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Intercellular bridges between oocytes in the chicken ovary

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Summary

Fine structural analysis of the functional (left) ovary of the newly-hatched chick reveals the presence of true intercellular bridges between developing oocytes in the early stages of the meiotic prophase. These structures are characterized by: 1) cytoplasmic continuity between the participating oocytes, 2) a dense, fibrillar material beneath the lateral limiting membrane and 3) numerous cellular organelles within their confines. In addition, microtubular elements, parallel to the long axis of the bridge, are routinely observed. This latter finding suggests that intercellular bridges originate through incomplete cytokinesis of mitotically active oogonia and that the dense material beneath the limiting membrane may represent the cortical microfilaments associated with the “contractile ring”. Functionally, these structures may serve as channels for transfer of nutrients and organelles between oocytes although the possibility that certain oocytes function as nurse cells, in the sense that these cells exist in invertebrate ovaries, seems unlikely. In addition, intercellular bridges may be responsible for both restriction of oogonial mitoses and meiotic synchrony.

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References

  • Bellairs, R.: Aspects of the development of yolk spheres in the hen's oocyte, studied by electron microscopy. J. Embryol. exp. Morph. 17, 267–281 (1967).

    Google Scholar 

  • Bentfield, M. E.: Studies on oogenesis in the rotifer, Asplanchna. I. Fine structure of the female reproductive system. Z. Zellforsch. 115, 165–183 (1971a).

    Google Scholar 

  • Bentfield, M. E.: Studies on oogenesis in the rotifer. II. Oocyte growth and development. Z. Zellforsch. 115, 184–195 (1971b).

    Google Scholar 

  • Callebaut, M. Bernheim, J. L.: Feulgen-cytophotometric determination of DNA content in the germ cell nuclei of the female chicken embryo during premeiosis. Experientia (Basel) 25, 978–980 (1969).

    Google Scholar 

  • Clawson, R. C., Domm, L. V.: Origin and early migration of primordial germ cells in the chick embryo: a study of the stages definitive primitive streak through eight somites. Amer. J. Anat. 125, 87–112 (1969).

    Google Scholar 

  • Dapples, C. C., King, R. C.: The development of the nucleolus of the ovarian nurse cell of Drosophila melanogaster. Z. Zellforsch. 103, 34–37 (1970).

    Google Scholar 

  • Dubois, R., Croisille, Y.: Germ-cell line and sexual differentiation in birds. Phil. Trans. Roy. Soc. Lond. B 259, 73–89 (1970).

    Google Scholar 

  • Dym, M., Fawcett, D. W.: Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol. Reprod. 4, 195–215 (1971).

    Google Scholar 

  • Fawcett, D. W.: Intercellular bridges. Exp. Cell Res., Suppl. 8, 174–187 (1961).

  • Fawcett, D. W., Ito, S., Slautterback, D. L.: The occurrence of intercellular bridges in groups of cells exhibiting synchronous differentiation. J. biophys. biochem. Cytol. 5, 453–460 (1959).

    Google Scholar 

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

    Google Scholar 

  • Freeman, J. A., Spurlock, B. O.: A new epoxy embedment for electron microscopy. J. Cell Biol. 13, 437–443 (1962).

    Google Scholar 

  • Gondos, B., Zamboni, L.: Ovarian development: the functional importance of germ cell interconnections. Fertil. and Steril. 20, 176–189 (1969).

    Google Scholar 

  • Greenfield, M. L.: The oocyte of the domestic chicken shortly after hatching, studied by electron microscopy. J. Embryol. exp. Morph. 15, 297–316 (1966).

    Google Scholar 

  • Hughes, G. C.: The population of germ cells in the developing female chick. J. Embryol. exp. Morph. 11, 513–536 (1963).

    Google Scholar 

  • Hughes, M., Berry, S. J.: The synthesis and secretion of ribosomes by nurse cells of Anthereaea polyphemus. Develop. Biol. 23, 651–664 (1970).

    Google Scholar 

  • King, R. C., Akai, H.: Spermatogenesis in Bombyx mori. I. The canal systems joining sister spermatocytes. J. Morph. 134, 47–56 (1971).

    Google Scholar 

  • Koch, E. A., King, R. C.: Further studies on the ring canal system of the ovarian cystocytes of Drosophila melanogaster. Z. Zellforsch. 102, 129–152 (1969).

    Google Scholar 

  • Koch, E. A., Smith, P. A., King, R. C.: The division and differentiation of Drosophila cystocytes. J. Morph. 121, 55–70 (1967).

    Google Scholar 

  • MacKinnon, E. A., Basrur, P. K.: Cytokinesis in the gonocysts of the drone honey bee (Apis mellifera, L.). Canad. J. Zool. 48, 1163–1166 (1970).

    Google Scholar 

  • McGregor, J. H.: The spermatogenesis of Amphiuma. J. Morph. 15, 57–104 (1899).

    Google Scholar 

  • Myer, D. B.: The migration of primordial germ cells in the chick embryo. Develop. Biol. 10, 154–190 (1964).

    Google Scholar 

  • Nagano, T.: The structure of cytoplasmic bridges in dividing spermatocytes of the rooster. Anat. Rec. 141, 73–79 (1961).

    Google Scholar 

  • Narbaitz, R.: Ultrastructural aspects of cortical differentiation in chick ovaries and intersexual gonads. Z. Zellforsch. 118, 315–325 (1971).

    Google Scholar 

  • Ribbert, D., Bier, K.: Multiple nucleoli and enhanced nucleolar activity in the nurse cells of the insect ovary. Chromosoma (Berl.) 27, 178–197 (1969).

    Google Scholar 

  • Ruby, J. R., Dyer, R. F., Gasser, R. F., Skalko, R. G.: Intercellular connections between germ cells in the developing human ovary. Z. Zellforsch. 105, 252–258 (1970a).

    Google Scholar 

  • Ruby, J. R., Dyer, R. F., Skalko, R. G.: The occurrence of intercellular bridges during oogenesis in the mouse. J. Morph. 127, 307–340 (1969).

    Google Scholar 

  • Ruby, J. R., Dyer, R. F., Skalko, R. G., Volpe, E. P.: Intercellular bridges between germ cells in the developing ovary of the tadpole, Rana pipiens. Anat. Rec. 167, 1–10 (1970b).

    Google Scholar 

  • Schroeder, T. E.: The contractile ring. I. Fine structure of dividing mammalian (HeLa) cells and the effects of cytochalasin B. Z. Zellforsch. 109, 431–449 (1970).

    Google Scholar 

  • Skalko, R. G., Kerrigan, J. M., Ruby, J. R., Dyer, R. F.: Electron microscopic observations of intercellular bridges between oocytes of the newly hatched chick. Anat. Rec. 169, 430–431 (1971) (abstr.).

    Google Scholar 

  • Swift, C. H.: Origin and early history of the primordial germ-cells in the chick. Amer. J. Anat. 15, 438–516 (1914).

    Google Scholar 

  • Swift, C. H.: Origin of the definitive sex-cells in the female chick and their relation to the primordial germ-cells. Amer. J. Anat. 18, 441–470 (1915).

    Google Scholar 

  • Venable, J. H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1955).

    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 

  • 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 (1967).

    Google Scholar 

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Partial support for this study was provided by grant DE-00241 from the National Institute for Dental Research administered by Dr. Melvin Hess. We gratefully acknowledge his support of the initial aspects of this study. We are pleased to express our appreciation to Mrs. Cindy G. Wilcox, Mr. Lloyd Thibodeau and Mr. Don Driscoll for their expert technical assistance.

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Skalko, R.G., Kerrigan, J.M., Ruby, J.R. et al. Intercellular bridges between oocytes in the chicken ovary. Z.Zellforsch 128, 31–41 (1972). https://doi.org/10.1007/BF00306886

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  • DOI: https://doi.org/10.1007/BF00306886

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