Summary
Structural and functional relationships between oocytes and their envelopes were studied by means of electron microscopy in several teleost species after injection of live fish with horseradish peroxidase. The marker first appeared in the capillaries and the pericapillary spaces of the ovarian stroma. It then entered the collagen-filled spaces between the granulosa and theca cells; these spaces are in direct connection with the pericapillary spaces. The marker penetrated between the follicle cells and into the channels of the zona radiata surrounding the microvilli which traverse these channels. The marker was never found inside the microvilli or in the follicle cells; finally, it reached the surface of the oocytes and was internalized via micropinocytosis. Six stages in the course of folliculogenesis were observed, determined by (1) the formation of follicular and thecal cellular layers and a collagen-filled space between them, (2) the development of microvilli of oocytal and follicular origin, (3) the differentiation of the vitelline envelope and the pore channels, (4) pinocytotic activity of the oocytes, and (5) rapid growth of the oocyte and its envelopes during vitellogenesis.
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References
Abraham M, Sandri C, Akert K (1979) Freeze-etch study of the teleostean pituitary. Cell Tissue Res 199:397–407
Abraham M, Hilge V, Lison S, Tibika H (1980) A functional analysis of the relationship between envelope cells and oocytes in the teleostean ovary. International Council for the Exploration of the Sea, Study Report CM/F:17, 1–9
Abraham M, Hilge V, Lison S, Tibika H (1981) The relationship between envelope cells and oocytes in the teleostean ovary — structure and function. Isr J Zool 30:110
Abraham M, Kieselstein M, Hilge V, Lison S (1982) Extravascular circulation in the pituitary of Mugil cephalus (Teleostei). Cell Tissue Res 225:567–579
Anderson E (1967) The formation of the primary envelope during oocyte differentiation in teleosts. J Cell Biol 35:193–212
Anderson E (1968) Cortical alveoli formation and vitellogenesis during oocyte differentiation in the pipefish, Syngnathus fuscus and the killifish, Fundulus heteroclitus. J Morphol 125:23–60
Anderson E (1972) The localization of acid phosphatase and the uptake of horseradish peroxidase in the oocyte and follicle cells of mammals. In: Biggers JD, Schuetz AW (eds) Oogenesis. University Park Press, Baltimore, 1–70
Anderson E (1974) Comparative aspects of the ultrastructure of the female gamete. In: Bourne GH, Danielli JF (eds) Int Rev Cytol [Suppl] 4:1–70
Anderson WA, Spielman A (1971) Permeability of the ovarian follicle of Aedes aegypti mosquitoes. J Cell Biol 50:201–221
Busson-Mabillot S (1973) Evolution des enveloppes de l'ovocyte et de l'oeuf chez un poisson téléostéen. J Microsc 18:23–44
Campbell CM, Jalabert B (1979) Selective protein incorporation by vitellogenic Salmo gairdneri oocytes in vitro. Ann Biol Anim Biochim Biophys 19 (2a):429–437
Dumont JN (1978) Oogenesis in Xenopus laevis (Daudin) VI. The route of injected tracer transport in the follicle and developing oocyte. J Exp Zool 204:193–218
Dumont JN, Wallace RA (1968) The synthesis, transport and uptake of yolk proteins in Xenopus laevis. J Cell Biol 39:37a
Enemar A, Eurenius L (1979) Organization and development of the perivascular space system in the neurohypophysis of the laboratory mouse. Cell Tissue Res 199:99–116
Flegler C (1977) Electron microscopic studies on the development of the chorion of the viviparous teleost Dermogenys pusillus (Hemirhamphidae). Cell Tissue Res 179:255–270
Flügel H (1967a) Elektronenmikroskopische Untersuchungen an den Hüllen der Oozyten und Eier des Flussbarsches Perca fluviatilis. Z Zellforsch 77:244–256
Flügel H (1967b) Lichtund elektronenmikroskopische Untersuchungen an Oozyten und Eiern einiger Knochenfische. Z Zellforsch 83:82–116
Glass LE, Cons JM (1968) Stage dependent transfer of systemically injected foreign protein antigen and radiolabel into mouse ovarian follicles. Anat Rec 162:139–155
Götting KJ (1965) Die Feinstruktur der Hüllschichten reifender Oocyten von Agonus cataphractus L. (Teleostei, Agonidae) Z Zellforsch 66:405–414
Götting KJ (1967) Die Follikel und die peripheren Strukturen der Oocyten der Teleosteer und Amphibien: Eine vergleichende Betrachtung auf der Grundlage elektronenmikroskopischer Untersuchungen. Z. Zellforsch 79:481–491
Graham R, Karnovsky MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302
Guraya SS (1978) Maturation of the follicular wall of nonmammalian vertebrates. In: Jones RE (ed) The vertebrate ovary. Plenum Press, New York, London 261–329
Hirose K (1972) The ultrastructure of the ovarian follicle of medaka, Oryzias latipes. Z Zellforsch 123:316–329
Jollie WP, Jollie LG (1964) The fine structure of the ovarian follicle of the ovoviviparous poeciliid Lebistes reticulatus I. Maturation of follicular epithelium. J Morphol 114:479–502
Kagawa H (1981) Estrogen synthesis in the teleost ovarian follicle: the two cell-type model of amago salmon. Ori Symposium on Fish Migration and Reproduction, Tokyo, p 24
Kraft AV, Peters HM (1963) Vergleichende Studien über die Oogenese in der Gattung Tilapia (Cichlidae, Teleostei). Z Zellforsch 61:434–485
Lison S (1976) Follicular development in the ovary of the teleosts Aphanius dispar and Aphanius mento. M Sc Thesis (in Hebrew), Jerusalem
Martinez-Palomo A (1970) The surface coats of animal cells. In: Bourne GH, Danielli JF (eds) Int Rev Cytol 29:29–74
Menn F le (1982) Ultrastructure of cellular and non-cellular layers surrounding the oocyte of a teleostean Gobius niger L.: preliminary observations. Proc Int Symp Reproductive Physiology of Fish, Wageningen 198
Nagahama Y, Chan K, Hoar WS (1976) Histochemistry and ultrastructure of preand post-ovulatory follicles in the ovary of the goldfish, Carassius auratus. Can J Zool 54:1128–1139
Nicholls TJ, Maple G (1972) 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 128:317–335
Selman K, Wallace RA (1982) The interand intracellular passage of proteins through the ovarian follicle in teleosts. Proc Int Symp Reproductive Physiology of Fish, Wageningen 151–154
Tesoriero JV (1977) Formation of the chorion (zona pellucida) in the teleost Oryzias latipes. I. Morphology of early oogenesis. J Ultrastruc Res 59:282–291
Tokarz RR (1978) Oogonial proliferation, oogenesis, and folliculogenesis in nonmammalian vertebrates. In: Jones RE (ed) The vertebrate ovary. Plenum Press, New York, London, 145–173
Wallace RA, Jared DW, Dumont JN, Sega MW (1973) Protein incorporation by isolated amphibian oocytes. III. Optimum incubation conditions. J Exp Zool 184:321–334
Wallace RA, Misulovin Z, Etkin LD (1981) Full-grown oocytes from Xenopus laevis resume growth when placed in culture. Proc Natl Acad Sci USA 78:3078–3082
Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343
Wegmann I, Götting KJ (1971) Untersuchungen zur Dotterbildung in den Oocyten von Xiphophorus helleri (Heckel, 1948) (Teleostei, Poeciliidae). Z Zellforsch 119:405–433
Wiebe JP (1968) The reproductive cycle of the viviparous seaperch Cymatogaster aggregata Gibbons. Can J Zool 46:1221–1234
Wiley HS, Dumont JN (1978) Stimulation of vitellogenenin uptake in stage IV Xenopus oocytes by treatment with chorionic gonadotropin in vitro. Biol Reprod 18:762–771
Yamazaki F (1965) Endocrinological studies on the reproduction of the female goldfish, Carassius auratus L., with special reference to the function of the pituitary gland. Mem Fac Fish Hokkaido Univ Vol 13 No. 1
Young G (1981) Endocrine control of oocyte maturation in the amago salmon. ORI Symposium on Fish Migration and Reproduction, Tokyo, 27
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This research was supported by a grant from the National Council for Research and Development, Israel, and the GKSS GeesthachtTesperhude, Federal Republic of Germany
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Abraham, M., Hilge, V., Lison, S. et al. The cellular envelope of oocytes in teleosts. Cell Tissue Res. 235, 403–410 (1984). https://doi.org/10.1007/BF00217866
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DOI: https://doi.org/10.1007/BF00217866