Ultrastructural changes in ovarian oocytes induced by exposure to ionizing radiations

  • Terry G. Baker
  • Leslie L. Franchi
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 2)


The transmission electron microscope has proved to be a most useful tool to the biologist and over the past twenty five years it has been used to explore the fine structure of a wide variety of cellular types and their organelles. The internal anatomy of the cell varies with function and characteristic changes are detectable by microscopy when its physiology and biochemistry become altered. It is therefore surprising that there have been few studies concerned with the ultrastructure of radiation damage, since this results from changes in cellular biochemistry (1–3). It will be shown in this chapter, however, that electron microscopy has provided little meaningful information about either the nature of the primary lesion or the sequence of events leading to radiation-induced cell death. It can be argued that a major reason for the paucity of such studies is the very complexity of the problem itself. Radiation biology is a complex interdisciplinary subject bridging large areas of physics, chemistry, biology and medicine. As a subject it is thwart with difficulties owing to the diversity of cell types and of processes of differentiation.


Germ Cell Granulosa Cell Follicle Cell Primordial Follicle Primordial Germ Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Lawrence CW: Cellular radiobiology. Institute of Biology Series, Studies in Biology 30, London, Arnold, 1971.Google Scholar
  2. 2.
    Puck TT: Radiation and the human cell. Sci Am 202: 142–153, 1960.PubMedCrossRefGoogle Scholar
  3. 3.
    Alper T: Cellular radiobiology, Cambridge, Cambridge University Press, 1979.Google Scholar
  4. 4.
    Baker TG: Comparative aspects of the effects of radiation during oogenesis. Mutat Res 11: pp 9–22, 1971.PubMedCrossRefGoogle Scholar
  5. 5.
    Baker TG: Radiosensitivity of mammalian oocytes with particular reference to the human female. Am J Obstet Gynecol 110: 746–761, 1971.PubMedGoogle Scholar
  6. 6.
    Baker TG, Neal P: Action of ionizing radiations on the mammalian ovary. In: The Ovary. Zuckerman S, Weir BJ (eds), New York, Academic Press, 1977 (2nd Edn) Vol. Ill, pp 1–58.Google Scholar
  7. 7.
    Mandl AM: The radiosensitivity of germ cells. Biol Rev Cambridge Philos Soc 39: 288–371, 1964.PubMedCrossRefGoogle Scholar
  8. 8.
    Franchi LL, Mandl AM, Zuckerman S: The development of the ovary and the process of oogenesis. In: The Ovary. Zuckerman S, Mandl AM, Eckstein P (eds), New York, Eckstein P (eds), 1962, Vol. I, pp 1–88.Google Scholar
  9. 9.
    Baker TG: Oogenesis and ovarian development. In: Reproductive Biology. Balin H, Glasser S (eds), Amsterdam, Excerpta Medica, 1972, pp 398–437.Google Scholar
  10. 10.
    Zuckerman S, Baker TG: The development of the ovary and the process of oogenesis. In: The Ovary. Zuckerman S, Weir BJ (eds), New York, Academic Press (2nd edn), 1977, Vol. I, pp 41–67.Google Scholar
  11. 11.
    Baker TG, McLaren A: The effect of tritiated thymidine on the developing oocytes of mice. J Reprod Fertil 34: 121–130, 1973.PubMedCrossRefGoogle Scholar
  12. 12.
    Heath JK: Mammalian primordial germ cells. In: Development in Mammals 3: Johnson MH (ed), Amsterdam, Elsevier/North Holland, 1978, pp 267–298.Google Scholar
  13. 13.
    Witschi E: Migration of the germ cells of human embryos from the yolk sac to the primitive gonadal folds. Contr Embryol Carneg Instn 32: 67–80, 1948.Google Scholar
  14. 14.
    Hardisty MW: The numbers of vertebrate primordial germ cells. Biol Rev Cambridge Philos Soc 42: 265–287, 1967.PubMedCrossRefGoogle Scholar
  15. 15.
    Baker TG: A quantitative and cytological study of germ cells in human ovaries. Proc R Soc London, Ser B 158: 417–433, 1963.Google Scholar
  16. 16.
    Jones EC, Krohn PL: The relationship between age and numbers of oocytes and fertility in virgin and multiparous mice. J Endocr 21: 469–495, 1961.PubMedCrossRefGoogle Scholar
  17. 17.
    Beaumont HM, Mandl AM: A quantitative and cytological study of oogonia and oocytes in the foetal and neonatal rat. Proc R Soc London, Ser B 155: 557–579, 1965.Google Scholar
  18. 18.
    Baker TG: A quantitative and cytological study of oogenesis in the rhesus monkey. J Anat 100: 761–776, 1966.PubMedGoogle Scholar
  19. 19.
    Baker TG, O W-S: Development of the ovary and oogenesis. In: Clinics in Obstetrics and Gynaecology 3(1). MacNaughton MC, Govan ADT (eds), London, Saunders, 1976, pp 3–26.Google Scholar
  20. 20.
    Ingram DL: Atresia. In: The Ovary. Zuckerman S, Mandl AM, Eckstein P (eds). New York, Eckstein P (eds). 1962, Vol I, pp 247–273.Google Scholar
  21. 21.
    Beaumont HM: Effect of hormone environment on the radiosensitivity of oocytes. In: Radiation biology of the fetal and juvenile mammal. Sikov MR, Mahlum DD (eds), CONF-690501, Washington DC, US Atomic Energy Comm, 1969, pp 557–579.Google Scholar
  22. 22.
    Byskov A-G: Atresia. In: Ovarian follicular development and function. Midgley AR, Sadler WA (eds), New York, Raven Press, 1979, pp 41–57.Google Scholar
  23. 23.
    Hay MF, Cran DG, Moor RM: Structural changes occurring during atresia in sheep ovarian follicles. Cell Tiss Res 169: 515–529, 1976.CrossRefGoogle Scholar
  24. 24.
    Baker TG, Franchi LL; Electron microscope studies of radiation- induced degeneration in oocytes of the sexually mature rhesus monkey. Z Zellforsch Mikrosk Anat 133: 435–454, 1972.PubMedCrossRefGoogle Scholar
  25. 25.
    Baker TG, Franchi LL: The fine structure of oogonia and oocytes in human ovaries. J Cell Sci 2: 213–224, 1967.PubMedGoogle Scholar
  26. 26.
    Beaumont HM: The short-term effects of acute X-irradiation on oogonia and oocytes. Proc R Soc London, Ser B 161: 550–570, 1965.Google Scholar
  27. 27.
    Beaumont HM: The effects of acute X-irradiation on primordial germ cells in the female rat. Int J Radiat Biol 10: 17–28, 1966.CrossRefGoogle Scholar
  28. 28.
    Mintz B: Continuity of the female germ cell line from embryo to adult. Arch Anat micr Morph exp 48: 155–172, 1959.PubMedGoogle Scholar
  29. 29.
    Beaumont HM: The radiosensitivity of germ cells at various stages of ovarian development. Int J Radiat Biol 4: 581–590, 1962.PubMedCrossRefGoogle Scholar
  30. 30.
    Baker TG, Beaumont HM: Radiosensitivity of oogonia and oocytes in the foetal and neonatal monkey. Nature (London) 214: 981–982, 1967.CrossRefGoogle Scholar
  31. 31.
    Gondos B, Hobel CJ: Germ cell degeneration and phagocytosis in the human foetal ovary. In: The development and maturation of the ovary and its functions. Peters H (ed), Amsterdam, Excerpta Medica, 1973, pp 77–83.Google Scholar
  32. 32.
    Franchi LL, Mandl AM: The ultrastructure of oogonia and oocytes in the foetal and neonatal rat. Proc R Soc London, Ser B 157: 99–114, 1962.Google Scholar
  33. 33.
    Franchi LL, Baker TG: Oogenesis and follicular growth. In: Human reproduction, Hafez ESE (ed), Hagerstown, Harper and Row, 1980 (2nd edn) pp 149–177.Google Scholar
  34. 34.
    O W-S: The interaction between the germinal and somatic cells in gonadal differentiation and development. In: Development in mammals 3. Johnson MH (ed), Amsterdam, Elsevier/North Holland, 1978, pp 299–322.Google Scholar
  35. 35.
    Norrevang A: Electron microscopic morphology of oogenesis. Int Rev Cytol 23: 114–486, 1968.Google Scholar
  36. 36.
    Zamboni L: Modulations of follicle cell-oocyte association in sequential stages of mammalian follicle development and maturation. In: Ovulation in the human. Crosignani PG, Mishell DR (eds), New York, Academic Press, 1976, pp 1–30.Google Scholar
  37. 37.
    Motta P, Hafez ESE (eds): Biology of the ovary; Developments in Obstetrics and Gynecology 2. The Hague, Martinus Nijhoff, 1980.Google Scholar
  38. 38.
    Anderson E: Follicular morphology. In: Ovarian follicular development and function. Midgley AR, Sadler WA (eds), New York, Raven Press, 1979, pp 91–105.Google Scholar
  39. 39.
    Edwards RG: Early human development: from the oocyte to implantation. In: Scientific foundations of obstetrics and gynaecology. Philipp EE, Barnes J, Newton M (eds), London, Wm Heinemann Medical Books, 2nd Edn 1977, pp 175–252.Google Scholar
  40. 40.
    Baker TG: The sensitivity of oocytes in postnatal rhesus monkey to X-irradiation. J Reprod Fertil 12: 183–192, 1966.PubMedCrossRefGoogle Scholar
  41. 41.
    Murray JM: A study of the histological structure of mouse ovaries following exposure to roentgen irradiation. Amer J Roentgenol 25: 1–45, 1931.Google Scholar
  42. 42.
    Lacassagne A: Etude histologique et physiologique des effects produits sur Tovaire par less rayons X. These Medecine, Lyon, 1913.Google Scholar
  43. 43.
    Lacassagne A, Duplan JF, Marcovich H, Raynaud A: The action of ionizing radiations on the mammalian ovary. In: The Ovary. Zuckerman S, Mandl AM, Eckstein P (eds), New York, Eckstein P (eds), 1962, Vol. II, pp 463–532.Google Scholar
  44. 44.
    Mandl AM: A quantitative study of the sensitivity of oocytes to X-irradiation. Proc R Soc London Ser B 150: 53–71, 1959.CrossRefGoogle Scholar
  45. 45.
    Ioannou JM: Radiosensitivity of oocytes in post-natal guinea-pigs. J Reprod Fertil 18: 287–295, 1969.PubMedCrossRefGoogle Scholar
  46. 46.
    Genther IT: Irradiation of the ovaries of guinea-pigs and its effects on the oestrous cycle. Am J Anat 48: 99–137, 1931.CrossRefGoogle Scholar
  47. 47.
    Van Eck GJV: Neo-ovogenesis in the adult monkey. Consequences of atresia of oocytes. Anat Ree 125: 207–224, 1956.CrossRefGoogle Scholar
  48. 48.
    Oakberg EF, Clark E: Species comparisons of radiation response of the gonads. In: Effects of ionizing radiation on the reproductive system. Carlson WD, Gassner FX (eds), Oxford, Pergamon, 1964, pp 11–24.Google Scholar
  49. 49.
    Hill RL: Ovarian changes induced by exogenous gonadotrophins and X-irradiation. PhD Thesis, University of Birmingham, Birmingham, UK, 1971.Google Scholar
  50. 50.
    Peters H, Borum K: The development of mouse ovaries after low-dose irradiation at birth. Int J Radiat Biol 3: 1–16, 1961.PubMedCrossRefGoogle Scholar
  51. 51.
    Parkin PA: The effects of X-irradiation on primordial oocytes in the rat BSc Thesis, University of Birmingham, Birmingham, UK, 1970.Google Scholar
  52. 52.
    Parsons DF: An electron microscope study of radiation damage in the mouse oocyte. J Cell Biol 14: 31–48, 1962.PubMedCrossRefGoogle Scholar
  53. 53.
    Ioannou JM: Oogenesis in the guinea-pig. J Embryol exp Morph 12: 673–691, 1964.PubMedGoogle Scholar
  54. 54.
    Smith LH, Congdon CC: Biological effects of ionizing radiation. In: Human transplantation. Rapaport FT, Dausset J (eds), New York, Grune and Stratton, 1968, pp 510–525.Google Scholar
  55. 55.
    Casare« GW: Radiation histopathology, Vols I and II, Boca Raton, CRC Press, 1980.Google Scholar
  56. 56.
    Alexander P, Dean CJ, Hamilton LDG, Lett JT, Parkins G: Critical structures other than DNA as sites for primary lesions of cell death induced by ionizing radiations. In: Cellular radiation biology. (18th Symp. fundamental cancer research), Baltimore, Williams and Wilkins, 1965, pp 241–263.Google Scholar
  57. 57.
    Crone M: Radiation stimulated incorporation of (3H) thymidine into diplotene oocytes of the guinea-pig. Nature (London) 228: 460, 1970.CrossRefGoogle Scholar
  58. 58.
    Masui Y, Pederson RA: Ultraviolet light-induced unscheduled DNA synthesis in mouse oocytes during meiotic maturation. Nature (London) 257: 705–706, 1975.CrossRefGoogle Scholar
  59. 59.
    Kofman-Alfaro S, Chandley AC: Radiation induced DNA synthesis in spermatogenic cells of the mouse. Exp Cell Res 69: 33–34, 1971.PubMedCrossRefGoogle Scholar
  60. 60.
    Sega GA, Sotomayor RE, Owens JG: A study of unscheduled DNA synthesis induced by X-rays in the germ cells of male mice. Mutat Res 49: 239–257, 1978.PubMedCrossRefGoogle Scholar
  61. 61.
    Wartenberg H, Stegner H-E: Uber die elektronenmikroskopische Feinstruktur des menschlichen Ovarialeies. Z Zellforsch Mikrosk Anat 52: 450–474, 1960.PubMedCrossRefGoogle Scholar
  62. 62.
    Wischnitzer S: Intramitochondrial transformations during oocyte maturation in the mouse. J Morph 121: 29–46, 1967.PubMedCrossRefGoogle Scholar
  63. 63.
    Weakley BS: A comparison of three different electron microscopical grades of glutaraldehydes used to fix ovarian tissue. J Microsc (OXF) 101: 127–141, 1974.CrossRefGoogle Scholar
  64. 64.
    Iqbal SJ, Weakley BS: The effects of different preparative procedures on the ultrastructure of the hamster ovary. I. effects of various fixative solutions on ovarian oocytes and their granulosa cells. Histochemistry 38: 95–122, 1974.PubMedCrossRefGoogle Scholar
  65. 65.
    Baker TG, Beaumont HM, Franchi LL: The uptake of tritiated uridine and phenylalanine by the ovaries of rats and monkeys. J Cell Sci 4: 655–675, 1969.PubMedGoogle Scholar
  66. 66.
    Chouinard LA: A light and electron microscope study of the nucleolus during growth of the oocyte in the prepubertal mouse. J Cell Sci 9: 637–663, 1971.PubMedGoogle Scholar
  67. 67.
    Palombi F, Stefanini M: Ultrastructural analysis of nucleolar evolution in the rat primary oocyte. J Ultrastruct Res 47: 61–73, 1974.PubMedCrossRefGoogle Scholar
  68. 68.
    Bojadjieva-Mihailova A: Electron microscopical studies of the ovaries of embryos and newborn white mice under the influence of roentgen rays. Izv Inst Morfol Bulg Akad Nauk 9–10, 161–165, 1964. Abstracted in Excerpta Medica Sect 14, Vol 19, Abst No. 2511, 1965.Google Scholar
  69. 69.
    Bojadjieva-Mihailova A, Boneva L, Hadjioloff D: Application of the mathemtical-statistical method for the evaluation of the ultrastructural dimensions of ovocytic mitochondria after X-ray irradiation. In: Proc European Reg Conf Electron Microsc 4th. Bocciarelli DS (ed), Rome, Vol. I, 1968, pp 605–606.Google Scholar
  70. 70.
    Jostes E, Scherer E: Beitrag zur Morphologie röntgen-und radiumbe-strahlter Mauseovarien. I. Mitteilung: Die Eizelle. Strahlentherapie 115: 337–365, 1961.PubMedGoogle Scholar
  71. 71.
    Jostes E, Scherer E: Beitrag zur Morphologie röntgen-und radiumbe-strahlter Mauseovarien. II. Mitteilung: Beobachtungen an Follikel-Theca-und Luteinzellen. Strahlentherapie 132: 59–78, 1967.PubMedGoogle Scholar
  72. 72.
    Matsumoto A: Behaviour of irradiated ovaries after intrasplenic transplantation in castrated rats. Ann Zool Japon 46: 165–172, 1973.Google Scholar
  73. 73.
    Pease DC: Histological techniques for electron microscopy. New York, Academic Press, 2nd edn, 1964.Google Scholar
  74. 74.
    Matsumoto A: Changes in ultrastructure of rat ovaries after early postnatal X-ray irradiation. Endocrinol Japon 22: 1–15, 1975.CrossRefGoogle Scholar
  75. 75.
    Sotelo JR, Porter KR: An electron microscope study of the rat ovum. J Biophys Biochem Cytol 5: 327–342, 1959.PubMedCrossRefGoogle Scholar
  76. 76.
    Odor DL: Electron microscopic studies on ovarian oocytes and un-fertilized tubal ova in the rat. J Biophys Biochem Cytol 7: 567–574, 1960.PubMedCrossRefGoogle Scholar
  77. 77.
    Odor DL: The ultrastructure of unilaminar follicles of the hamster ovary. Am J Anat 116: 493–522, 1965.PubMedCrossRefGoogle Scholar
  78. 78.
    Gondos B: Cell degeneration: light and electron microscopic study of ovarian germ cells. Acta Cytol 18: 504–509, 1974.PubMedGoogle Scholar
  79. 79.
    Odor DL, Blandau RJ: Ultrastructural observations on atresia in whole organ cultures of foetal mouse ovaries. In: The development and maturation of the ovary and its functions. Peters H (ed), Amsterdam, Excepta Medica, 1973, pp 63–76.Google Scholar
  80. 80.
    Bonilla-Musoles F, Renau J, Hernandez-Yago J, Torres J: How do oocytes disappear? Arch Gynak 218: 233–241, 1975.CrossRefGoogle Scholar
  81. 81.
    Van Blerkom J, Motta P: The cellular basis of mammalian reproduction. Baltimore, Urban and Schwarzenberg, 1979.Google Scholar
  82. 82.
    Tesarik J, Dvorak M: Human cumulus oophorus preovulatory development. J Ultrastruct Res 78: 60–72, 1982.PubMedCrossRefGoogle Scholar
  83. 83.
    Vasquez-Nin GH, Sotelo JR: Electron microscope study of the atretic oocytes of the rat. Z Zellforsch Mikrosk Anat 80: 518–533, 1967.CrossRefGoogle Scholar
  84. 84.
    Baker TG, Franchi LL: The origin of cytoplasmic inclusions from the nuclear envelope of mammalian oocytes. Z Zellforsch Mikrosk Anat 92: 45–55, 1969.Google Scholar
  85. 85.
    Ulrich M: Abtotung von Drosophila-Eiern verschiedenen Alters durch partielle Röntgenbestrahlung. Naturwissenschaften 38: 530–543, 1951.CrossRefGoogle Scholar
  86. 86.
    von Borstel RC, Rogers RW: Alpha-particle bombardment of the Habrobacon egg, II. Response of the cytoplasm. Radiation Res 8: 248, 1958.CrossRefGoogle Scholar
  87. 87.
    Boyadjieva-Mihailova A, Bakalska-Nesheva M, Kancheva L, Anastosova-Kristeva M: Ultrastructural changes in chick ovaries after X-ray irradiation. Arkh anat Gistol Embriol 73: 42–46, 1977. Abstracted in Biol Absts 65: No 24045, 1978.Google Scholar
  88. 88.
    Baker TG, Franchi LL: The structure of the chromosomes in human primordial oocytes. Chromosoma 22: 358–377, 1967.PubMedCrossRefGoogle Scholar
  89. 89.
    Miller OL, Carrier RF, von Borstel RC: In situ and in vivo breakage of lampbrush chromosomes by X-irradiation. Nature (London) 206: 905, 1965.CrossRefGoogle Scholar
  90. 90.
    Weibel ER: Stereological methods, Vol I: Practical methods for biological morphometry. New York, Academic Press, 1979.Google Scholar
  91. 91.
    Moore GPM, Lintern-Moore S, Peters H, Faber M: RNA synthesis in the mouse oocyte, J Cell Biol 60: 416–422, 1974.PubMedCrossRefGoogle Scholar
  92. 92.
    Wolgemuth DJ, Jagiello GM, Henderson AS: Quantitation of ribosomal RNA genes in fetal human oocyte nuclei using rRNA hybridization in situ: Evidence for increased mutiplicity. Expl Cell Res 118: 181–190, 1979.CrossRefGoogle Scholar
  93. 93.
    Mangia F, Canipari R: Biochemistry of growth and maturation in mammalian oocytes. In: Development in mammals 2. Johnson MH (ed), Amsterdam, Elsevier/North Holland, 1977, pp 1–29.Google Scholar
  94. 94.
    Miller OL Jr, Bakken A: Morphological studies of transcription. Acta Endocrinol 168 suppl: 155–177, 1973.Google Scholar
  95. 95.
    Kierszenbaum AL, Tres L: Transcription sites in spread meiotic prophase chromosomes from mouse spermatocytes. J Cell Biol 63: 923–935, 1974.PubMedCrossRefGoogle Scholar

Copyright information

© Martinus Nijhoff Publishers, Boston, The Hague, Dordrecht, Lancaster 1984

Authors and Affiliations

  • Terry G. Baker
    • 1
  • Leslie L. Franchi
    • 2
  1. 1.School of Medical SciencesUniversity of BradfordBradfordUK
  2. 2.Department of AnatomyUniversity of BirminghamBirminghamUK

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