Hostname: page-component-745bb68f8f-hvd4g Total loading time: 0 Render date: 2025-01-14T19:15:02.912Z Has data issue: false hasContentIssue false
  • English
  • Français

Thimerosal reveals calcium-induced calcium release in unfertilised sea urchin eggs

Published online by Cambridge University Press:  26 September 2008

Alex McDougall ,
Isabelle Gillot  and
Michael Whitaker
Alex McDougall
Affiliation:
Department of Physiology, University College, London, London, UK
Isabelle Gillot
Affiliation:
Department of Physiology, University College, London, London, UK
Michael Whitaker*
Affiliation:
Department of Physiology, University College, London, London, UK
*
Michael Whitaker, Department of Physiology, University College London, Gower Street, London WC1E 6BT, UK. Telephone: +44 71 388 9304. Fax: +44 71 388 3892.
Get access Rights & Permissions [Opens in a new window]

Summary

The fertilisation calcium wave in sea urchin eggs triggers the onset of development. The wave is an explosive increase in intracellular free calcium concentration that begins at the point of sperm entry and crosses the egg in about 20 s. Thimerosal is a sulphydryl reagent that sensitises calcium release from intracellular stores in a variety of cell types. Treatment of unfertilised eggs with thimerosal causes a slow increase that results eventually in a large, spontaneous calcium transient and egg activation. At shorter times after thimerosal treatment, egg activation and the calcium transient can be triggered by calcium influx through voltage-gated calcium channels, a form of calcium-induced/calcium release (CICR). Thimerosal treatment also reduces the latency of the fertilisation calcium response and increases the velocity of the fertilisation wave. These results indicate that thimerosal can unmask CICR in sea urchin eggs and suggest that the ryanodine receptor channel based CICR may contribute to explosive calcium release during the fertilisation wave.

Keywords

Calcium waveCalcium-induced calcium release (CICR)FertilisationInositol trisphosphate receptorRyanodine receptor
Type
Article
Information
Zygote , Volume 1 , Issue 1 , February 1993 , pp. 35 - 42
Copyright
Copyright © Cambridge University Press 1993

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

Berridge, M.J. & Galione, A.. (1988). Cytosolic calcium oscillators.FASEB J. 2, 3074–82.CrossRefGoogle ScholarPubMed
Bezprovzanny, I., Watras, J. & Erlich, B.E. (1991). Bell-shaped calcium response of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum. Nature 351, 751–4.CrossRefGoogle Scholar
Buck, R.W., Rakow, T.L. & Shen, S.S. (1992). Synergistic release of calcium in sea urchin eggs by caffeine and ryanodine. Exp. Cell Res. 202, 59–66.CrossRefGoogle ScholarPubMed
Chambers, E.L. & de Armendi, J.. (1979). Membrane potential, action potential and activation potential of the eggs of the sea urchin Lytechinus variegatus. Exptl Cell Res. 126, 333–342.Google Scholar
Chambers, E.L. & Hinckley, R.E. (1979). Non-propagative cortial reactions induced by the divalent ionophore A23187 in the eggs of the sea urchin Lytechninus variegatus. Exp. Cell Res. 124, 441–6.CrossRefGoogle Scholar
Ciapa, B., Borg, B. & Whitaker, M.J. (1992). Polyphosphoinositide metabolism during the fertilization wave in sea urchin eggs. Development 115, 187–95.CrossRefGoogle ScholarPubMed
Crossley, I., Whalley, T. & Whitaker, M.J. (1991). Guanosine 5-thiotriphosphate may stimulate phophoinositide messenger production in sea urchin eggs by a different route than the fertilizing sperm Cell Regulation 2, 121–33.CrossRefGoogle Scholar
David, C., Halliwell, J. & Whitaker, M.J. (1988). Some properties of the membrane currents underlying the fertilization potential in sea urchin eggs. J. Physiol. (Lond). 402, 139–54.CrossRefGoogle ScholarPubMed
Endo, M.. (1977). Calcium release from the sarcoplasmic reticulum. Physiol. Rev. 57, 71–108.CrossRefGoogle ScholarPubMed
Fabiato, A. (1985). Stimulated calcium current can both cause calcium loading in and trigger calcium release from the sarcoplasmic reticulum of a skinned cardiac Purkinje cell. J. Gen. Physiol. 85, 291–320.CrossRefGoogle ScholarPubMed
Finch, E.A., Turner, T.J. & Goldin, S.M. (1991). Calcium as a coagonist of inositol 1,4,5-triphosphate induced calcium release. Science 252, 443–6.CrossRefGoogle ScholarPubMed
Furuichi, T., Yoshikawa, S., Miyawaki, A., Wada, K., Maeda, N. & Mikoshiba, K.(1980). Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature 342, 32–8.CrossRefGoogle Scholar
Galione, A. (1992). Calcium-induced calcium release and its modulation by cyclic ADP-ribose. Trends Pharmacol. Sci. 13, 304–6.CrossRefGoogle Scholar
Galione, A., Lee, H.C. & Busa, W.B. (1991). Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253, 1143–6.CrossRefGoogle Scholar
Hamaguchi, Y. & Kuriyama, R. (1982). Aster formation in sand dollar eggs by microinjection of calcium buffers Exptl Cell Res. 141, 450–54.CrossRefGoogle ScholarPubMed
Hatzelman, A., Haurand, M. & Ullrich, V. (1990). Involvement of calcium in the thimerosal-stimulated formation of leukotriene by fMLP in human polymorphonuclear leukocytes. Biochem. Pharmacol. 39, 559–67.CrossRefGoogle Scholar
Hecker, M., Brüner, B., Decker, K. & Ullrich, V. (1989). The sulphydryl reagent thimerosal elicits human platelet aggregation by mobilization of intracellular calcium and secondary prostaglandin endoperoxide formation. Biochem. Biophys. Res. Commun. 159, 961–8.CrossRefGoogle ScholarPubMed
Hill, T.D., Berggren, P. & Boynton, A.L. (1987). Heparin inhibits inositol trisphosphate–induced calcium release from permeabilized rat liver cells. Biochem. Biophys. Res. Commun. 149, 870–901.CrossRefGoogle ScholarPubMed
Igusa, Y. & Miyazaki, S. (1983). Effects of altered extracellular and intracellular calcium concentration on hyperpolarizing responses of hamster egg. J. Physiol. (Lond.) 340, 611–;32.CrossRefGoogle ScholarPubMed
Islam, M.S., Rorsman, P. & Beggren, P.O. (1992). Ca2+-induced Ca2+-release in insulinsecreting cells. FEBS Lett. 296, 287–91.CrossRefGoogle Scholar
Jacob, R. (1990). Calcium oscillations in electrically nonexcitable cells. Biochim. Biophys. Acta 1052, 427–58.CrossRefGoogle Scholar
Jaffe, L.F. (1983). Sources of calcium in egg activation: a review and hypothesis. Dev. Biol. 99, 256–76.CrossRefGoogle ScholarPubMed
Kacser, H. (1955). The cortical changes on fertilization in the sea urchin egg. J. Exp. Biol. 32, 451–67.CrossRefGoogle Scholar
Lai, F.A., Erickson, H.P., Rousseau, E., Lin, Q.Y. & Meissner, G. (1988). Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331, 315–19.Google ScholarPubMed
Lee, H.C., Walseth, T.F., Bratt, G.T., Hayes, R.N. & Clapper, D.L. (1989). Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity. J. Biol. Chem. 264, 1608–;15.CrossRefGoogle ScholarPubMed
McPherson, S.M., McPherson, P.S., Matthews, L., Campbell, K.P. & Longo, F.J. (1992). Cortical localization of calcium release channel in sea urchin eggs. J. Biol. 116 1111–21.Google ScholarPubMed
Meyer, T. & Stryer, L. (1988). Molecular model for receptor stimulated calcium spiking. Proc. Natl. Acad. Sci. USA 85, 5051–5.CrossRefGoogle ScholarPubMed
Mignery, G.A., Sūdhof, T.C., Takei, K. & De Camilli, P.(1989). Putative receptor for inositol, 1,4,5-trisphosphate similar ryanodine receptor. Nature 342, 192–5.CrossRefGoogle ScholarPubMed
Missiaen, L., Taylor, C.W. & Berridge, M.J. (1991). Spontaneous calcium release from inositol trisphosphatesensitive calcium stores. Nature 352, 241–2.CrossRefGoogle ScholarPubMed
Miyazaki, S., Yuzaki, M., Nakada, K., Shirakawa, H., Nakanishi, S., Nakade, S. & Mikoshiba, K.. (1992).Block of Ca2+ wave and Ca2+ oscillation by antibody to the IP3 receptor in fertilized hamster eggs. Science 257, 251–5.CrossRefGoogle Scholar
Sardet, C., Gillot, I., Ruscher, A., Payan, P., Girard, J.P & de Renzis, G. (1992). Ryanodine activates sea urchin eggs. Devi. Growth Differ. 34, 37–42.CrossRefGoogle ScholarPubMed
Swann, K. (1991). Thimerosal causes calcium oscillations and sensitizes calcium-induced calcium release in unfertilized hamster eggs. FEBS Lett. 278, 175–178.CrossRefGoogle ScholarPubMed
Swann, K.S. & Whitaker, M.J. (1986). The part played by inositol trisphosphate and calcium in the propagation of the fertilization wave in sea urchin eggs. J. Cell Biol. 103, 2333–42.CrossRefGoogle ScholarPubMed
Turner, P.R., Sheetz, M.P. & Jaffe, L.A. (1984).Fertilization increases the polyphosphoinositide content of sea urchin eggs. Nature 310, 414–15.CrossRefGoogle ScholarPubMed
Whitaker, M.J. & Aitchison, M.J. (1985). Calcium-dependent polyphosphoinositide hydrolysis is associated with exocytosis in vitro. FEBS Lett. 182, 119–24.CrossRefGoogle ScholarPubMed
Whitaker, M.J. & Irvine, R.F. (1984). Micro-injection of inositol trisphosphate activates sea urchin eggs. Nature 312, 636–8.CrossRefGoogle Scholar
Whitaker, M.J. & Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 1–12.CrossRefGoogle Scholar
Whitaker, M.J., Swann, K. & Crossley, I.B. (1989). What happens during the latent period at fertilization in sea urchin eggs. In: Mechanisms of Egg Activation, ed. Nuccitelli, R., pp. 159–63. New York: Plenum Press.Google Scholar
Wilson, W.A. & Goldner, M.M. (1975). Voltage clamping with a single microelectrode. J. Neurobiol. 6, 411–22.CrossRefGoogle ScholarPubMed