Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-05T11:00:16.110Z Has data issue: false hasContentIssue false
  • English
  • Français

Cortical changes in starfish (Asterina pectinifera) oocytes during 1-methyladenine-induced maturation and fertilisation/activation

Published online by Cambridge University Press:  26 September 2008

Frank J. Longo ,
Mark Woerner ,
Kazuyoshi Chiba  and
Motonori Hoshi
Frank J. Longo*
Affiliation:
Department of Anatomy, University of Iowa, USA and Tokyo Institute of Tehnology, Japan.
Mark Woerner
Affiliation:
Department of Anatomy, University of Iowa, USA and Tokyo Institute of Tehnology, Japan.
Kazuyoshi Chiba
Affiliation:
Department of Anatomy, University of Iowa, USA and Tokyo Institute of Tehnology, Japan.
Motonori Hoshi
Affiliation:
Department of Anatomy, University of Iowa, USA and Tokyo Institute of Tehnology, Japan.
*
Frank J. Longo, Department of Anatomy, University of Iowa, Iowa City, IA 52242, USA.
Get access Rights & Permissions [Opens in a new window]

Summary

Maturation of the starfish oocyte cortex to produce an effective cortical granule reaction and fertilisation envelope is believed to develop in three phases: (1) pre-methyladenine (1-MA) stimulation; (2) post-1-MA stimulation, pregerminal vesicle breakdown; and (3) post-germinal vesicle breakdown. The present study was initiated to identify what each of these phases may encompass, specifically with respect to structures associated with the oocyte cortex, including cortical granules, microvilli and vitelline layer. 1-MA treatment brought about an orientation of cortical granules such that they became positioned perpendicular to the oocyte surface, and an ∼ 4-fold decrease in microvillar length. A-23187 activation of immature oocytes treated with (10 min; pregerminal vesicle breakdown) or without 1-MA resulted in a reduction in cortical granule number of 21% and 41%, respectively (mature oocytes underwent a 96% reduction in cortical granules). Elevation of the fertilisation envelope in both cases was significantly retarded compared with activated mature oocytes. In activated mature oocytes, the vitelline layer elevated 20.0 ± 5.4 μm from the egg's surface, whereas in immature oocytes treated with just A-23187 or with 1-MA (10 min) and A-23187, it lifted 0.35 ± 0.1 and 0.17 ± 0.04 μm, respectively. The fertilisation envelopes of activated (or fertilised) immature oocytes also differed morphologically from those of mature oocytes. In activated, immature oocytes, the fertilisation envelope was not uniform in its thickness and possessed thick and thin regions as well as fenestrations. Additionally, it lacked a complete electron-dense stratum that characterised the fertilisation envelopes of mature oocytes. The nascent perivitelline space of immature oocytes was also distinguished by the presence of numerous vesicles which appeared to be derived from microvilli. Differences in the morphology of cortices from activated (fertilised) and non-activated, immature and mature oocytes substantiate previous investigations demonstrating three phases of cortical maturation, and are consistent with physiological changes that occur during oocyte maturation, involving ionic conductance of the plasma membrane, establishment of slow and fast blocks to polyspermy and elevation of a fertilisation envelope.

Keywords

CortexCortical granule reactionFertilisationOocyte maturationPolyspermy prevention
Type
Article
Information
Zygote , Volume 3 , Issue 3 , August 1995 , pp. 225 - 239
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alliegro, M.C., & Schuel, H. (1988). Immunocytochemical localization of the 35-kDa sea urchin egg trypsin-like protease and its effects upon the egg surface. Dev. Biol. 125, 168–80.CrossRefGoogle ScholarPubMed
Anderson, E. (1968). Oocyte differentiation in the sea urchin, Arbacia punctulata, with particular reference to the origins of cortical granules and their participation in the cortical reaction. J. Cell Biol. 37, 514–39.CrossRefGoogle Scholar
Arion, D., Meijer, L., Brizuela, L., & Beach, D. (1988). cdc2 is a component of the M phase-specific histone H1 kinase: evidence for identity with MPF. Cell 55, 371–8.CrossRefGoogle Scholar
Carroll, E.J., & Epel, D. (1975). Isolation and biological activity of the proteins released by sea urchin eggs following fertilization. Dev. Biol. 44, 22–32.CrossRefGoogle Scholar
Cayer, M.L., Kishimoto, T., & Kanatani, H. (1975). Formation of the fertilization membrane by insemination of immature starfish oocytes pretreated with calcium-free sea water. Dev. Growth Differ. 17, 119–25.CrossRefGoogle Scholar
Chambers, R. (1930). The manner of sperm entry in the starfish egg. Biol. Bull. 58, 344–69.CrossRefGoogle Scholar
Chandler, D.E., & Heuser, J. (1980). The vitelline layer of the sea urchin egg and its modification during fertilization. J. Cell Biol. 84, 618–32.CrossRefGoogle ScholarPubMed
Chiba, K., & Hoshi, M. (1989a). Three phases of cortical maturation during meiosis reinitiation in starfish oocytes. Dev. Growth Differ. 31, 447–51.CrossRefGoogle ScholarPubMed
Chiba, K., & Hoshi, M. (1989b). Activation of starfish oocytes modifies their hormone dependent period for 1-methyladenine meiosis reinitiation. Dev. Growth Differ. 31, 453–8.CrossRefGoogle ScholarPubMed
Chiba, K., Kado, R.T., & Jaffe, L.A. (1990). Development of calcium release mechanisms during starfish oocyte maturation. Dev. Biol. 140, 300–6.CrossRefGoogle ScholarPubMed
Detering, N.K., Decker, G.L., Schmell, E.D., & Lennarz, W.J. (1977). Isolation and characterization of plasma membrane-associated cortical granules from sea urchin eggs. J. Cell Biol. 75, 899–914.CrossRefGoogle ScholarPubMed
Fol, H. (1877). Sur le commencement de l'henogénie chez divers animaux. Arch. Zool. Exp. Gen. 6, 145–69.Google Scholar
Gardiner, D.M., & Grey, R.D. (1983). Membrane junctions in Xenopus eggs: their distribution suggests a role in calcium regulation. J. Cell Biol. 96, 1159–63.CrossRefGoogle ScholarPubMed
Gilligan, D.M., & Satir, B.H. (1982). Protein phosphorylation/dephosphorylation and stimulus–secretion coupling in wild type and mutant Paramecium. J. Biol. Chem. 257, 13903–6.CrossRefGoogle ScholarPubMed
Green, J.D., & Summers, R.G. (1980). Formation of the cortical concavity at fertilization in the sea urchin egg. Dev. Growth Differ. 22, 812–9.CrossRefGoogle ScholarPubMed
Guerrier, P., Moreau, M., & Dorée, M. (1977). Hormonal control of meiosis in starfish: stimulation of protein phosphorylation induced by 1-methyladenine. Mol. Cell Endocrinol. 7, 137–50.CrossRefGoogle ScholarPubMed
Hall, H.G. (1978). Hardening of the sea urchin fertilization envelope by peroxide-catalyzed phenolic coupling of tyrosines. Cell 15, 343–55.CrossRefGoogle Scholar
Hirai, S., & Shida, H. (1979). Shortening of microvilli during the maturation of starfish oocyte from which vitelline coat was removed. Bull. Mar. Biol. Station Asamushi, Tohoku Univ. 16, 161–7.Google Scholar
Hirai, S., Kubota, J., & Kanatani, H. (1971). Induction of cytoplasmic maturation by 1-methyladenine in starfish oocytes after removal of the germinal vesicle. Exp. Cell Res. 68, 137–43.CrossRefGoogle ScholarPubMed
Hirai, S., Nagahama, Y., Kishimoto, T., & Kanatani, H. (1981). Cytoplasmic maturity revealed by the structural changes in incorporated spermatozoon during the course of starfish oocyte maturation. Dev. Growth Differ. 23, 465–78.CrossRefGoogle ScholarPubMed
Holland, N. (1980). Electron microscopic study of the cortical reaction in eggs of the starfish (Patiria miniata). Cell Tissue Res. 205, 67–76.CrossRefGoogle Scholar
Hylander, B.L., & Summers, R.G. (1981). The effect of local anesthetics and ammonia on cortical granule–plasma membrane attachment in the sea urchin egg. Dev. Biol. 86, 1–11.CrossRefGoogle ScholarPubMed
Jaffe, L.A., & Terasaki, M. (1993). Structural changes of the endoplasmic reticulum of sea urchin eggs during fertilization. Dev. Biol. 156, 566–73.CrossRefGoogle ScholarPubMed
Jaffe, L.A., & Terasaki, M. (1994). Structural changes in the endoplasmic reticulum of starfish oocytes during meiotic maturation and fertilization. Dev. Biol. 164, 579–87.CrossRefGoogle ScholarPubMed
Labbé, J.C., Lee, M.G., Nurse, P., Picard, A., & Dorée, M. (1988). Activation at M-phase of a protein kinase encoded by a starfish homologue of the cell cycle control gene cdc2+. Nature 335, 251–4.CrossRefGoogle ScholarPubMed
Longo, F.J. (1978). Insemination of immature sea urchin (Arbacia punctulata) eggs. Dev. Biol. 62, 271–91.CrossRefGoogle ScholarPubMed
Longo, F.J. (1981). Morphological features of the surface of the sea urchin (Arbacia punctulata) egg: oolemma–cortical granule association. Dev. Biol. 84, 173–82.CrossRefGoogle ScholarPubMed
Longo, F.J., & Anderson, E. (1970). A cytological study of the relation of the cortical granule reaction to subsequent events of fertilization in urethane-treated eggs of the sea urchin, Arbacia punctulata. J. Cell Biol. 47, 646–65.CrossRefGoogle ScholarPubMed
Longo, F.J., So, F., & Schuetz, A.W. (1982). Meiotic maturation and the cortical granule reaction in starfish eggs. Biol. Bull. 163, 453–76.CrossRefGoogle Scholar
Lynn, J.W., McCulloh, D.H., & Chambers, E.L. (1988). Voltage clamp studies of fertilization in sea urchin eggs. II. Current patterns in relation to sperm entry, nonentry, and activation. Dev. Biol. 128, 305–23.CrossRefGoogle ScholarPubMed
McCulloh, D.H., Lynn, J.W., & Chambers, E.L. (1987). Membrane depolarization facilitates sperm entry, large fertilization cone formation, and prolonged current responses in sea urchin oocytes. Dev. Biol. 124, 177–90.CrossRefGoogle ScholarPubMed
Meijer, L., & Guerrier, P. (1984). Maturation and fertilization in starfish oocytes. Int. Rev. Cytol. 86, 129–96.CrossRefGoogle ScholarPubMed
Michener, M.L.Dawson, W.B., & Creutz, C.E. (1986). Phosphorylation of a chromaffin granule-binding protein in stimulated chromaffin cells. J. Biol. Chem. 261, 6548–55.CrossRefGoogle ScholarPubMed
Millonig, G. (1969). Fine structure analysis of the cortical reaction in the sea urchin egg: after normal fertilization and after electrical induction. J. Submicrosc. Cytol. 1, 69–84.Google Scholar
Miyazaki, S. (1979). Fast polyspermy block and activation potential: electrophysiological bases for their changes during oocyte maturation of a starfish. Dev. Biol. 70, 341–54.CrossRefGoogle ScholarPubMed
Miyazaki, S., & Hirai, S. (1979). Fast polyspermy block and activation potential: correlated changes during oocyte maturation of a starfish. Dev. Biol. 70, 327–40.CrossRefGoogle ScholarPubMed
Miyazaki, S.I., Ohmori, H., & Sasaki, S. (1975a). Action potential and non-linear current–voltage relation in starfish oocytes. J. Physiol. (Lond.) 246, 37–54.CrossRefGoogle ScholarPubMed
Miyazaki, S.I., Ohmori, H., & Sasaki, S. (1975b). Potassium rectification of the starfish oocyte membrane and their changes during oocyte maturation. J. Physiol. (Lond.) 246, 55–78.CrossRefGoogle ScholarPubMed
Momayezi, M., Lumpert, C.J., Kersken, H., Gras, U., Plattner, H., Krinks, M.H., & Klee, C.B. (1987). Exocytosis induction in Paramecium tetraurelia cells by exogenous phosphoprotein phosphotase in vivo and in vitro: possible involvement of calcineurin in exocytotic membrane fusion. J. Cell Biol. 105, 181–9.CrossRefGoogle Scholar
Moody, W.J., & Bosma, M.M. (1985). Hormone-induced loss of surface membrane during maturation of starfish oocytes: differential effects on potassium and calcium channels. Dev. Biol. 112, 396–404.CrossRefGoogle ScholarPubMed
Otto, J.J., & Schroeder, T.E. (1984). Assembly–disassembly of actin bundles in starfish oocytes: an analysis of actin-associated proteins in the isolated cortex. Dev. Biol. 101, 263–73.CrossRefGoogle ScholarPubMed
Picard, A., & Dorée, M. (1983). Is calcium the second messenger of 1-methyladenine in meiosis reinitiation of starfish oocytes?. Exp. Cell Res. 145, 325–37.CrossRefGoogle ScholarPubMed
Picard, A., Giraud, F., LeBouffant, F., Sladeczek, F., LePeuch, C., & Dorée, M. (1985). Inositol 1,4,5-triphosphate microinjection triggers activation, but not meiotic maturation in amphibian and starfish oocytes. FEBS Lett. 182, 446–50.CrossRefGoogle Scholar
Richardson, K.C., Jarett, L., & Finke, E.H. (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–23.CrossRefGoogle ScholarPubMed
Rosenberg, M.P., Hoesch, P., & Lee, H.H. (1977). The relationship between 1-methyladenine induced surface changes and fertilization in starfish oocytes. Exp. Cell Res. 107, 239–45.CrossRefGoogle ScholarPubMed
Sano, K. (1985). Calcium- and cyclic AMP–independent, labile protein kinase appearing during starfish oocyte maturation: its extraction and partial characterization. Dev. Growth Differ. 27, 263–75.CrossRefGoogle ScholarPubMed
Schroeder, T.E. (1981). Microfilament–mediated surface change in starfish oocytes in response to 1-methylade- nine: implications for identifying the pathway and receptor sites for maturation-inducing hormones. J. Cell Biol. 90, 362–71.CrossRefGoogle Scholar
Schroeder, T.E., & Otto, J.J. (1984). Cyclic assembly–disassembly of cortical microtubules during maturation and early development of starfish oocytes. Dev. Biol. 103, 493–503.CrossRefGoogle ScholarPubMed
Schroeder, T.E., & Otto, J.J. (1991). Snoods: a periodic network containing cytokeratin in the cortex of starfish oocytes. Dev. Biol. 144, 240–7.CrossRefGoogle ScholarPubMed
Schroeder, T.E., & Stricker, S.A. (1983). Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev. Biol. 98, 373–84.CrossRefGoogle ScholarPubMed
Schuel, H. (1985).Functions of egg cortical granules. In Biology of Fertilization, Metz, C.B., & Monroy, A. 3 1–43. New York:Academic Press.Google Scholar
Schuel, H., Kelly, J.W., Berger, E.R., & Wilson, W.L. (1974). Sulfated acid mucopolysaccharides in the cortical granules of eggs. Exp. Cell Res. 88, 24–30.CrossRefGoogle ScholarPubMed
Schuetz, A.N. (1975). Cytoplasmic activation of starfish oocytes by sperm and divalent ionophore A–23187. J. Cell Biol. 66, 86–94.CrossRefGoogle ScholarPubMed
Shapiro, B.M., Somers, C.E., & Weidman, P.J. (1989). Extra-cellular remodeling during fertilization. In The Cell Biology of Fertilization, Schatten, H., & Schatten, G..251–76.New York: Academic Press.CrossRefGoogle Scholar
Shen, S., & Steinhardt, R.A. (1976). An electro-physiological study of the membrane properties of the immature and mature oocyte of the batstar, Patiria miniata. Dev. Biol. 48, 148–62.CrossRefGoogle Scholar
Simoncini, L. & Moody, W.J. (1990). Changes in voltage-dependent currents and membrane area during maturation of starfish oocytes: species differences and similarities. Dev. Biol. 138, 194–201.CrossRefGoogle ScholarPubMed
Stevens, M. (1970). Procedures for induction of spawning and meiotic maturation of starfish oocytes by treatment with 1-methyladenine. Exp. Cell Res. 59, 482–4.CrossRefGoogle ScholarPubMed
Stieghart, W., Theoharides, T.C., Alper, S.L., Douglas, W.W., & Greengard, P. (1978). Calcium-dependent protein phosphorylation during secretion by exocytosis in the mast cell. Nature 275, 329–31.CrossRefGoogle Scholar
Stricker, S.A., Centonze, V.E., & Melendez, R.F. (1994). Calcium dynamics during starfish oocyte maturation and fertilization. Dev. Biol. 166, 34–58.CrossRefGoogle ScholarPubMed
Terasaki, M., & Jaffe, L.A. (1991). Organization of the sea urchin egg endoplasmic reticulum and its reorganization at fertilization. J. Cell Biol. 114, 929–40.CrossRefGoogle ScholarPubMed
Troyer, H. (1980).Principles and Techniques of Histochemistry. Boston. MA: Little Brown.Google Scholar
Veron, M., Foerder, C., Eddy, E.M., & Shapiro, B.M. (1977). Sequential biochemical and morphological events during assembly of the fertilization membrane of the sea urchin. Cell 10, 321–8.CrossRefGoogle ScholarPubMed