  • Karasaki, S.: Electron microscopic studies on cytoplasmic structures of ectoderm cells of the triturus embryo during the early phase of differentiation. Embryologia (Nagoya) 4, 247–272 (1959).

    Google Scholar 

  • Kessel, R. G.: The formation and subsequent differentiation of cytoplasmic vesicles in oocytes of necturus. Anat. Rec. 145, 363 (1963).

    Google Scholar 

  • —: Electron microscope studies on oocytes of an echinoderm, Thyone briareus, with special reference to the origin and structure of the annulate lamellae. J. Ultrastruct. Res. 10, 498–514 (1964).

    Google Scholar 

  • Kislev, N., H. Swift, and L. Bogorad: Nucleic acids of chloroplasts and mitochondria in Swiss chard. J. Cell Biol. 25, 327–344 (1965).

    Google Scholar 

  • Lafontaine, J. G., and C. Allard: A light and electron microscope study of the morphological changes induced in rat liver cells by the azo dye 2-Me-Dab. J. Cell Biol. 22, 143–172 (1964).

    Google Scholar 

  • Lansing, A. I., J. Hillier, and T. B. Rosenthal: Electron microscopy of some marine egg inclusions. Biol. Bull. 103, 294 (1952).

    Google Scholar 

  • Lanzavecchia, G., e A. Le Coultre: Origine dei mitocondri durante lo sviluppo emhrionale di Rana esculenta. Arch. ital. Anat. Embriol. 63, 445–458 (1958).

    Google Scholar 

  • —, e C. Mangioni: Moltiplicazione dei mitocondri in oociti di Xenopus laevis D. Istituto Lombardo (Rend. Sci.) B 97, 341–365 (1963).

    Google Scholar 

  • Lever, J. D.: Physiologically induced changes in adrenocortical mitochondria. J. biophys. biochem. Cytol. 2, Suppl., 313–318 (1956).

    Google Scholar 

  • Levi-Montalcini, R., et G. Levi: Recherches quantitatives sur la marche du processus de différenciation des neurones dans les ganglions spinaux de l'embryon de poulet. Arch. Biol. (Liège) 54, 189–206 (1943).

    Google Scholar 

  • Lewis, M. R., and W. H. Lewis: Mitochondria (and other cytoplasmic structures) in tissue culture. Amer. J. Anat. 17, 339–401 (1915).

    Google Scholar 

  • Linnane, A. W., E. Vitols, and P. G. Nowland: Studies on the origin of yeast mitochondria. J. Cell Biol. 13, 345–350 (1962).

    Google Scholar 

  • Luck, D. J. L.: Formation of mitochondria in Neurospora crassa. A quantitative radioautographic study. J. Cell Biol. 16, 483–499 (1963).

    Google Scholar 

  • —: Formation of mitochondria in Neurospora crassa. J. Cell Biol. 24, 461–470 (1965).

    Google Scholar 

  • Lund, H. A., A. E. Vatter, and J. B. Hanson: Biochemical and cytological changes accompanying growth and differentiation in the roots of Zea mays. J. biophys. biochem. Cytol. 4, 87–98 (1958).

    Google Scholar 

  • Maltzahn, K. V., and K. Mühlethaler: Observations on division of mitochondria in dedifferentiating cells of Splachnum ampullaceum (L.) Hedw. Experientia (Basel) 18, 315 (1962).

    Google Scholar 

  • Menefee, M. G., and V. J. Evans: Structural differences produced in mammalian cells by changes in their environment. J. nat. Cancer Inst. (Wash.) 25, 1303–1323 (1960).

    Google Scholar 

  • Nass, M. M. K., and S. Nass: Intramitochondrial fibers with DNA characteristics. I and II. J. Cell Biol. 19, 593–611, 613–629 (1963).

    Google Scholar 

  • —: and B. A. Afzelius: The general occurrence of mitochondrial DNA. Exp. Cell Res. 37, 516–539 (1965).

    Google Scholar 

  • Newcomer, E. H.: Mitochondria in plants. Bot. Rev. 6, 85–147 (1940).

    Google Scholar 

  • Oberling, C.: The structure of cytoplasm. Int. Rev. Cytol. 8, 1–31 (1959).

    Google Scholar 

  • Pannese, E.: Formazione delle membrane di mitocondri dall'involucro nucleare in neuroblasti. Boll. Soc. It. Biol. Sper. 41, 407–410 (1965).

    Google Scholar 

  • Pannese, E.: Structures possibly related to the formation of new mitochondria in spinal ganglion neuroblasts. J. Ultrastruct. Res. 15, 57–65 (1966).

    Google Scholar 

  • Parks, H. F.: Unusual formations of ergastoplasm in parotid acinous cells of mice. J. Cell Biol. 14, 221–234 (1962).

    Google Scholar 

  • Pasteels, J. J., P. Castiaux, et G. Vandermeerssche: Ultrastructure du cytoplasme et distribution de l'acide ribonucleique dans l'œuf fecondé, tant normal que centrifugé de Paracentrotus lividus. Arch. Biol. (Liège) 69, 627–643 (1959).

    Google Scholar 

  • Policard, A., et A. Collet: Certains rapports inframicroscopiques entre mitochondries et éléments du réticulum endoplasmique. Bull. Micr. appl. 3, 71–73 (1958).

    Google Scholar 

  • Porter, K. R.: The endoplasmic reticulum: some current interpretations of its forms and functions. In: Biological structure and function, vol. 1, p. 127 (T. W. Goodwin and O. Lindberg ed.). London and New York: Academic Press 1961a.

    Google Scholar 

  • —: The ground substance; observations from electron microscopy. In: The cell, vol. 2, p. 621–675 (J. Brachet and A. E. Mirsky, ed.), London and New York: Academic Press 1961 b.

    Google Scholar 

  • Robertson, J. D.: The ultrastructure of cell membranes and their derivatives. Biochem. Soc. Symp. 16, 3–43 (1959).

    Google Scholar 

  • Roth, L. E.: An electron microscope study of the cytology of the protozoan Euplotes patella. J. biophys. biochem. Cytol. 3, 985–1000 (1957).

    Google Scholar 

  • Rouiller, C., and W. Bernhard: „Microbodies” and the problem of mitochondrial regeneration in liver cells. J. biophys. biochem. Cytol. 2, Suppl., 355–359 (1956).

    Google Scholar 

  • Schjeide, O. A., and R. McCandless: On the formation of mitochondria. Growth 26, 309–321 (1962).

    Google Scholar 

  • —, R. G. McCandless, and R. J. Munn: Mitochondrial morphogenesis. Nature (Lond.) 203, 158–160 (1964).

    Google Scholar 

  • Schulz, H.: Die Pathologie der Mitochondrien im Alveolarepithel der Lunge. Beitr. path. Anat. 119, 45–70 (1958).

    Google Scholar 

  • Stoeckenius, W.: Some electron microscopical observations on liquid-crystalline phases in lipid-water systems. J. Cell Biol. 12, 221–229 (1962).

    Google Scholar 

  • —, J. H. Schulman, and L. M. Prince: The structure of myelin figures and microemulsions as observed with the electron microscope. Kolloid-Z. 169, 170–182 (1960).

    Google Scholar 

  • Stroganova, N. S., and M. A. Monakhova: The formation of mitochondria from the cellwall in spermatogonia of the grain mite. Dokl. Akad. Nauk SSSR 160, 937–939 (1965).

    Google Scholar 

  • Tahmisian, T. N., E. L. Powers, and R. L. Devine: Light and electron microscope studies of morphological changes of mitochondria during spermatogenesis in the grasshopper. J. biophys. biochem. Cytol. 2, Suppl., 325–330 (1956).

    Google Scholar 

  • Wallace, P. G., and A. W. Linnane: Oxygen-induced synthesis of yeast mitochondria. Nature (Lond.) 201, 1191–1194 (1964).

    Google Scholar 

  • Weissenfels, N.: Über die Entleerung und Entwicklung der Mitochondrien und den Feinbau des Cytoplasmas von embryonalen Zellen. Z. Naturforsch. 13b, 182–186 (1958).

    Google Scholar 

  • Wohlfarth-Bottermann, K. E.: Cytologische Studien. IV. Die Entstehung, Vermehrung und Sekretabgabe der Mitochondrien von Paramecium. Z. Naturforsch. 12b, 164–167 (1957).

    Google Scholar 

  • Yamamoto, T.: On the thickness of the unit membrane. J. Cell Biol. 17, 413–422 (1963).

    Google Scholar 

  • Zollinger, H. U.: Les mitochondries. Rev. Hémat. 5, 696–745 (1956).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Research supported by a C.N. R. grant.

I wish to thank Prof. R. Amprino and Prof. J. D. Robertson for much useful discussion and criticism, Dr. phis. S. de Petris for the help given in the statistical evaluation of the data, Mrs. G. Fiori for technical assistance, and Miss A. Bertolasi for drawing Fig. 17.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pannese, E. Expansive growth of the nuclear envelope and formation of mitochondria in ganglionic neuroblasts. Zeitschrift für Zellforschung 72, 295–324 (1966). https://doi.org/10.1007/BF00341538

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00341538

Keywords

Navigation