Skip to main content
SpringerLink
Log in

Variations in mitochondrial size and ultrastructure during germ cell development

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Size variations and ultrastructural changes in mitochondria of developing germ cells of the female hamster were analyzed. Mitochondria in oogonia of foetus and newborn were elongate with transverse cristae. During pre-dictyate meiotic prophase they became small, rounded, and electron-dense with pleomorphic cristae. These changes were largely reversed when dictyate was reached. Maximum mitochondrial size and complexity of cristae were reached just at the beginning of the phase of rapid oocyte growth, and thereafter declined. As mitochondrial size and number of cristae decreased in the rapidly enlarging oocyte, the ratio of length to width increased, as did electron density of the matrix, until the formation of an antrum within the follicle. After antrum formation, the mitochondria again became more rounded and cristae were seldom seen. An attempt is made to correlate changes of mitochondrial morphology with other events occurring during oogenesis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson, E., Beams, H.W.: Cytological observations on the fine structure of the guinea pig ovary with special reference to the oogonium, primary oocyte and associated follicle cells. J. Ultrastruct. Res. 3, 432–446 (1960)

    Google Scholar 

  • Anderson, E., Condon, W., Sharp, D.: A study of oogenesis and early embryogenesis in the rabbit, Oryctolagus cuniculus, with special reference to the structural changes of mitochondria. J. Morph. 130, 67–92 (1970)

    Google Scholar 

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

    Google Scholar 

  • Barer, R., Joseph, S., Meek, G.A.: The origin and fate of the nuclear membrane in meiosis. Proc. roy. Soc. B 152, 353–366 (1960)

    Google Scholar 

  • Beams, H.W., Kessel, R.G.: Problem of germ cell determinants. Int. Rev. Cytol. 39, 413–479 (1974)

    Google Scholar 

  • Bellairs, R.: The conversion of yolk into cytoplasm in the chick blastoderm as shown by electron microscopy. J. Embryol. exp. Morph. 6, 129–161 (1958)

    Google Scholar 

  • Beltermann, R.: Elektronenmikroskopische Befunde bei beginnender Follikelatresie im Ovar der Maus. Arch. Gynäk. 200, 601–609 (1965)

    Google Scholar 

  • Biggers, J.D.: Metabolism of the oocyte. In: Oogenesis (eds. J.D. Biggers and A.W. Schuetz), pp. 241–251. London: Butterworths 1972

    Google Scholar 

  • Biggers, J.D., Whittingham, D.G., Donahue, R.P.: The pattern of energy metabolism in the mouse oocyte and zygote. Proc. nat. Acad. Sci. (Wash.) 58, 560–567 (1967)

    Google Scholar 

  • Chase, J.W., Dawid, I.B.: Biogenesis of mitochondria during Xenopus laevis development. Develop. Biol. 27, 504–518 (1972)

    Google Scholar 

  • Clerot, J.-C.: Mise en évidence par cytochimie ultrastructurale de l'émission de protéines par le noyau d'auxocytes de Batraciens. J. Microscopie 7, 973–992 (1968)

    Google Scholar 

  • Czolowska, R.: Observations on the origin of the “germinal cytoplasm” in Xenopus laevis. J. Embryol. exp. Morph. 22, 229 (1969)

    Google Scholar 

  • Dhainaut, A.: Étude en microscopie électronique et par autoradiographie à haute résolution des extrusions nucléaires au cours de l'ovogénèse de Nereis pelagica (Annélide Polychète). J. Microscopie 9, 99–118 (1970)

    Google Scholar 

  • Droller, M.J., Roth, T.F.: An electron microscope study of yolk formation during oogenesis in Lebistes reticulatus guppy. J. Cell Biol. 28, 209–232 (1966)

    Google Scholar 

  • Eddy, E.M.: Fine structural observations on the form and distribution of nuage in germ cells of the rat. Anat. Rec. 178, 731–758 (1974)

    Google Scholar 

  • Eddy, E.M., Ito, S.: Fine structural and radioautographic observations on dense perinuclear cytoplasmic material in tadpole oocytes. J. Cell Biol. 49, 90–108 (1971)

    Google Scholar 

  • Enders, A.C., Schlafke, S.J.: Fine structure of the blastocyst: some comparative studies. In: Ciba Foundation Symposium on preimplantation stages of pregnancy (eds. G.E.W. Wolstenholme and M. O'Connor), pp. 29–54. London: J. & A. Churchill, Ltd. 1965

    Google Scholar 

  • Enders, A.C., Schlafke, S.J.: A morphological analysis of the early implantation stages in the rat. Amer. J. Anat. 120, 1–12 (1967)

    Google Scholar 

  • Grillo, M.A.: Cytoplasmic inclusion bodies resembling nucleoli in sympathetic neurons of adult rats. J. Cell Biol. 45, 100–117 (1970)

    Google Scholar 

  • Hackenbrock, C.R.: Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J. Cell Biol. 30, 269–297 (1966)

    Google Scholar 

  • Hackenbrock, C.R.: Ultrastructural bases for metabolically linked mechanical activity in mitochondria. II. Electron transport-linked ultrastructural transformations in mitochondria. J. Cell Biol. 37, 345–369 (1968)

    Google Scholar 

  • Hadek, R.: The structure of the mammalian egg. Int. Rev. Cytol. 18, 29–71 (1965)

    Google Scholar 

  • Halkka, L., Halkka, O.: Accumulation of gene products in the oocytes of the dragonfly Cordulia aenea L. The nematosomes. J. Cell Sci. 19, 103–116 (1975)

    Google Scholar 

  • Hernandez-Verdun, D.: Étude cytochimique du corps glomérulaire dans le trophoblaste de Souris J. Ultrastruct. Res. 40, 68–86 (1972)

    Google Scholar 

  • Hertig, A.T., Barton, B.R.: Fine structure of mammalian oocytes and ova. In: Handbook of physiology (eds. Greep, R.O. and E.B. Astwood), Sect. 7, Endocrinology, Vol. 2, Female reproductive system, Part 1, Chap. 13, pp. 317–348. Washington, D.C.: American Physiological Society 1973

    Google Scholar 

  • Hope, J.: The fine structure of the developing follicle of the Rhesus monkey. J. Ultrastruct. Res. 12, 592–610 (1965)

    Google Scholar 

  • Karasaki, S.: Studies on amphibian yolk. I. The ultrastructure of the yolk platelet. J. Cell Biol. 18, 33–48 (1963)

    Google Scholar 

  • Kellems, R.E., Allison, V.F., Butow, R.A.: Cytoplasmic type 80S ribosomes associated with yeast mitochondria. II. Evidence for the association of cytoplasmic ribosomes with the outer mitochondrial membrane in situ. J. clin. Invest. 53, 3297–3303 (1974)

    Google Scholar 

  • Kellems, R.E., Allison, V.F., Butow, R.A.: Cytoplasmic type 80S ribosomes associated with yeast mitochondria. IV. Attachment of ribosomes to the outer membrane of isolated mitochondria. J. Cell Biol. 65, 1–14 (1975)

    Google Scholar 

  • Kellems, R.E., Butow, R.A.: Cytoplasmic type 80S ribosomes associated with yeast mitochondria. 3. Changes in the amount of bound ribosomes in response to changes in metabolic state. J. clin. Invest. 53, 3304–3310 (1974)

    Google Scholar 

  • Kessel, R.G.: Cytodifferentiation in the Rana pipiens oocyte. I. Association between mitochondria and nucleolus-like bodies in young oocytes. J. Ultrastruct. Res. 28, 61–77 (1969)

    Google Scholar 

  • Kishi, K.: Fine structural and cytochemical observations on cytoplasmic nucleolus-like bodies in nerve cells of rat medulla oblongata. Z. Zellforsch. 132, 523–532 (1972)

    Google Scholar 

  • Lanzavecchia, G., Mangioni, C.: Étude de la structure des constituants du follicle humain dans l'ovaire foetal. I. Le follicle primordial. J. Microscopie 3, 447–464 (1964)

    Google Scholar 

  • Lardy, H.A., Ferguson, S.M.: Oxidative phosphorylation in mitochondria. A. Rev. Biochem. 38, 991–1034 (1969)

    Google Scholar 

  • LeBeaux, Y.J., Langelier, P., Poirier, L.J.: Further ultrastructural data on the cytoplasmic nucleolus resembling bodies or nematosomes. Their relationship with the synaptic web and a cytoplasmic filamentous network. Z. Zellforsch. 118, 147–155 (1971)

    Google Scholar 

  • Martin, B.J., Spicer, S.S.: Ultrastructural features of cellular maturation and aging in human trophoblast. J. Ultrastruct. Res. 43, 133–149 (1973)

    Google Scholar 

  • Massover, W.H.: Intramitochondrial yolk-crystals of frog oocytes. I. Formation of yolk-crystal inclusions by mitochondria during bullfrog oogenesis. J. Cell Biol. 48, 266–279 (1971a)

    Google Scholar 

  • Massover, W.H.: Intramitochondrial yolk-crystals of frog oocytes. II. Expulsion of intramitochondrial yolk-crystals to form single-membrane bound hexagonal crystalloids. J. Ultrastruct. Res. 36, 603–620 (1971b)

    Google Scholar 

  • Morita, M., Best, J.B., Noel, J.: Electron microscopic studies of planarian regeneration. I. Fine structure of neoblasts in Dugesia dorotocephala. J. Ultrastruct. Res. 27, 7–23 (1969)

    Google Scholar 

  • Nass, S.: The significance of the structural and functional similarities of bacteria and mitochondria. Int. Rev. Cytol. 25, 55–129 (1969)

    Google Scholar 

  • Nayyar, R.P.: The yolk nucleus of fish oocytes. Quart. J. micr. Sci. 105, 353–358 (1964)

    Google Scholar 

  • Norrevang, A.: Electron microscopic morphology of oogenesis. Int. Rev. Cytol. 23, 113–186 (1968)

    Google Scholar 

  • Odor, D.L.: The ultrastructure of unilaminar follicles of the hamster ovary. Amer. J. Anat. 116, 493–522 (1965)

    Google Scholar 

  • Packer, L., Wrigglesworth, J.M., Fortes, P.A.G., Pressman, B.C.: Expansion of the inner membrane compartment and its relation to mitochondrial volume and ion transport. J. Cell Biol. 39, 382–391 (1968)

    Google Scholar 

  • Peach, R.: Nematosomes in trigeminal ganglia. J. Cell Biol. 55, 718–721 (1972)

    Google Scholar 

  • Petit, J.: Étude morphologique et cytochimique de deux types de groupements mitochondriaux dans les jeunes ovocytes. J. Microscopie 17, 41–54 (1973)

    Google Scholar 

  • Pressman, B.C.: Induced active transport of ions in mitochondria. Proc. nat. Acad. Sci. (Wash.) 53, 1076–1083 (1965)

    Google Scholar 

  • Rasmussen, H., Chance, B., Ogata, E.: A mechanism for the reactions of calcium with mitochondria. Proc. nat. Acad. Sci. (Wash.) 53, 1069–1076 (1965)

    Google Scholar 

  • Raven, C.P.: Oogenesis: The storage of developmental information. Oxford and New York: Pergamon Press 1961

    Google Scholar 

  • Rouiller, C.: Physiological and pathological changes in mitochondrial morphology. Int. Rev. Cytol. 9, 227–292 (1960)

    Google Scholar 

  • Sanchez, S.: Formation et rôle des nucléoles des ovocytes de Trituras helveticus Raz-Étude autoradiographique et ultramicroscopique. J. Embryol. exp. Morph. 22, 127–143 (1969)

    Google Scholar 

  • Schatz, G., Mason, T.L.: The biosynthesis of mitochondrial proteins. A. Rev. Biochem. 43, 51–87 (1974)

    Google Scholar 

  • Schlafke, S., Enders, A.C.: Cytological changes during cleavage and blastocyst formation in the rat. J. Anat. (Lond.) 102, 13–32 (1967)

    Google Scholar 

  • Spirin, A.S.: On “masked” forms of messenger RNA in early embryogenesis and in other differentiating systems. In: Current topics in developmental biology, Vol. I, pp. 1–38. London: Academic Press 1966

    Google Scholar 

  • Spirin, A.S.: Informosomes. Europ. J. Biochem. 10, 20–35 (1969)

    Google Scholar 

  • Srivastava, M.D.L.: Cytoplasmic inclusions in oogenesis. Int. Rev. Cytol. 18, 73–98 (1965)

    Google Scholar 

  • Stern, S., Biggers, J.D., Anderson, E.: Mitochondria and early development of the mouse. J. exp. Zool. 176, 179–192 (1971)

    Google Scholar 

  • Szollosi, D.: Development of “yolky substance” in some rodent eggs. Anat. Rec. 151, 424 (Abs.), (1965)

    Google Scholar 

  • Terakado, K.: Origin of yolk granules and their development in the snail, Physia acuta. J. Electron Microsc. 23, 99–106 (1974)

    Google Scholar 

  • Van Dam, K., Meyer, A.J.: Oxidation and energy conservation by mitochondria. A. Rev. Biochem. 40, 115–160 (1971)

    Google Scholar 

  • Wartenberg, H., Stegner, H.E.: Über die elektronenmikroskopische Feinstruktur des menschlichen Ovarialeies. Z. Zellforsch. 52, 450–474 (1960)

    Google Scholar 

  • Weakley, B.S.: Electron microscopy of the oocyte and granulosa cells in the developing ovarian follicles of the golden hamster (Mesocricetus auratus). J. Anat. (Lond.) 100, 503–534 (1966)

    Google Scholar 

  • Weakley, B.S.: Light and electron microscopy of developing germ cells and follicle cells in the ovary of the golden hamster: twenty-four hours before birth to eight days post partum. J. Anat. (Lond.) 101, 435–459 (1967a)

    Google Scholar 

  • Weakley, B.S.: “Balbiani's Body” in the oocyte of the golden hamster. Z. Zellforsch. 83, 582–588 (1967b)

    Google Scholar 

  • Weakley, B.S.: Investigations into the structure and fixation properties of cytoplasmic lamellae in the hamster oocyte. Z. Zellforsch. 81, 91–99 (1967c)

    Google Scholar 

  • Weakley, B.S.: Comparison of cytoplasmic lamellae and membranous elements in the oocytes of five mammalian species. Z. Zellforsch. 85, 109–123 (1968)

    Google Scholar 

  • Weakley, B.S.: Granular cytoplasmic bodies in oocytes of the golden hamster during the post-natal period. Z. Zellforsch. 101, 394–400 (1969a)

    Google Scholar 

  • Weakley, B.S.: Initial stages in the formation of cytoplasmic lamellae in the hamster oocyte and the identification of electron dense particles. Z. Zellforsch. 97, 438–448 (1969b)

    Google Scholar 

  • Weakley, B.S.: Basic protein and ribonucleic acid in the cytoplasm of the ovarian oocyte in the golden hamster. Z. Zellforsch. 112, 69–84 (1971)

    Google Scholar 

  • Weibel, E.R.: Stereological techniques for electron microscopic morphometry. In: Principles and techniques of electron microscopy (ed. M.A. Hayat), Biological applications, Vol. 3, pp. 237–296. London and New York: Van Nostrand Reinhold Co., 1973

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, University of Dundee, Dundee, Scotland

    Brenda S. Weakley

Authors
  1. Brenda S. Weakley
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The author wishes to thank the Department of Anatomy, University of Dundee, for financial support and for the use of the AEI EM 801 electron microscope

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weakley, B.S. Variations in mitochondrial size and ultrastructure during germ cell development. Cell Tissue Res. 169, 531–550 (1976). https://doi.org/10.1007/BF00218151

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00218151

Key words

Search

Navigation