Summary
The follicular epithelial layers of the developing ovary of two cichlid species were examined by electron microscopy for evidence of steroid secretion. As each oocyte grew, its follicular cell layers increased in height, eventually becoming somewhat columnar; no development could be detected in follicle cells of non-activated oocytes. Isolated cells close to capillaries in the thecal layer developed large amounts of smooth membrane indicative of steroidogenesis, appearing similar at maturity to testicular Leydig cells. In Cichlasoma nigrofasciatum the mitochondria of differentiated thecal elements contained microtubule-like inclusions. It is suggested that these cells may produce estrogens during vitellogenesis.
In developing granulosa cells, active synthesis of granular endoplasmic reticulum occurred. This membrane appeared to arise from the nuclear envelope, and in the pre-ovulatory stage was always intermediate between smooth and granular forms, being only partly associated with ribosomes. Evidence for steroid biosynthesis in the granulosa at this time was therefore equivocal. Evidence was found of transfer of micropinocytotic vesicles from the granulosa cells into the ooplasm.
The fate of the post-ovulatory follicle was investigated in Cichlasoma. Thecal elements remained separate from granulosa and unchanged in ultrastructure for up to ten days. The granulosa cells proliferated and differentiated within a few hours after ovulation into a cell type containing much smooth reticulum, characteristic of steroidogenesis. However, after approximately three days numerous signs of degenerative processes became visible. The significance of the observed ultrastructural changes in relation to endocrine function is discussed.
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References
Bailey, R. E.: The effect of estradiol on serum calcium and protein in the goldfish. J. exp. Zool. 136, 455–469 (1957).
Bara, G.: Histochemical localization of δs-3 β-hydroxysteroid dehydrogenase in the ovaries of a teleost fish, Scomber scomber L. Gen. comp. Endocr. 5, 284–296 (1965).
Black, V. H., Christensen, A. K.: Differentiation of interstitial cells and Sertoli-cells in fetal guinea-pig testes. Amer. J. Anat. 124, 211–238 (1969).
Blanc-Livni, N., Abraham, A., Leray, C., Yachouv, A.: Histochemical localization of hydroxysteroid dehydrogenases in the ovary of a euryhaline teleost fish: Mugil capito. Gen. comp. Endocr. 13, 493 (1969).
Blum, V., Fiedler, K.: Hormonal control of reproductive behaviour in some cichlid fish. Gen. comp. Endocr. 5, 186–196 (1965).
Bretschneider, L. H., Duyvene-de-Wit, J. J.: Sexual endocrinology of non-mammalian vertebrates. Amsterdam: Elsevier 1947.
Christensen, A. K., Gillim, S. W.: The correlation of fine structure and function in steroidsecreting cells, with emphasis on those of the gonads. In: The gonads, ed. K. W. McKerns. New York: Appleton-Century-Crofts 1969.
Eckstein, B., Katz, Y.: Steroidgenesis in post- and pre-spawned ovaries of a cichlid fish, Tilapia aurea. Comp. Biochem. Physiol. 38A, 329–338 (1971).
Fawcett, D. W., Long, A. J., Jones, A. L.: The ultra-structure of endocrine glands. Rec. Progr. Hormone Res. 25 (1969).
Flügel, H.: Licht- und elektronenmikroskopische Untersuchungen an Oozyten und Eiern einiger Knochenfische. Z. Zellforsch. 83, 82–116 (1967).
Follenius, E.: Cytologie et cytophysiologie des cellules interstitielles de l'epinoche: Gasterosteus aculeatus L. Etude au microscope électronique. Gen. comp. Endocr. 11, 198–219 (1968).
Gottfried, H.: The occurrence and biological significance of steroids in lower vertebrates. Steroids 3, 219–242 (1964).
Hirsch, J. G., Fedorko, M. E.: Ultrastructure of human leucocytes after simultaneous fixation with glutaraldehyde and osmium tetroxide and “post-fixation” in uranyl acetate. J. Cell Biol. 38, 615–627 (1968).
Hoar, W. S.: Comparative physiology: Hormones and reproduction in fishes. Ann. Rev. Physiol. 27, 51–70 (1965).
— Reproduction: in Fish physiology (eds. W. S. Hoar and D. J. Randall), vol. III, p. 1–72. New York: Academic Press 1969.
Jollie, W. P., Jollie, L. G.: The fine structure of the ovarian follicle of the ovoviviparous poeciliid fish, Lebistes reticulatus. J. Mnrph. 114, 479–502 (1964).
Joly, M. J.: Mise en évidence histochimique d'une δs-3β-hydroxystéroide-deshydrogénase dans l'ovaire de l'urodele Salamandra salamandra (L) a différents stades du cycle sexuel. C. R. Acad. Sci. (Paris) 261, 1569–1571 (1965).
Kemp, N. E., Allen, M. D.: Electron microscopic observations on the development of the chorion of Fundulus. Biol. Bull 3, 293 (1956).
Kessel, R. G., Panje, W. R.: Organization and activity in the pre- and postovulatory follicle of Necturus maculosus. J. Cell Biol. 39, 1–34 (1968).
Lambert, J. G. D.: The ovary of the guppy Poecilia reticulata. The granulosa cells as sites of steroid biosynthesis. Gen. comp. Endocr. 15, 464–476 (1970a).
— The ovary of the guppy Poecilia reticulata. The atretic follicle, a corpus atreticum or a corpus luteum praeovulationis? Z. Zellforsch. 107, 54–67 (1970b).
Lehrman, D. S.: Interaction between external and internal environments in the regulation of the reproductive cycle of the ring-dove. In: Sex and behaviour (ed. F. A. Beach), p. 355–380. New York: Wiley 1965.
Noble, G. K., Kumpf, K. F., Billings, V. N.: The induction of brooding behaviour in the jewel fish. Endocrinology 23, 353–359 (1938).
Redshaw, M. R., Follett, B. K., Nicholls, T. J.: Comparative effects of the oestrogens and other steroid hormones on serum lipids and proteins in Xenopus laevis Daudin. J. Endocr. 43, 47–53 (1969).
Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).
Schjeide, O. A., Galey, F., Grellert, E. A., I-San Lin, R., Vellis, J. de, Mead, J. F.: Macromolecules in oocyte maturation. Biol. Reproduction, Suppl. 2, 14–43 (1970).
Takano, K.: On the egg formation and the follicular changes in Lebistes reticulatus. Bull. Fac. Fish. Hokkaido Univ. 15, 147–155 (1964).
Urist, M. R., Schjeide, O. A.: The partition of calcium and protein in the blood of oviparous vertebrates during estrus. J. gen. Physiol. 44, 743–756 (1961).
Wyburn, G. M., Johnson, H. S., Aitken, R. N. C.: Fate of the granulosa cells in the hen's follicle. Z. Zellforsch. 72, 53–65 (1965).
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Nicholls, T.J., Maple, G. Ultrastructural observations on possible sites of steroid biosynthesis in the ovarian follicular epithelium of two species of cichlid fish, Cichlasoma nigrofasciatum and Haplochromis multicolor . Z.Zellforsch 128, 317–355 (1972). https://doi.org/10.1007/BF00306973
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DOI: https://doi.org/10.1007/BF00306973