Summary
This study describes the effects of acute X-irradiation of the ovaries upon the structure of primordial follicles in mature rhesus monkeys. Doses of 1000 r to 12000 r, and post-irradiation intervals of 7 hours to 30 days were used. Oocytes in biopsies from irradiated ovaries were compared with those removed from the same ovaries prior to treatment or from contra-lateral controls. The results of the treatment were assessed using light and electron microscopy.
The fine structural features of normal primordial oocytes are described, with particular reference to mitochondria and dense granular bodies. Some observations on spontaneous degenerative changes are included.
Irradiated ovaries are classified into four arbitrary groups according to the severity of cellular damage visible in primordial follicles with the light microscope. Effects are more marked following higher doses and/or longer intervals; the most obvious changes are pyknosis of nuclei and accumulation of dense granules in the follicle cell cytoplasm. Early changes in oocytes are relatively difficult to detect, but lead to clumping of cytoplasmic and nuclear contents at more advanced stages of degeneration. Alterations in oocyte fine structure consist mainly in swelling and disruption of membrane-bound organelles, and condensation of nuclear and nucleolar chromatin. They thus resemble those occurring during spontaneous atresia, although the damage to follicle cells is evident much sooner after irradiation.
These findings are compared with those made for species in which primordial follicles are known to be destroyed by much lower doses of X-rays than were used here. The contribution to the radiation-response made by the relative radiosensitivities of oocytes and follicle cells in different species is discussed.
Similar content being viewed by others
References
Adams, A. E., Hertig, A. T.: Studies on guinea pig oocytes I: Electron microscopic observations on the development of cytoplasmic organelles in oocytes of primordial and primary follicles. J. Cell Biol. 21, 397–427 (1964).
Baker, T. G.: A quantitative and cytological study of germ cells in human ovaries. Proc. roy. Soc. B 158, 417–433 (1963).
Baker, T. G.: The sensitivity of oocytes in post-natal rhesus monkeys to X-irradiation. J. Reprod. Fertil. 12, 183–192 (1966).
Baker, T. G.: Comparative aspects of the effects of radiation during oogenesis. Mutation Res. 11, 9–22 (1971a).
Baker, T. G.: Electron microscopy of the primary and secondary oocytes. In: Advances in the biosciences, vol. 6, p. 7–27 (Raspé, G., ed.). Oxford and Braunschweig: Pergamon Press-Vieweg, 1971b.
Baker, T. G.: The radiosensitivity of mammalian oocytes with particular reference to the human female. Amer. J. Obstet. Gynec. 110, 746–776 (1971c).
Baker, T. G., Beaumont, H. M., Franchi, L. L.: The uptake of tritiated uridine and phenylalanine by the ovaries of rats and monkeys. J. Cell Sci. 4, 655–675 (1969).
Baker, T. G., Franchi, L. L.: The fine structure of oogonia and oocytes in human ovaries. J. Cell Sci. 2, 213–224 (1967a).
Baker, T. G., Franchi, L. L.: The structure of the chromosomes in human primordial oocytes. Chromosoma (Berl.) 22, 358–377 (1967b).
Baker, T. G., Franchi, L. L.: The origin of cytoplasmic inclusions from the nuclear envelope of mammalian oocytes. Z. Zellforsch. 93, 45–55 (1969).
Baker, T. G., Franchi, L. L.: The fine structure of oogonia and oocytes in the rhesus monkey (Macaca mulatta). Z. Zellforsch. 126, 53–74 (1972).
Baker, T. G., Kelly, W. A., Marston, J. H.: The reproductive capacity of Rhesus monkeys following X-irradiation of the ovaries. Strahlentherapie 138, 355–360 (1969).
Blanchette, E. J.: A study of the fine structure of the rabbit primary oocyte. J. Ultrastruct. Res. 5, 349–363 (1961).
Bojadjieva-Mihailova, A.: Electron microscopical studies of the ovaries of embryos and newborn white mice under the influence of roentgen rays. Izv. Inst. Morfol. Sofiya 9–10, 161–165 (1964). Cited in: Excerpta Med. part II 1965, Abstr. 3650, p. 716.
Bojadjieva-Mihailova, A., Boneva, L., Hadjioloff, A.: Application of the mathematical-statistical method for the evaluation of the ultrastructural dimensions of ovocytic mitochondria after X-ray irradiation. Proc. 4th European Regional Conf. Electron Microscopy, Vol. 1, 605–606, Rome, 1968 (Bocciarelli, D. S., ed.) (1968).
Eck-Vermande, G. J. van: Neo-ovogenesis in the adult monkey. Consequences of atresia of ovocytes. Anat. Rec. 125, 207–224 (1956).
Eck-Vermande, G. J. van: Effect of low-dosage X-irradiation upon pituitary gland and ovaries of the rhesus monkey. Fert. and Steril. 10, 190–202 (1959).
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).
Franchi, L. L., Mandl, A. M.: The ultrastructure of germ cells in foetal and neonatal male rats. J. Embryol. exp. Morph. 12, 289–308 (1964).
Franchi, L. L., Mandl, A. M.: The ultrastructure of male germ cells in rats X-irradiated at birth. Proc. roy. Soc. B 165, 136–154 (1966).
Hollaender, A., Stapleton, G. E.: Ionizing radiation and the cell. Sci. Amer. 201, 3, 94–100 (1959).
Hope, J.: The fine structure of the developing follicle of the rhesus ovary. J. Ultrastruct. Res. 12, 592–610 (1965).
Hugon, J., Borgers, M.: Ultrastructural and cytochemical studies on karyolytic bodies in the epithelium of the duodenal crypts of whole-body irradiated mice. Lab. Invest. 15, 1528–1543 (1966a).
Hugon, J., Borgers, M.: Ultrastructural and cytochemical changes in spermatogonia and Sertoli cells of whole-body irradiated mice. Anat. Rec. 155, 15–32 (1966b).
Hugon, J., Borgers, M.: Fine structural changes and localization of phosphatases in the epithelium of the duodenal crypt of X-irradiated mice. Histochemie 6, 209–225 (1966c).
Ioannou, J. M.: Radiosensitivity of oocytes in post-natal guinea-pigs. J. Reprod. Fertil. 18, 287–295 (1969).
Mandl, A. M.: A quantitative study of the sensitivity of oocytes to X-irradiation. Proc. roy. Soc. B 150, 53–71 (1959).
Mandl, A. M.: The radiosensitivity of germ cells. Biol. Rev. 39, 288–371 (1964).
Oakberg, E. F., Clark, E.: Species comparisons of radiation response of the gonads. In: Effects of ionizing radiations on the reproductive system, p. 11–24 (Carlson, W. D. and Gassner, F. X., eds.). New York: Pergamon Press 1964.
Parkin, P.: The effects of X-irradiation on primordial oocytes in the rat. B. Sc. Thesis, Anatomy, University of Birmingham (1970).
Parsons, D. F.: An electron microscope study of radiation damage in the mouse oocyte. J. Cell Biol. 14, 31–48 (1962).
Puck, T. T.: Radiation and the human cell. Sci. Amer. 202, 4, 142–153 (1960).
Reifferscheid, K.: Histologische Untersuchungen über die Beeinflussung menschlicher und tierischer Ovarien durch Röntgenstrahlen. Z. Röntgenol. 12, 233–254 (1910).
Reifferscheid, K.: Die Einwirkung der Röntgenstrahlen auf tierische und menschliche Eierstöcke. Strahlentherapie 5, 407–426 (1914).
Wolff, S.: Mechanism of dose-rate effect; insights obtained from intensity and fractionation studies on chromosome aberration induction. Jap. J. Genet. 40, 38–48 (1965).
Author information
Authors and Affiliations
Additional information
This study was supported by grants to Lord Zuckerman, O. M., K. C. B., F. R. S., by the Medical Research Council and the Ford Foundation, and to Dr. H. M. Beaumont by the U. S. Atomic Energy Commission (Contract no. AT (30-1) 3846). We are indebted to the Medical Research Council for the provision of the electron microscopes and to the Nuffield Foundation for the X-ray apparatus. Our thanks are due to Dr. H. M. Beaumont for her advice during the preparation of the manuscript.
Rights and permissions
About this article
Cite this article
Baker, T.G., Franchi, L.L. Electron microscope studies of radiation-induced degeneration in oocytes of the sexually mature rhesus monkey. Z.Zellforsch 133, 435–454 (1972). https://doi.org/10.1007/BF00307127
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00307127