Summary
The structural changes that characterize primary, secondary and tertiary atresia in sheep Graafian follicles have been studied by means of histological, histochemical and ultrastructural techniques.
In primary atresia vacuoles representing swollen endoplasmic reticulum are prominent along the antral border together with disorganized granulosa cells containing pyknotic nuclei. Phagocytic cells, which increase in number as atresia progresses, were seen within the membrana granulosa and are considered to be transformed granulosa cells. Even in follicles classified as nonatretic, a few antral vacuoles and occasional pyknotic nuclei are present.
During secondary atresia there is a large increase in the number of cells with pyknotic nuclei; many of these nuclei had been extruded and had fused to form the characteristic Feulgen-positive atretic bodies found along the edge of the antral cavity. These bodies usually have a diameter of up to 15 μm but occasionally reached as much as 400 μm. A second area of degeneration is frequently present in the membrana granulosa, two or three cell layers from the basal lamina, and it is at this level that exfoliation of granulosa cells occurs in tertiary atresia. In contrast to the membrana granulosa, there are during secondary atresia, only slight indications of degeneration in the cumulus.
In tertiary atresia the membrana granulosa is highly disorganized; the atretic bodies are often fewer in number than at earlier stages. The basal lamina remains essentially intact. It is at this stage that the first clear signs of degeneration occur in the theca interna. Despite some disintegration of the cumulus, the integrity of the oocyte is maintained and its nucleus remains vesicular.
Changes in the thecal microcirculation may play a key role in atresia: adjacent to the basal lamina of non-atretic follicles, there is a well-developed capillary network which is significantly reduced as atresia progresses.
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References
Antonucci, R.: L'Irrorazione del follicolo ooforo dell'ovario di alcuni mammiferi. Acta med. Vet. Napoli 18, 201–211 (1972)
Baillie, A.H., Ferguson, M.M., Hart, D. McK.: Developments in steroid histochemistry. London and New York: Academic Press 1966
Bjersing, L., Hay, M.F., Kann, G., Moor, R.M., Naftolin, F., Scaramuzzi, R.J., Short, R.V., Younglai, E.V.: Changes in gonadotrophins, ovarian steroids and follicular morphology in sheep at oestrus. J. Endocr. 52, 465–479 (1972)
Bloom, W., Fawcett, D.W.: A text-book of histology, 9th ed. Philadelphia: Saunders 1968
Brand, A., de Jong, W.H.R.: Qualitative and quantitative micromorphological investigations of the tertiary follicle population during the oestrous cycle in sheep. J. Reprod. Fertil. 33, 431–439 (1973)
Bruce, N.W., Moor, R.M.: Capillary blood flow to ovarian follicles, stroma and corpora lutea of anaesthetized sheep. J. Reprod. Fertil. 46, 299–304 (1976)
Burkl, W.: Zur kausalen Genese der Follikelatresie. Arch. Gynäk. 200, 689–698 (1965)
Burkl, W., Ratzenböck, W.: Über feulgenpositive Einschlüsse im Liquor folliculi atresierender Tertiärfollikel bei der Ratte. Acta histochem. (Jena) 16, 290–301 (1963)
Byskov, A.G.S.: Cell kinetic studies of follicular atresia in the mouse ovary. J. Reprod. Fertil. 37, 277–285 (1974)
Call, E.L., Exner, S.B.: Zur Kenntnis des Graafschen Follikels und der Corpus luteum beim Kaninchen. S.-B. Akad. Wiss. Wien 71, 321–328 (1875)
Chayen, J., Bitensky, L., Butcher, R.G., Poulter, L.W.: A guide to practical histochemistry. Edinburgh: Oliver & Boyd 1969
Corteel, M.: Étude histologique de la transformation du follicle préovulatoire en corps jaune cyclique chez la Brebis. I. Évolution des ultrastructures des cellules de la granulosa. Ann. Biol. anim. Biochim. Biophys. 13, 249–260 (1973)
Farquhar, M.G., Palade, G.E.: Cell junctions in amphibian skin. J. Cell Biol. 26, 263–291 (1965)
Hay, M.F., Moor, R.M.: Distribution of Δ5-3β-hydroxysteroid dehydrogenase activity in the Graafian follicle of the sheep. J. Reprod. Fertil. 43, 313–322 (1975a)
Hay, M.F., Moor, R.M.: Functional and structural relationships in the Graafian follicle population of the sheep ovary. J. Reprod. Fertil. 45, 583–593 (1975b)
Ingram, D.L.: Atresia. In: The ovary, Vol. 1 (ed. S. Zuckerman), pp. 247–273. New York and London: Academic Press 1962
Jones, E.C.: Atresia in the ovaries of vertebrates. Bibliogr. Reprod. 15, 129–132, 245–247 (1970)
Lendrum, A.C., Fraser, D.S., Slidders, W., Henderson, R.: Studies on the character and staining of fibrin. J. clin. Path. 15, 401–413 (1962)
Moor, R.M., Hay, M.F., McIntosh, J.E.A., Caldwell, B.V.: Effect of gonadotrophins on the production of steroids by sheep ovarian follicles cultured in vitro. J. Endocr. 58, 599–611 (1973)
Pederson, T.: Follicle kinetics in the ovary of the cyclic mouse. Acta endocr. (Kbh.) 64, 304–323 (1970)
Rajakoski, E.: The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical and left-right variations. Acta endocr. (Kbh.), Suppl. 52, 1–68 (1960)
Turnbull, K.E., Braden, A.W.H.: The pattern of follicular growth and atresia in the ovine ovary. Aust. J. biol. Sci., in press (1976)
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The authors are greatly indebted to Dr. H.M. Dott and Mr. G.C. Foster for carrying out the analysis with the Quantimet image analysing computer. The skilled technical assistance of Mrs. Linda Collins is also gratefully acknowledged
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Hay, M.F., Cran, D.G. & Moor, R.M. Structural changes occurring during atresia in sheep ovarian follicles. Cell Tissue Res. 169, 515–529 (1976). https://doi.org/10.1007/BF00218150
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DOI: https://doi.org/10.1007/BF00218150