Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Ultrastructural alterations associated with the initiation of follicular atresia

  • 30 Accesses

  • 20 Citations


To identify and describe ovarian follicles committed to undergo follicular degeneration (atresia), immature rats were primed with pregnant mare serum gonadotropin (PMSG). After PMSG treatment, preovulatory follicles develop but subsequently degenerate. Prior to the appearance of pyknotic nuclei (Stage I of atresia), degenerative changes were observed in focal areas of the granulosa cell layer. These changes include “blebbing” of the cytoplasm and alterations in the shape of the granulosa cells. The appearance of these degenerative changes coincides with a decrease in ovarian concentrations of estradiol and testosterone. Since estrogens and androgens maintain the follicle, the decline in estradiol and testosterone could be responsible for the further degenerative alterations that lead to complete deterioration of the preovulatory follicle. In Stage I atretic follicles, lysosome-derived autophagic vacuoles develop and macrophages invade both the thecal and granulosa cell layers. The combined actions of the autophagic vacuoles and macrophages could destroy both the granulosa-cell and thecal layers and thereby transform the preovulatory follicle into an ovarian cyst.

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


  1. Armstrong DT, Goff AK, Dorrington JH (1979) Regulation of follicular estrogen biosynthesis. In: Midgley AR, Sadler WA (eds) Ovarian follicular development and function. Raven Press, New York, pp 169–181

  2. Bukovsky A, Trebichavsky I, Presl J (1979) Lymphoid cells in the uterine cervix after electrocoagulation. J Reprod Med 23:42–45

  3. Byskov AGS (1974) Cell kinetic studies of follicular atresia in the mouse ovary. J Reprod Fertil 37:277–285

  4. Byskov AGS (1978) Follicular atresia. In: Jones RE (ed) The vertebrate ovary. Plenum Press, New York, pp 533–554

  5. Campbell CS, Schwartz NB, Firlit MG (1977) The role of adrenal and ovarian steroids in the control of serum LH and FSH. Endocrinology 101:162–172

  6. Drury RAB, Wallington EA (1967) Lipids. In: Carleton's histological technique (fourth edition). Oxford University Press, London, pp 291–304

  7. Dorrington JH (1977) Steroidogenesis in vitro. In: Zuckerman S, Weir BJ (eds) The ovary, Vol III. Academic Press, New York, pp 359–399

  8. Elfont EA, Roszka JP, Dimino MJ (1977) Cytochemical studies of acids phosphatase in ovarian follicles: a suggested role for lysosomes in Steroidogenesis. Biol Reprod 17:787–795

  9. Gay VL, Kerhand JT (1978) Serum LH and FSH following passive immunization against circulating testosterone in the intact male rat and in orchidectomized rats bearing subcutaneous silastic implants of testosterone. Arch Androl 1:239–247

  10. Gibori G, Antczak E, Rothschild I (1977) The role of estrogen in the regulation of luteal progesterone secretion in the rat after day 12 of pregnancy. Endocrinology 100:1438–1495

  11. Goldenberg RL, Vaitukaitis JL, Ross GT (1972) Estrogen and follicle stimulating hormone interactions of follicle growth in the rat. Endocrinology 90:1492–1498

  12. Guraya SS, Greenwald GS (1964) A comparative histochemical study of interstitial tissue and follicular atresia in the mammalian ovary. Anat Rec 149:411–434

  13. Hamberger L, Hamberger A, Herlitz H (1971) Methods for metabolic studies on isolated granulosa and theca cells. Acta Endocrinol (Suppl) 153:41–61

  14. Hay MF, Cran DG, Moor RM (1976) Structural changes occurring during atresia in sheep ovarian follicles. Cell Tissue Res 169:515–529

  15. Leonard EJ, Skeel AH (1980) Enhancement of spreading, phagocytosis and chemotaxis by macrophage stimulating protein (MSP). Adv Exp Med Biol 121B:181–194

  16. Merk FB, Botticelli CR, Albright JT (1972) An intercellular response to estrogen by granulosa cells in the rat ovary; an electron microscope study. Endocrinology 90:992–1007

  17. Mizcjewski GJ (1976) Studies of human chorionic gonadotropin in steroid-primed hypophysectomized rats. Acta Endocrinol 82:801–808

  18. Peluso JJ, Steger RW (1978) Role of FSH in regulating granulosa cell division and follicular atresia in rats. J Reprod Fertil 54:275–278

  19. Peluso JJ, Steger RW, Hafez E (1977a) Sequential changes associated with the degeneration of preovulatory rat follicles. J Reprod Fertil 49:215–218

  20. Peluso JJ, Steger RW, Hafez E (1977b) Surface ultrastructural changes in granulosa cells of atretic follicles. Biol Reprod 16:600–605

  21. Peluso JJ, Breitenecker G, Hafez E (1979a) Atresia of ovarian follicles and ova. In: Hafez E (ed) Human ovulation. Elsevier/North-Holland Biomedical Press, pp 177–204

  22. Peluso JJ, Brown I, Steger RW (1979b) Effects of cyproterone acetate, a potent antiandrogen, on the preovulatory follicle. Biol Reprod 21:929–936

  23. Peluso JJ, Stude D, Steger RW (1980) Role of androgens in hCG-induced ovulation in PMSG-primed immature rats. Acta Endocrinol 93:505–512

  24. Richards JS, Ireland JJ, Rao MC, Bernath GA, Midgley AR, Reichert LE (1976) Ovarian follicular development in the rat: hormone receptor regulation by estradiol, follicle-stimulating hormone and luteinizing hormone. Endocrinology 99:1562–1570

  25. Steger RW, Peluso JJ, Huang H, Meites J (1976) Gonadotropin-binding sites in the ovary of aged rats. J. Reprod Fertil 48:205–207

  26. Zeleznik AJ (1979) Regulation of pregnenolone metabolism in developing granulosa cells by follicle stimulating hormone. Biol Reprod (Suppl 1) 49a

Download references

Author information

Correspondence to Dr. J. J. Peluso.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Peluso, J.J., England-Charlesworth, C., Bolender, D.L. et al. Ultrastructural alterations associated with the initiation of follicular atresia. Cell Tissue Res. 211, 105–115 (1980). https://doi.org/10.1007/BF00233727

Download citation

Key words

  • Rat
  • Preovulatory follicle
  • Ultrastructure
  • Degeneration
  • Atresia