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Long-lasting exocytosis and massive structural reorganisation in the egg periphery during cortical reaction in Platynereis dumerilii (Annelida, Polychaeta)

Published online by Cambridge University Press:  26 September 2008

B. Kluge
Affiliation:
Zoologisches Institut der Universität Mainz, D-55099 Mainz, Germany.
M. Lehmann-Greif
Affiliation:
Zoologisches Institut der Universität Mainz, D-55099 Mainz, Germany.
A. Fischer*
Affiliation:
Zoologisches Institut der Universität Mainz, D-55099 Mainz, Germany.
*
Dr A. Fischer, Zoologisches Institut der Universität Mainz, D-55099 Mainz, Germany. Telephone: 6131-392577. Fax:6131-393835.

Summary

The course of the cortical reaction in the Platynereis dumerilii egg is described from live observation and from sectioned fixed material and is found to differ in several aspects from the course of cortical reactions in better-known systems. Cortical granules are unusually numerous. They are discharged by exocytosis during a period of about 25 min following fertilisation (18°C). Most of the surplus membrane material brought to the egg surface by exocytosis is set free into the perivitelline space. Swelling of egg jelly precursor secreted by cortical granule exocytosis may be causal for the detachment of the vitelline envelope from the egg cell surface which, however, remains attached punctately to the vitelline envelope by about 30000 microvilli. Under the strain of the distending vitelline envelope, the bases of the microvilli move and line up, pulling the cell surface into a network of ridges. The grooves in between the ridges are the sites of exocytoses. Cytochalasin B, generally destabilising actin filaments, induces rupture of the microvilli and exaggerated distension of the vitelline envelope during the cortical reaction. In a final phase of the cortical reaction the vitelline envelope wrinkles and falls back onto the egg cell surface, the microvilli shorten and the egg cell transiently becomes deformed by local contractions. The cortical reaction in the nereid egg is discussed as a process of distortion and reorganisation of the egg cortex and plasmalemma. The abundance of cortical granules accommodating egg jelly precursor in the Platynereis oocyte is attributed to the mode of so-called diffuse oogenesis characteristic of nereids, i.e. of differentiation of oocytes freely suspended in the coelomic fluid. In nereids, egg jelly therefore forms after fertilisation as opposed to ovulation.

Type
Article
Copyright
Copyright © Cambridge University Press 1995

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References

Anderson, E. (1968). Oocyte differentiation in the sea urchin, Arbacia punctulata, with particular reference to the cortical granules, and their participation in the cortical reaction. J. Cell Biol. 37, 514–39.CrossRefGoogle Scholar
Bannon, G. & Brown, G.C. (1980). Vesicle involvement in the egg cortical reaction of the horseshoe crab, Limulus polyphemus. Dev. Biol. 76, 418–27.CrossRefGoogle ScholarPubMed
Brummet, A.R. & Dumont, J.N. (1981). Cortical vesicle breakdown in fertilized eggs of Fundulus heteroclitus. J. E. Zool. 216, 63–79CrossRefGoogle Scholar
Carron, C.P. & Longo, F.J. (1984). Pinocytosis in fertilized sea urchin (Arbacia punctulata) eggs. J. Exp. Zool. 231, 413–22.CrossRefGoogle Scholar
Chambers, R. (1933). The manner of sperm entry in various marine ova. J.Exp. Biol. 10, 130–41.CrossRefGoogle Scholar
Chandler, D.E. (1984). Comparison of quick-frozen and chemically fixed sea-urchin eggs: structural evidence that cortical granule exocytosis is preceded by a local increase in membrane mobility. J.Cell Sci. 72, 2336.CrossRefGoogle ScholarPubMed
Chandler, D.E. (1991). Multiple intracellular signals coordinate structural dynamics in the sea urchin egg cortex at fertilization. J. Electron. Microsc.Technique 17, 266–93.CrossRefGoogle ScholarPubMed
Chandler, D.E. & Heuser, J. (1979). Membrane fusion during secretion: cortical granule exocytosis in sea urchin eggs as studied by quick-freezing and freeze-fracture. J. Cell Biol. 83, 91108.CrossRefGoogle ScholarPubMed
Chandler, D.E. & Heuser, J. (1981). Postfertilization growth of microvilli in the sea urchin egg: new views from eggs that have been quick frozen, freeze fractured, and deeply etched. Dev. Biol. 82, 393400.CrossRefGoogle ScholarPubMed
Costello, D.P. (1949). The relations of the plasma membrane, vitelline membrane, and jelly in the egg of Nereis limbata. Gen. Physiol. 32, 351–66.CrossRefGoogle ScholarPubMed
Costello, D.P. (1958). The cortical response of the ovum to activation after centrifuging. Physiol. Zool. 31, 179–88.CrossRefGoogle Scholar
Dewel, W.C. & Clark, W.H. (1974). A fine structural investigation of surface specializations and the cortical reaction in eggs of the cnidarian Bunodosoma cavernata. J. Cell Biol. 60, 7891.CrossRefGoogle ScholarPubMed
Dhainaut, A. (1969). Origine et structure des formations mucopolysaccharidiques de la zone corticale de l'ovocyte de Nereis diversicolor O.F. Müller (Annéflide polychète). J.Microscopie 8, 6986.Google Scholar
Dhainaut, A. (1970). Etude cytochimique et ultrastructurale de l'evolution ovocytaire de Nereis pelagica L. (Annélide polychète).. I. Ovogenèse naturelle.Z. Zellforsch. 104, 375–90.CrossRefGoogle Scholar
Dondua, A.K. & Sidorova, P.A. (1986). The egg vitelline envelope of Nereis virens Sars and the alteration of its permeability after cytochalasin B application. (In Russian, English summary). Cytologia 28, 173–9.Google Scholar
Donovan, M.J. & Hart, N.H. (1986). Cortical granule exocytosis is coupled with membrane retrieval in the egg of Brachydanio. J. Exp. Zool. 237, 391405.CrossRefGoogle ScholarPubMed
Dorresteijn, A.W.C. (1990). Quantitative analysis of cellular differentiation during early embryogenesis of Platynereis dumerilii. Rouxs Arch.Dev. Biol. 199, 1430.CrossRefGoogle Scholar
Dorresteijn, A.W.C. & Kluge, B. (1990). On the establishment of polarity in polychaete eggs. In Experimental Embryology of Aquatic Plants and Animals, ed. Marthy, H.J., pp. 197209. New York: Plenum Press.CrossRefGoogle Scholar
Emanuelsson, H. & Odselius, R. (1985). Presence of calcium in polychaete cortical granules demonstrated by X-ray microanalysis on ultrathin cryosections of oocytes and eggs. Cell Tissue Res. 242, 225–8.CrossRefGoogle Scholar
Fallon, J.F. & Austin, C.R., (1967). Fine structure of gametes of Nereis limbata (Annelida) before and after interaction. J. Exp. Zool. 166, 225–42.CrossRefGoogle ScholarPubMed
Fisher, G.W. & Rebhun, L.I. (1983). Sea urchin cortical granule exocytosis is followed by a burst of membrane retrieval via uptake into costed vesicles. Dev. Biol. 99, 456–72.CrossRefGoogle Scholar
Hauenschild, C. & Fischer, A. (1969). Platynereis dumerilii: Mikroskopische Anatomie, Fortpflanzung, Entwicklung. Grosses Zoologisches Praktikum 10b. Stuttgart: Gustav Fischer Verlag.Google Scholar
Holland, N.D. (1979). Electron microscopic study of the cortical reaction of an ophiurid echinoderm. Tissue Cell 11, 445–55.CrossRefGoogle Scholar
Iwamatsu, T. & Ohta, T. (1976). Breakdown of the cortical alveoli of the medaka eggs at the time of fertilization, with a particular reference to the possible role of spherical bodies in the alveoli. Rouxs Arch. Dev, Biol. 180, 297309.CrossRefGoogle Scholar
Jaffe, L.F. (1983). Sources of calcium in egg activation: a review and hypothesis. Dev. Biol. 99, 265–76.CrossRefGoogle ScholarPubMed
Jaffe, L.F. (1985). The role of calcium explosions, waves and pulses in activating eggs. In Biology of Fertilization, vol. 3, ed. Metz, C.B. & Monroy, A., pp. 128–65. New York: Academic Press.Google Scholar
Just, E.E. (1939). The Biology of the Cell Surface.Philadelpia: Blakiston.Google Scholar
Kluge, B. (1990). Cytologische Analyse der fruhesten Entwicklungsvorgange bei Platynereis dumerilii (Annelida, Polychaeta). Thesis, University of Mainz.Google Scholar
Lillie, F.R. (1911). Studies of fertilization in Nereis. I. The cortical changes in the egg. II. Partial fertilization. J.Morphol. 22, 361–93.CrossRefGoogle Scholar
Longo, F.J. (1988). Reorganization of the egg surface at fertilization. Int. Rev. Cytol. 113, 233–69.CrossRefGoogle ScholarPubMed
Millonig, G. (1969). Fine structure analysis of the cortical reaction in the sea urchin egg after normal fertilization and after electric induction. J.Submicrosc. Cytol. 1, 6984.Google Scholar
Novikoff, A.B. (1939). Changes at the surface of Nereis limbata eggs after insemination. J.Exp. Biol. 16, 403–8.CrossRefGoogle Scholar
Ohta, T., Iwamatsu, T., Tanaka, M. & Yoshimoto, Y. (1990). Cortical alveolus breakdown in the eggs of the freshwater teleost Rhodeus ocellatus ocellatus. Anat. Rec. 227, 486–96.CrossRefGoogle ScholarPubMed
Pasteels, J.J. (1966). La reaction corticale de fécondation de l'oeuf de Nereis diversicolor, étudiée au microscopie éléctronique. Acta Embryol. Morphol. Exp. 6, 155–65.Google Scholar
Picheral, B. & Charbonneau, M. (1982). Anuran fertilization:a morphological reinvestigation of some early events. J.Ultrastruct. Res. 81, 306–21.CrossRefGoogle ScholarPubMed
Porchet, M. & Spik, G. (1978). Biochemical analysis of Nereidae gametogenesis. I. Evolution of glycoconjugates during natural oogenesis in Perinereis cultrifera Grube (polychaete annelid). Comp. Biochem. Physiol. 59B, 175–81.Google Scholar
Sato, M. & Osanai, K. (1986). Morphological identification of sperm receptors above egg microvilli in the polychaete, Neanthes japonica. Dev. Biol. 113,263–70.CrossRefGoogle ScholarPubMed
Schmell, E.D., Gulyas, B.J. & Hedrick, L. (1983). Egg surface changes during fertilization and the molecular mechanism of the block to polyspermy. In Mechanism and Control of Animal Fertilization, ed Hartmann, J.F., 365413New York: Academic Press.Google Scholar
Schroeder, T.E. (1979). Surface area change at fetilization:Resorption of the mosaic membrane. Dev. Biol. 70 306–26.CrossRefGoogle Scholar
Schuel, H. (1985). Functions of egg cortical granules. In Biology of Fertilization, 3 Metz, C.B. & Monroy, A.251–76. New York: Academic Press.Google Scholar
Spek, J. (1930). Zustandsanderungen der Plasmakolloide bei Befruchtung und Entwicklung des Nereis-Eies Protoplasma 9 370427.CrossRefGoogle Scholar
Spiegel, E.Howard, L. & Spiegel, M. (1989). Elongated microvilli support the sea urchin embryo concentrically within the perivitelline space until hatching Arch. Dev. Biol. 199 228–36.CrossRefGoogle Scholar
Takashima, Y. & Tominaga, A. (1978). Ultracytochemistry of the cortical granules and cortical alveoli of Japanese palolo eggs. Acta Histochem. Cytochem. 11 171–9.CrossRefGoogle Scholar
Vacquer, V.D. (1981). Dynamic changes of the egg cortex. Dev. Biol. 84 126.CrossRefGoogle Scholar
Yonemura, S. & Mabuchi, I. (1987). Wave of cortical actin polymerization in the sea urchin egg. Cell Motil 7 4653.CrossRefGoogle ScholarPubMed