Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-23T22:59:08.307Z Has data issue: false hasContentIssue false
  • English
  • Français

Different calcium-dependent pathways control fertilisation-triggered glycoside release and the cortical contraction in ascidian eggs

Published online by Cambridge University Press:  26 September 2008

Alex McDougall ,
Christian Sardet  and
Charles. C Lambert
Alex McDougall*
Affiliation:
Station Zoologique, Villefranche-sur-Mer, France, Station Biologique, Roscoff, France, and Biology Department, California state University, Fullerton, USA
Christian Sardet
Affiliation:
Station Zoologique, Villefranche-sur-Mer, France, Station Biologique, Roscoff, France, and Biology Department, California state University, Fullerton, USA
Charles. C Lambert
Affiliation:
Station Zoologique, Villefranche-sur-Mer, France, Station Biologique, Roscoff, France, and Biology Department, California state University, Fullerton, USA
*
Alex McDougall, URA 671 CNRS/Paris VI, Station Zoologique, F-06230 Villefranche-sur-Mer, France. Fax: 33.93.76.37.92.
Get access Rights & Permissions [Opens in a new window]

Summary

Fertilisation of ascidian eggs induces the rapid release of a cell surface N-acetylglycosaminidase that blocks sperm binding to vitelline coat sperm receptors resulting in a block to polyspermy. Fertilisation also triggers a large contraction of the egg (thus stimulating ooplasmic segregation) that is completed within 5 min of insemination. In eggs of the ascidian Phallusia mammillata, glycosidase release and cortical contractions are blocked by BAPTA-AM [bis-(o-aminophenoxy-ethane-N,N,N',N' -tetraacetic acid, tetra(acetoxymethyl)-ester], a cell-permeant calcium chelator, indicating that both processes are probaly dependent on a rise in intracellular calcium levels. Both glycosidase release and the cortical contraction are induced by treatment of the egg with the protein synthesis inhibitor emetine, while only the glycosidase release is induced by isoproterenol, carbachol or acetylcholine. Previous work with ryanodine demonstrated that ryanodine also caused glycosidase release but not the cortical contraction Inversely, activation by ionomycin in calcium-free sea water causes cortical contractions but not glycosidase release. Thus the two processes can be activated independently. Dextran-coupled (10kDa) calcium green-1 injected eggs show an increase in intracellular calcium 30–40s before the cortical contraction is triggered by fertilisation or ionomycin- induced activation. This confirms previous findings that the cortical contraction is a consequence of the activation calcium the triggered by te sperm. The extracellular calcium requirement for the glycosidase release suggests that calcium influx may be more important for this phase of egg activation. Thus activation eggs appears to involve two independent pathways involving calcium.

Keywords

AscidianCalciumCortical contractionEggGlycosidase release
Type
Article
Information
Zygote , Volume 3 , Issue 3 , August 1995 , pp. 251 - 258
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

Abdelmajid, H.Leclerc-David, C.Moreau, M.Guerrier, P. & Ryazanov, A. (1993). Release from the metaphase I block in invertebrate oocytes possible involvement of Ca2+/calmodulin-dependent kinase III. Int.J. Dev. Biol. 37 279–90.Google ScholarPubMed
Arnoult, C.Georges, D. & Villaz, M. (1994). Cell cycle-related fluctuations in oocyte surface area of the ascidian Ciona intestinalis after meiosis resumption. Dev. Biol. 166 1–10.CrossRefGoogle ScholarPubMed
Berridge, M.J. (1993). Inositol triphosphate and calcium signaling Nature 361, 315–25.CrossRefGoogle Scholar
Bezprovanny, I.Watras, J. & Ehrlich, B.E. (1991). Bell-shaped calcium- response curves of Ins(1,4,5,)P3- and calciumgated channels from endoplasmic reticulum of cerebellum Nature 351, 751–4.CrossRefGoogle Scholar
Colas, P.Launay, C.Van Loon, A. & Guerrier, P. (1993) Protein synthesis controls cyclin stability im metaphase I-arrested oocytes of Patella vulgata Exp. Cell Res. 208 518–21.CrossRefGoogle Scholar
Dale, B. (1988) Primary and secondary messengers in the activation of ascidian eggs. Exp. Cell Res. 177 215–11.CrossRefGoogle ScholarPubMed
Dasilva, A.M. & Klein, C. (1989). Characterization of a glycosyl-phosphatidylinositol degarding actvity in Dicytostelium discoideum membranes Exp. Cell Res. 185 464–72.CrossRefGoogle Scholar
Galione, A. & White, A. (1994). Ca++ release induced by cyclic ADP-ribose Trends Cell Biol. 4 436–6.CrossRefGoogle ScholarPubMed
Galione, A.McDougall, A.Busa, W.BWillmott, N.Gilott, I. & Whitaker, M. (1993) Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science. 261, 348–52.CrossRefGoogle ScholarPubMed
Goudeau, M. & Goudeau, H. (1993). In the egg of Phallusia mammallata, removal of external calcium modifies fertilization potential, induces polyspermy, and blocks the resumption of meiosis. Dev. Biol. 160, 165–77.CrossRefGoogle ScholarPubMed
Hille, B. (1984). Ionic Channels of Excitable Membranes. SunderlandMA: Sinauer Associates.Google Scholar
Kawahara, H. & Yokosawa, H. (1994). Intracellular calcium calcium mobilization regulates the activity of 26 S proteosome during the metaphase-anaphase transition in the ascidian cell cycle Dev. Biol. 166 623–33.CrossRefGoogle ScholarPubMed
Kiehart, D.P. (1982). Microinjection of echinoderm eggs. In Methods Cell Biol. 25 13–31.Google ScholarPubMed
Kline, D. & Kline, J.T. (1992) Thapsigargin activates a calcium influx pathway in the unfertilized mouse egg and suppresses repetitive calcium transients in the fertilized eggs. J. Biol. Chem. 267 17624–30.CrossRefGoogle Scholar
Lambert, C.C. (1989). Ascidian eggs release glycosidase activity which aids in the block against polyspermy. Development 105, 415–20.CrossRefGoogle ScholarPubMed
Lambert, C.C. & Goode, C.A. (1992.) Glycolipid linkage of a polyspermy blocking glycosidase to the ascidian egg surface. Dev. Biol. 153 95–100.CrossRefGoogle Scholar
Lambert, C.C.Gonzalez, G.P. & Millar, K.M. (1994). Independent initiation of calcium dependent glycosidase release and cortical contractions during the activation of ascidian eggs. Dev. Growth Differ. 36 133–9.CrossRefGoogle ScholarPubMed
Lee, H.C.Aarhus, R. & Walseth, T.F. (1993). Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261, 352–5.CrossRefGoogle ScholarPubMed
Marks, P.W. & Maxfield, F.R. (1990). Transient increases in cytosolic free calcium appear to be required for the migration of adherent human neutrophils. J.Cell Biol. 110 43–52.CrossRefGoogle ScholarPubMed
McDougall, A. & Sardet, C. (1995). Function and characteristics of repetitive calcium waves associated with meiosis. Curr.Biol. 5, 318–28.CrossRefGoogle ScholarPubMed
McDougall, A.D.Gillot, I. & Whitaker, M. (1993). Thimerosal reveals calcium-induced calcium release in unfertilised sea urchin eggs. Zygote 1, 35–43.CrossRefGoogle ScholarPubMed
Miyazaki, S.Katayama, Y. & Swann, K. (1990) Synergistic activation by serotonin and GTP analogue and inhibition by phorbol ester of cyclic Ca2+ rises in hamster eggs. J. physiol.(Lond) 426 209–27.CrossRefGoogle ScholarPubMed
Nuccitelli, R. (1991). How do sperm activate eggs? Curr. Top. Dev. Biol. 25 1–16.CrossRefGoogle ScholarPubMed
Nuccitelli, R.Yim, D.L. & Smart, T. (1993). The sperm induced Ca++ wave following fertilization in Xenopus eggs requires the production of Ins(1,4,5)P3 Dev. Biol. 158 200–12.CrossRefGoogle ScholarPubMed
Putney, J.W. (1993). Excitement about calcium signaling in unexcitable cells. Science 262 676–78.CrossRefGoogle Scholar
Sardet, C.Speksnijder, J.Inoué, S. & Jaffe, L. (1989). Fertilization and ooplasmic movements in the ascidian egg. Development 105 237–50.CrossRefGoogle ScholarPubMed
Speksnijder, J.Corson, D.W.Sardet, C. &Jaffe, L.F. (1989). Free calcium pulses following fertilization in the ascidian egg. Dev. Biol. 135 182–90.CrossRefGoogle ScholarPubMed
Speksnijder, J.E.Sardet, C. & Jaffe, L.F. (1990). The activation wave of calcium in the ascidian egg and its role in ooplasmic segregation. J. Cell Biol. 110 1589–98.CrossRefGoogle ScholarPubMed
Swann, K. (1991). Thimerosol causes calcium oscillations and sensitizes calcium-induced calcium release in unfertilized hamster eggs. FEBS Lett 278 175–8.CrossRefGoogle ScholarPubMed
Swann, K. & Whitaker, M. (1986). The part played by inositol trisphosphate and calcium in the propagation of the fertilization wave in sea urchins. J. Cell. Biol. 103 2333–42.CrossRefGoogle Scholar
Swann, K.McDougall, A. & Whitaker, M. (1994). Calcium signaling at fertilization J. Mar. Biol. Assoc. U.k. 74 3–16.CrossRefGoogle Scholar
Ting, A.E. & Pogano, R.E. (1990). Detection of a phosphati-dylinositol-specific phospholipase C at the surface of Swiss 3T3 cells and its potential role in the regulation of cell growth. J. Biol. chem 265 5337–40.CrossRefGoogle ScholarPubMed
Ting, A.E. & Pogano, R.E. (1991). Density dependent inhibition of cell growth is correlated with the activity of a phosphatidyl- inositol specific phospholipase C. Eur. J. Cell Biol. 56 401–6.Google Scholar
Volwerk, J.J.Birrell, G.B.Hedberg, K.K. &Griffith, O.H. (1992) A high level of cell-surface phosphatidylinositol- specific phospholipase—activity is characterristic of growth arrested 3T3 fibroblasts but not of transformed variants. J. cell. physiol. 151 613–22.CrossRefGoogle Scholar
Whitaker, M. & Swann, K. (1993). Lighting the fuse at fertilization. Development 117 1–12.CrossRefGoogle Scholar