Summary
Comparative histochemical studies on the fish (Channa maruleus) and amphibian (Bufo stomaticus) oogenesis demonstrate a great similarity in the growth and differentiation of their egg follicle. The ooplasm, germinal vesicle and egg-membranes show distinct morphological and cytochemical changes during previtellogenesis and vitellogenesis.
During previtellogenesis the various components of the follicle are engaged in the synthesis of protoplasm as shown by the proliferation of yolk nucleus substance, mitochondria and some lipid bodies in the ooplasm and of nucleoli in the germinal vesicle. The substance of the yolk nucleus consisting of proteins, lipoproteins and RNA first appears adjacent to the nuclear membrane. Numerous mitochondria of lipoprotein composition, and some lipid bodies consisting of unsaturated phospholipids lie in association with the yolk nucleus which forms substratum for the former. The lipid bodies, present inside the germinal vesicle, follicular epithelium, and adjacent to the plasma membrane in association with some pinocytotic vacuoles, have been considered to play a significant role in the active transport of some substances from the environment into the ooplasm and from the latter into the germinal vesicle. The follicular epithelium itself is very poorly developed, negating its appreciable role in the contribution of specific substances into the oocyte, which seem to be contributed by the germinal vesicle showing a considerable development of nuclear sap, basophilic granules and nucleoli consisting of RNA and proteins; many large nucleoli bodily pass into the cytoplasm during the previtellogenesis of Channa, where their substance is gradually dissolved. The intense, diffuse, basophilic substance of the cytoplasm is believed due to free ribosomes described in many previous ultrastructural studies.
During vitellogenesis, the various deutoplasmic inclusions, namely carbohydrate yolk, proteid yolk and fatty yolk, are deposited in the ooplasm. The carbohydrate yolk bodies rich in carbohydrates originate in association with the plasma membrane and correspond to vesicles and cortical granules of previous studies. The proteid yolk consisting of proteins and some lipoproteins, and fatty yolk containing first phospholipids and some triglycerides and then triglycerides only are deposited under the influence of yolk nucleus substance, mitochondria and cytoplasm. The mitochondria and yolk nucleus substance foreshadow in some way the pattern of these two deutoplasmic inclusions and persist at the animal pole of mature egg while the other inclusions of previtellogenesis disappear from view. The pigment granules, which also show a gradient from the animal to vegetal pole in Bufo, are also formed in association with yolk nucleus substance and mitochondria. Some glycogen also appears in both the species. The nuclear membrane becomes irregular due to the formation of lobes. The lipid bodies of the germinal vesicle come to lie outside the nuclear membrane, suggesting active transport of some substances into the ooplasm; many nucleoli bodily pass into the ooplasm of Bufo, where they are gradually absorbed. The amount of basophilic granules is considerably increased in the germinal vesicle during vitellogenesis. Various egg-membranes such as outer epithelium, thin theca, single-layered follicular epithelium, zona pellucida or vitelline membrane surround the vitellogenic oocytes. The zona pellucida formed between the oocyte and follicle cells consists of a carbohydrate-protein complex. The follicle cells show lipid droplets, mitochondria and basophilic substance in their cytoplasm. The various changes that occur in the components of the follicle during vitellogenesis seem to be initiated by gonadrotrophins formed under the influence of specific environmental conditions.
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Literature
Afzelius, B. A.: Electron microscopy on the basophilic structures of the sea urchin egg. Z. Zellforsch. 45, 660–675 (1957).
Anderson, E., and H. W. Beams: Cytological observations on the fine structure of the guinea pig ovary with special reference to the oogonium, primary oocyte and associated follicle cells. J. Ultrastruct. Res. 3, 432–446 (1960).
André, J., and C. Rouiller: The ultrastructure of the vitelline body in the oocytes of the spider Tegenaria parietina. J. biophys. biochem. Cytol. 33, 977–984 (1957).
Balinsky, B. I., and R. J. Devis: Origin and differentiation of cytoplasmic structures in the oocytes of Xenopus laevis. Acta Embryol. Morph. exp. 6, 55–108 (1963).
Barka, T., and P. J. Anderson: Histochemistry. New York: Hoeber Medical Division, Harper & Row 1963.
Brachet, J.: Chemical embryology (trans. by L. G. Barth). New York: Interscience Publ. 1950.
—: The biochemistry of development. New York: Pergamon Press 1960.
Chiquoine, A. D.: The development of the zona pellucida of the mammalian ovum. Amer. J. Anat. 106, 149–170 (1960).
Chopra, H. C.: A morphological and histochemical study of the oocytes of the fish, Ophiocephalus punctatus, with particular reference to lipids. Quart. J. micr. Sci. 99, 149–158 (1958a).
—: Morphological and histochemical study of oocytes of the fish, Barbus ticto (punctius), with particular reference to lipids. Res. Bull. Panjab Univ. 152, 211–221 (1958b).
—: Cytological and cytochemical study of the growing oocytes of the fish, Boleophthalmus dussumerii. Cellule 60, 303–318 (1958c).
Cooper, R. S.: A study of frog egg antigens with serum-like reactive groups. J. exp. Zool. 107, 397–437 (1948).
Culling, C. F. A.: Handbook of histopathological techniques (including museum technique). London: Butterworths 1963.
Flickinger, R. A., and D. E. Rounds: The maternal synthesis of egg yolk proteins as demonstrated by isotopic and serological means. Biochim. biophys. Acta (Amst.) 22, 38–42 (1956).
—, and O. A. Schjeide: The localization of phosphorus and the site of calcium binding in the yolk protein of the frog's egg. Exp. Cell Res. 13, 312–316 (1957).
Glass, L. E.: Immuno-histological localization of serum-like molecules in frog oocytes. J. exp. Zool. 141, 257–282 (1959).
Guraya, S. S.: The structure and function of the so-called yolk nucleus in the oogenesis of birds. Quart. J. micr. Sci. 103, 411–416 (1962).
—: Histochemical studies on the yolk nucleus in fish oogenesis. Z. Zellforsch. 60, 659–666 (1963a).
—: Histochemical studies on the yolk nucleus in the oogenesis of Indian reptiles. Anat. Rec. 146, 17–21 (1963b).
—: Histochemical studies on the yolk nucleus in the oogenesis of mammals. Amer. J. Anat. 114, 283–291 (1964a).
—: A histochemical study of lipids in the mammalian testis. In: IInd International Congress of Histochemistry and Cytochemistry. Frankfort/M. Springer-Verlag, 16–21 August, 210–211, (1964b).
- A histochemical study of follicular atresia in the snake ovary. J. Morph. in press (1965).
—, and G. S. Greenwald: Histochemical studies on the interstitial gland in the rabbit ovary. Amer. J. Anat, 114, 495–520 (1964a).
—: A comparative histochemical study of interstitial tissue and follicular atresia in the mammalian ovary. Anat. Rec. 149, 411–434 (1964b).
Hibbard, H., et M. Parat: Nature et évolution des constituants cytoplasmiques de l'ovocyte de deux Téléostéens. Bull. Hist. 5, 313–330 (1928).
Hisaoka, K. K., and C. F. Firlit: The localization of nucleic acids during oogenesis in the zebrafish. Amer. J. Anat. 110, 203–215 (1963).
Holtfreter, J.: Experiments on the formed inclusions of the amphibian egg. 1. The effect of PH and electrolytes on the yolk and lipochondria. J. exp. Zool. 101, 355–406 (1946).
Hope, J., A. A. Humphries, and G. H. Bourne: Ultrastructural studies on developing oocytes of the salamander Triturus viridescens. 1. The relationship between follicle cells and developing oocytes. J. Ultrastruct. Res. 9, 302–324 (1963).
—: Ultrastructural studies on developing oocytes of the salamander Triturus viridescens. II. The formation of yolk. J. Ultrastruct. Res. 10, 547–556 (1964).
Jollie, W. P., and L. G. Jollie: The fine structure of the ovarian follicle of the ovoviviparous poeciliid fish, Lebistes reticulatus. I. Maturation of follicular epithelium. J. Morph. 114, 479–501 (1964).
Karasaki, S.: Studies on amphibian yolk. 1. The ultrastructure of yolk platelets. J. Cell Biol. 18, 135–151 (1963a).
Karasaki, S.: Studies on amphibian yolk. 5. Electron microscopic observations on the utilization of yolk platelets during embryogenesis. J. Ultrastruct. Res. 9, 225–247 (1963b).
Karasaki, S. and T. Komoda: Electron micrographs of a crystalline lattice structure in yolk platelets of the amphibian embryo. Nature (Lond.) 181, 407–408 (1958).
Kemp, N. E.: Electron microscopy of growing oocytes of Rana pipiens. J. biophys. biochem. Cytol. 2, 281–292 (1956).
Kessel, R. G.: Electron microscope studies on the origin of annulate lamellae in oocytes of Necturus. J. Cell Biol. 19, 391–414 (1963).
Kraft, A. V., u. H. M. Peters: Vergleichende Studien über die Oogenese in der Gattung Tilapia (Cichlidae, Teleostei). Z. Zellforsch. 61, 434–485 (1963).
Lanzavecchia, G.: The formation of the yolk in frog oocytes, in proceedings of European Regional Conference on Electron Microscopy. De Nederlandse Vereniging Voor Electronenmicroscopic, Delft, 2, 746 (1960).
Lillie, R. D.: Histopathologic technic and practical histochemistry. New York: Blakinston Press 1954.
Malone, T. E., and K. K. Hisaoka: A histochemical study of the formation of deutoplasmic components in developing oocytes of the zebrafish, Brachydanio rerio. J. Morph. 112, 61–76 (1963).
Moses, M. J.: The nucleus and chromosomes: A cytological perspective. In: Cytology and cell physiology, edit, by G. H. Bourne. New York: Academic Press 1964.
Nath, V.: A demonstration of vacuome and Golgi apparatus as independent cytoplasmic components in the fresh egg of frog. Z. Fellforsch. 13, 82–108 (1931).
—, B. L. Gupta, and R. Kaur: Histochemical and morphological studies of the lipids in oogenesis. VI. The frog, Rana tigrina. Res. Bull. Panjab Univ. 155, 223–234 (1958).
—, and S. K. Malhotra: Microphotographs demonstrating the vacuome, Golgi bodies, mitochondria and nucleolar extrusions in the fresh eggs of frog as studied under the phase contrast microscope. Res. Bull. Panjab Univ. 59, 149–152 (1954).
—: Oogenesis of the toad, Bufo stomaticus lutken, with observations under the phase contrast microscope. Res. Bull. Panjab Univ. 68, 39–49 (1955).
—, and M. D. Nangia: A demonstration of the vacuome and the Golgi apparatus as independent cytoplasmic components in the fresh eggs of Teleostean fishes. J. Morph. 52, 277–308 (1931).
Ohno, S., S. Karasaki. and K. Takata: Histo- and cytochemical studies on the superficial layer of yolk platelets in the Triturus embryo. Exp. Cell Res. 33, 310–318 (1964).
Pearse, A. G. E.: Histochemistry. London: J. and H. Churchill Ltd. 1960.
Raven, C. P.: Oogenesis. The storage of developmental information. New York: Pergamon Press 1961.
Rebhun, L. I.: Electron microscopy of basophilic structures of some invertebrate oocytes. I. Periodic lamellae and the nuclear envelope. J. biophys. biochem. Cytol. 2, 93–104 (1956a).
—: Electron microscopy of basophilic structures of some invertebrate oocytes. II. Fine structure of yolk-nuclei. J. biophys. biochem. Cytol. 2, 159–170 (1956b).
—: Some electron microscope observations on membranous basophilic elements of invertebrate eggs. J. Ultrastruct. Res. 5, 208–225 (1961).
Ringle, D. A.: Organization and composition of amphibian yolk platelets. Thesis, New York University, New York 1960. Quoted from Ward 1962a.
Rosenbaum, R. M.: Histochemical observations on the cortical region of the oocytes of Rana pipiens. Quart. J. micr. Sci. 99, 159–169 (1958).
Schechtman, A. M.: Uptake and transfer of macromolecules by cells with special reference to growth and development. Int. Rev. Cytol. 5, 303–322 (1956).
Seshachar, B. R., and R. P. Nayyar: Intranuclear lipids in the early oocytes of Heteropneustes fossilis (Teleostei). Quart. J. micr. Sci. 104, 69–73 (1963).
Sotelo, J. R., and O. Trujillo-Cenoz: Electron microscopy study of the vitelline body of some spider oocytes. J. biophys. biochem. Cytol. 3, 301–310 (1957).
Stenger, H. E., u. H. Wartenberg: Elektronenmikroskopische und histopochemische Untersuchungen über Struktur und Bildung der Zona pellucida menschlicher Eizellen. Z. Zellforsch. 53, 702–713 (1961).
Subramaniam, M. K., and R. G. Aiyar: Oogenesis of Acentrogobius neilli (Gobius neilli Day), with special reference to the behaviour of the nucleoli J. roy. micr. Soc. 55, 174–183 (1935).
Trujillo-Cenoz, O., and J. R. Sotelo: Relationship of the ovular surface with follicle cells and origin of the zona pellucida in rabbit oocytes. J. biophys. biochem. Cytol. 5, 347–350 (1959).
Voss, H. u. H. Wartenberg: Der topochemische Nachweis einer frühzeitigen polaren Differenzierung des Amphibieneies mit Hilfe der PAS-reaktion. Wiss. Z. Univ. Jena 4, 413–417 (1955).
Wallace, R. A., and S. Karasaki: Studies on amphibian yolk. 2. The isolation of yolk platelets from the eggs of Rana pipiens. J. Cell Biol. 18, 153–166 (1963).
Ward, R. T.: The origin of protein and fatty yolk in Rana pipiens. II. Electron microscopical and cytochemical observations of young and mature oocytes. J. Cell Biol. 14, 309–341 (1962a).
—: The origin of protein and fatty yolk in Rana pipiens. I. Phase microscopy. J. Cell Biol. 14, 303–308 (1962b).
Wartenberg, H.: Elektronenmikroskopische und histochemische Studien über die Oogenese der Amphibieneizelle. Z. Zellforsch. 58, 427–486 (1962).
Wartenberg, H., u. W. Schmidt: Elektronenmikroskopische Untersuchungen der strukturellen Veränderungen im Rindenbereich des Amphibieneies im Ovar und nach der Befruchtung. Z. Zellforsch. 54, 118–146 (1961).
Wischnitzer, S.: The ultrastructure of the yolk platelets of amphibian oocytes. J. biophys. biochem. Cytol. 3, 1040–1042 (1957).
—: The ultrastructure of the nucleus and nucleocytoplasmic relations. Int. Rev. Cytol. 10, 137–162 (1960).
—: An electron microscopic study of the Golgi apparatus of amphibian oocytes. Z. Zellforsch. 57, 202–212 (1962).
—: The ultrastructure of the layers enveloping yolk-forming oocytes from Tritutus viridescens. Z. Zellforsch. 60, 452–462 (1963).
—: Ultrastructural changes in the cytoplasm of developing amphibian oocytes. J. Ultrastruct. Res. 10, 14–26 (1964).
Yamamoto, K.: Studies on the formation of fish eggs. VIII. The fate of the yolk vesicle in the oocyte of the smelt, Hypomesus japonicus, during vitellogenesis. Embryologia (Nagoya) 3, 131–138 (1956).
Yamamoto, T.: Physiology of fertilization in fish eggs. Int. Rev. Cytol, 12, 361–405 (1961).
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The author wishes to express sincere appreciation and gratitude to Dr. Gilbert S. Greenwald, who has made the completion of this investigation possible.
Ph. D. Population Council Post-doctoral Fellow.
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Guraya, S.S. A comparative histochemical study of fish (Channa maruleus) and amphibian (Bufo stomaticus) oogenesis. Zeitschrift für Zellforschung 65, 662–700 (1965). https://doi.org/10.1007/BF00342590
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DOI: https://doi.org/10.1007/BF00342590