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Calcium signalling at fertilization

Published online by Cambridge University Press:  11 May 2009

Karl Swann ,
Alex McDougall  and
Michael Whitaker
Karl Swann
Affiliation:
MRC Experimental Embryology and Teratology Unit, St George's Hospital Medical School, Cranmer Terrace, London, SW17 ORE.
Alex McDougall
Affiliation:
Department of Physiology, University College London, Gower Street, London, WC1E 6BT (address correspondence to M. Whitaker).
Michael Whitaker
Affiliation:
Department of Physiology, University College London, Gower Street, London, WC1E 6BT (address correspondence to M. Whitaker).
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Extract

It is generally agreed that fertilization in deuterostomes is accompanied by a large intracellular calcium wave that triggers the onset of development, but we still do not know exactly how the calcium wave is generated. The question has two parts: how does interaction of sperm and egg initiate the calcium wave, and how does the calcium wave spread across the cell? Two provisional answers are available to the first part of the question, one involving receptor-G-protein interactions of the sort that mediate trans-membrane signal transduction in somatic cells, the other injection of an activating messenger when sperm and egg fuse. Both these ideas are being actively pursued; the dialectic is productive, albeit no synthesis is in sight. We discuss their strengths and weaknesses. The second part of the question can now be much more precisely formulated: thanks to the recent flush of interest in calcium waves in somatic cells, new ideas and new experimental tools are available. The work on somatic cells repays a debt to eggs, where the basic properties of calcium waves were first set out, ten years before they turned up in somatic cells.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 74 , Issue 1 , February 1994 , pp. 3 - 16
Copyright
Copyright © Marine Biological Association of the United Kingdom 1994

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References

Allen, R.D. & Griffin, J.L., 1958. The time sequence of early events at fertilization of sea urchin eggs. Experimental Cell Research, 12, 163–173.CrossRefGoogle Scholar
Berridge, M.J. & Galione, A., 1988. Cytosolic calcium oscillators. FASEB Journal, 2, 3074–3082.CrossRefGoogle ScholarPubMed
Bezprovzanny, I., Watras, J. & Erlich, B.E., 1991. Bell-shaped calcium response of Ins(l,4,5)P3- and calcium-gated channels from endoplasmic reticulum. Nature, London, 351, 751–754.CrossRefGoogle Scholar
Blobel, C.P., Wolfsberg, T.G., Turck, C.W., Myles, D.G., Primakoff, P. & White, J.M., 1992. A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature, London, 356, 248–252.CrossRefGoogle Scholar
Buck, R.W., Rakow, T.L. & Shen, S.S., 1992. Synergistic release of calcium in sea urchin eggs by caffeine and ryanodine. Experimental Cell Research, 202, 59–66.CrossRefGoogle ScholarPubMed
Busa, W.B., Ferguson, J.E., Suresh, K.J., Williamson, J.R. & Nuccitelli, R., 1985. Activation of frog (Xenopus laevis) eggs by inositol trisphosphate. I. Characterization of Ca2+ release from intracellular stores. Journal of Cell Biology, 101, 677–682.CrossRefGoogle ScholarPubMed
Busa, W.B. & Nuccitelli, R., 1985. An elevated free cytosolic Ca2+ wave follows fertilization in eggs of the frog Xenopus laevis. Journal of Cell Biology, 100, 1325–1329.CrossRefGoogle ScholarPubMed
Chambers, E.L., 1989. Fertilization in voltage-clamped sea urchin eggs. In Mechanisms of egg activation (ed. R., Nuccitelliet al.), pp. 1–18. New York: Plenum Press.Google Scholar
Ciapa, B., Borg, B. & Epel, D., 1991. Polyphosphoinosites, tyrosine kinase and sea urchin egg activation. In Proceedings of the Seventh International Echinoderm Conference. Biology of the Echinodermata (ed. Y., Yanagisawaet al.), pp. 41–50. Rotterdam: A.A. Balkema.Google Scholar
Ciapa, B., Borg, B. & Whitaker, M.J., 1992. Polyphosphoinositide metabolism during the fertilization wave in sea urchin eggs. Development, 115, 187–195.CrossRefGoogle ScholarPubMed
Ciapa, B. & Whitaker, M.J., 1986. Two phases of inositol polyphosphate and diacylglycerol production at fertilization. FEBS Letters, 195, 347–351.CrossRefGoogle Scholar
Clapper, D.L., Walseth, T.F., Dargie, P.J. & Lee, H.-C., 1987. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. Journal of Biological Chemistry, 262, 9561–9568.CrossRefGoogle ScholarPubMed
Cran, D.G., Moor, R.M. & Irvine, R.F., 1988. Initiation of the cortical reaction in hamster and sheep oocytes in response to inositol trisphosphate. Journal of Cell Science, 91, 139–144.CrossRefGoogle ScholarPubMed
Crossley, I., Swann, K., Chambers, E.L. & Whitaker, M.J., 1988. Activation of sea urchin eggs by inositol phosphates is independent of external calcium. Biochemical Journal, 252, 257–262.CrossRefGoogle ScholarPubMed
Crossley, I., Whalley, T. & Whitaker, M.J., 1991. Guanosine 5'-thiotriphosphate may stimulate phosphoinositide messenger production in sea urchin eggs by a different route than the fertilizing sperm. Cell Regulation, 2, 121–133.CrossRefGoogle Scholar
Dale, B., Defelice, L.J. & Taglietti, V. 1978. Membrane noise and conductance increase during single spermatozoon-egg interactions. Nature, London, 275, 217–219.CrossRefGoogle ScholarPubMed
Endo, M., 1977. Calcium release from the sarcoplasmic reticulum. Physiological Reviews, 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. Journal of General Physiology, 85, 291–320.CrossRefGoogle ScholarPubMed
Finch, E.A., Turner, T.J. & Goldin, S.M., 1991. Calcium as a coagonist of inositol 1,4,5-trisphosphate induced calcium release. Science, New York, 252, 443–446.CrossRefGoogle ScholarPubMed
Florman, H.M., Tombes, R.M., First, N.L. & Babcock, D.F., 1989. An adhesion-associated agonist from the zona pellucida activates G protein-promoted elevations of intracellular calcium and pH that mediate mammalian sperm acrosomal exocytosis. Developmental Biology, 135, 133–146.CrossRefGoogle ScholarPubMed
Foltz, K.R. & Lennarz, W.J., 1990. Purification and characterization of an extracellular fragment of the sea urchin receptor for sperm. Journal of Cell Biology, 111, 2951–2959.CrossRefGoogle ScholarPubMed
Foltz, K.R. & Lennarz, W.J., 1992. Identification of the sea urchin egg receptor for sperm using an antiserum raised against a fragment of its extracellular domain. Journal of Cell Biology, 116, 647–658.CrossRefGoogle ScholarPubMed
Foltz, K.R., Partin, J.S. & Lennarz, W.J., 1993. Sea urchin egg receptor for sperm: sequence similarity of binding domain and hsp70. Science, New York, 259, 1421–1425.CrossRefGoogle ScholarPubMed
Fujiwara, A., Taguchi, K. & Yasumasu, I., 1990. Fertilization membrane formation in sea urchin eggs induced by drugs known to cause Ca2+ release from isolated sarcoplasmic reticulum. Development, Growth and Differentiation, 32, 303–314.CrossRefGoogle ScholarPubMed
Furuichi, T., Yoshikawa, S., Miyawaki, A., Wada, K., Maeda, N. & Mikoshiba, K., 1989. Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature, London, 342, 32–38.CrossRefGoogle ScholarPubMed
Galione, A., 1992. Calcium-induced calcium release and its modulation by cyclic ADP-ribose. Trends in Pharmacological Science, 13, 304–307.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, New York, 253, 1143–1146.CrossRefGoogle Scholar
Galione, A., McDougall, A., Busa, W.B., Willmott, N., Gillot, I. & Whitaker, M.J., 1993. Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science, New York, 261, 348–352.CrossRefGoogle ScholarPubMed
Ghosh, T.R., Mullaney, G.M., Terazi, F.I. & Gill, D.L., 1989. GTP-activated communication between distinct inositol 1,4,5-trisphosphate-sensitive and -insensitive calcium pools. Nature, London, 340, 236–239.CrossRefGoogle ScholarPubMed
Glabe, C.G., 1985a. Interaction of the sperm adhesive protein, bindin, with phospholipid vesicles. I. Specific association of bindin with gel-phase phospholipid vesicles. Journal of Cell Biology, 100, 794–799.CrossRefGoogle ScholarPubMed
Glabe, C.G., 1985b. Interaction of the sperm adhesive protein, bindin, with phospholipid vesicles. II. Bindin induces the fusion of mixed-phase vesicles that contain phosphatidykholine and phosphatidylserine in vitro. Journal of Cell Biology, 100, 800–806.CrossRefGoogle ScholarPubMed
Glabe, C.G., Hong, K. & Vacquier, V.D., 1991. Fusion of sperm and egg plasma membranes during fertilization. In Membrane fusion (ed. I., Wilschut and D., Hoekstra), pp. 627–646. New York: Dekker.Google Scholar
Henson, J.H., Beaulieu, S.M., Kaminer, B. & Begg, D.A., 1990. Differentiation of a calsequestrin-containing endoplasmic reticulum during sea urchin oogenesis. Developmental Biology, 142, 255–269.CrossRefGoogle ScholarPubMed
Henson, J.H., Begg, D.A., Beaulieu, S.M., Fishkind, D.J., Bonder, E.M., Terasaki, M., Lebeche, D. & Kaminer, B., 1989. A calsequestrin-like protein in the endoplasmic reticulum of the sea urchin: localization and dynamics in the egg and first cell embryo. Journal of Cell Biology, 109, 149–161.CrossRefGoogle Scholar
Hinckley, R.E., Wright, B.D. & Lynn, J.W., 1986. Rapid visual detection of sperm-egg fusion using the DNA-specific fluorochrome Hoechst 33342. Developmental Biology, 118, 148–154.CrossRefGoogle Scholar
Igusa, Y. & Miyazaki, S., 1983. Effects of altered extracelluar and intracellular calcium concentration on hyperpolarizing responses of hamster egg. Journal of Physiology, 340, 611–632.CrossRefGoogle Scholar
Igusa, Y., Miyazaki, S. & Yamashita, N., 1983. Periodic hyperpolarizing responses in hamster and mouse eggs fertilized with mouse sperm. Journal of Physiology, 340, 643–647.CrossRefGoogle ScholarPubMed
Iwasa, K.H., Ehrenstein, G., Defelice, L.J. & Russell, J.T., 1990. High concentrations of inositol 1,4,5-trisphosphate in sea urchin sperm. Biochemical and Biophysical Research Communications, 172, 932–938.CrossRefGoogle ScholarPubMed
Jacob, R., 1990. Calcium oscillations in electrically non-excitable cells. Biochimica et Biophysica Acta, 1052, 427–458.CrossRefGoogle ScholarPubMed
Jaconi, M.E.E., Theler, J.M., Schlegel, W., Appel, R.D., Wright, S.D. & Lew, P.D., 1991. Multiple elevations of cytosolic free Ca2+ in human neutrophils: initiation by adherence receptors of the integrin family. Journal of Cell Biology, 112, 1249–1257.CrossRefGoogle ScholarPubMed
Jaffe, L.A., 1976. Fast block to polyspermy in sea urchin eggs is electrically mediated. Nature, London, 261, 68–71.CrossRefGoogle ScholarPubMed
Jaffe, L.A., Sharp, A.P. & Wolf, D.P., 1983. Absence of an electrical block to polyspermy in the mouse. Developmental Biology, 96, 317–323.CrossRefGoogle ScholarPubMed
Jaffe, L.A., Turner, P.R., Kline, D., Kado, R.T. & Shilling, F., 1988. G-proteins and egg activation. Cell Differentiation and Development, Supplement 25, 15–18.CrossRefGoogle ScholarPubMed
Jaffe, L.F., 1980. Calcium explosions as triggers of development. Annals of the New York Academy of Sciences, 339, 86–101.CrossRefGoogle ScholarPubMed
Jaffe, L.F., 1983. Sources of calcium in egg activation: a review and hypothesis. Developmental Biology, 99, 265–276.CrossRefGoogle ScholarPubMed
Jaffe, L.F., 1990. The roles of intermembrane calcium in polarizing and activating eggs. In Mechanisms of fertilization: plants to humans (ed. B., Dale), pp. 389–417. Berlin: Springer Verlag. [Nato ASI Series H, Cell Biology 45.]CrossRefGoogle Scholar
Jaffe, L.F., 1991. The path of calcium in cytosolic calcium oscillations: a unifying hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 88, 9883–9887.CrossRefGoogle ScholarPubMed
Kline, D. & Kline, J.T., 1992. Effects of microinjection of inositol 1,4,5-trisphosphate on the repetitive calcium transients and the role of calcium in exocytosis and cell cycle control in the mouse egg. Developmental Biology, 145, 80–89.CrossRefGoogle Scholar
Kline, D., Kopf, G.S., Muncy, L.F. & Jaffe, L.A., 1991. Evidence for the involvement of a pertussis toxin-insensitive G-protein in egg activation of the frog, Xenopus laevis. Developmental Biology, 143, 218–229.CrossRefGoogle ScholarPubMed
Kline, D., Simoncini, L., Mandel, G., Maue, R.A., Kado, R.T. & Jaffe, L.A., 1988. Fertilization events induced by neurotransmitters after injection of mRNA in Xenopus eggs. Science, New York, 241, 464–467.CrossRefGoogle ScholarPubMed
Kopf, G.S., Tubb, D.J., & Garbers, D.L., 1979. Activation of sperm respiration by a low molecular weight egg factor and by 8-bromoguanosine 3',5'-monophosphate. Journal of Biological Chemistry, 254, 8554–8560.CrossRefGoogle ScholarPubMed
Kornberg, L.J., Earp, H.S., Turner, C.E., Prokop, C. & Juliano, R.L., 1991. Signal transduction by integrins: increased protein phosphorylation caused by clustering of β1, integrins. Proceedings of the National Academy of Sciences of the United States of America, 88, 8392–8396.CrossRefGoogle Scholar
Kurasawa, S., Schultz, R.M. & Kopf, G.S., 1989. Egg-induced modifications of the zona pellucida of mouse eggs: effects of microinjected inositol 1,4,5-trisphosphate. Developmental Biology, 133, 295–304.CrossRefGoogle ScholarPubMed
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, London, 331, 315–319.Google ScholarPubMed
Lechleiter, J.D. & Clapham, D.E., 1992. Molecular mechanisms of intracellular calcium excitability in Xenopus laevis oocytes. Cell, 69, 283–294.CrossRefGoogle Scholar
Lee, H.C., Aarhus, R. & Walseth, T.F., 1993. Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science, New York, 261, 352–355.CrossRefGoogle 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. Journal of Biological Chemistry, 264, 1608–1615.CrossRefGoogle ScholarPubMed
Loeb, J., 1913. Artificial parthenogenesis and fertilization. Chicago: University of Chicago Press.Google Scholar
Longo, F.J., 1978. Effects of cytochalasin B on sperm-egg interactions. Developmental Biology, 67, 249–265.CrossRefGoogle ScholarPubMed
Longo, F., Cook, S., McCulloh, D., Ivonnet, P. & Chambers, E.L., 1990. Gamete interaction and the initiation of egg activation in sea urchins. In Mechanisms of fertilization: plants to humans (eDale, D. B.), pp. 389–417. Berlin: Springer Verlag. [Nato ASI Series H, Cell Biology 45.]Google Scholar
Longo, F.J., Lynn, J.W., McCulloh, D.H. & Chambers, E.L., 1986. Correlative ultrastructural and electrophysiological studies of sperm-egg interactions of the sea urchin, Lytechnus variegatus. Developmental Biology, 118, 155–166.CrossRefGoogle ScholarPubMed
Lopez, A., Miraglia, S.J. & Glabe, C.G., 1993. Structure/function analysis of the sea urchin sperm adhesive protein bindin. Developmental Biology, 156, 24–33.CrossRefGoogle ScholarPubMed
Lorca, T., Galas, S., Fesquet, D., Devault, A., Cavadore, J.C. & Doree, M., 1991. Degradation of the proto-oncogene product p38mos is not necessary for cyclin proteolysis and exit from meiotic metaphase: requirement for a Ca2+-calmodulin dependent event. EMBO Journal, 10, 2087–2093.CrossRefGoogle Scholar
McCulloh, D.H. & Chambers, E.L., 1992. Fusion of membranes during fertilization: increases of sea urchin egg's membrane capacitance and membrane conductance at the site of contact with the sperm. Journal of General Physiology, 99, 137–175.CrossRefGoogle ScholarPubMed
McCulloh, D.H., Ivonnet, P.I. & Chambers, E.L., 1989. Blockers of Ca influx promote sperm entry in sea urchin eggs at clamped negative membrane potentials. Journal of Cell Biology, 109, 126a.Google Scholar
McCulloh, D.H., Ivonnet, P.I. & Chambers, E.L., 1990. Microinjection of a Ca2+ chelator, EGTA and BAPTA promotes sperm entry in sea urchin eggs clamped at negative potentials. Journal of Cell Biology, 111, 113a.Google Scholar
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. Journal of Cell Biology, 116, 1111–1121.CrossRefGoogle ScholarPubMed
Mignery, G.A., Südhof, T.C., Takei, K. & De Camilli, P., 1989. Putative receptor for inositol 1,4,5-trisphosphate similar to ryanodine receptor. Nature, London, 342, 192–195.CrossRefGoogle ScholarPubMed
Missiaen, L., Taylor, C.W. & Berridge, M.J., 1991. Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores. Nature, London, 352, 241–244.CrossRefGoogle ScholarPubMed
Miyazaki, S., 1988. Inositol 1,4,5-trisphosphate-induced calcium release and guanine nucleotide-binding protein-mediated periodic calcium rises in golden hamster eggs. Journal of Cell Biology, 106, 345–353.CrossRefGoogle ScholarPubMed
Miyazaki, S., Hashimoto, N., Yoshimoto, Y., Kishimoto, T., Igusa, Y. & Hiramoto, Y., 1986. Temporal and spatial dynamics of the periodic increase in intracellular calcium at fertilization of golden hamster eggs. Developmental Biology, 118, 259–267.CrossRefGoogle ScholarPubMed
Miyazaki, S. & Igusa, Y., 1981. Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations. Nature, London, 290, 706–707.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. Journal of Physiology, 426, 209–227.CrossRefGoogle ScholarPubMed
Miyazaki, S., Shirakawa, H., Nakada, K. & Honda, Y., 1993. Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilization of mammalian eggs. Developmental Biology, 158, 62–78.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, New York, 257, 251–255.CrossRefGoogle Scholar
Parys, J.B., Sernett, S.W., Delisle, S., Snyder, P.M., Welsh, M.J. & Campbell, K.P., 1992. Isolation, characterization and localization of the inositol 1,4,5-trisphosphate receptor protein in Xenopus laevis oocytes. Journal of Biological Chemistry, 267, 18776–18782.CrossRefGoogle ScholarPubMed
Rakow, T.L. & Shen, S.S., 1990. Multiple stores of calcium are released in the sea urchin egg during fertilization. Proceedings of the National Academy of Sciences of the United States of America, 87, 9285–9289.CrossRefGoogle ScholarPubMed
Rhee, S.G., 1991. Inositol phospholipids-specific phospholipase C: interaction of the gamma isoform with tyrosine kinase. Trends in Biochemical Science, 16, 297–301.CrossRefGoogle ScholarPubMed
Ross, C.A., Meldolesi, J., Milner, T.A., Satoh, T., Supattopone, S. & Snyder, S.H., 1989. Inositol 1,4,5-trisphosphate receptor localised to endoplasmic reticulum in cerebellar Purkinje neurones. Nature, London, 339, 468–470.CrossRefGoogle Scholar
Sardet, C, Gillot, I., Ruscher, A., Payan, P., Girard, J.-P. & Renzis, G. De, 1992. Ryanodine activates sea urchin eggs. Development, Growth and Differentiation, 34, 37–42.CrossRefGoogle ScholarPubMed
Schackmann, R.W., 1989. Ionic regulation of the sea urchin sperm acrosome reaction and stimulation by egg-derived peptides. In The cell biology of fertilization (ed. Schatten, H. and Schatten, G.). San Diego: Academic Press.Google Scholar
Sealfon, S.C., Mundamattom, S. & Gillo, B., 1990. Modulation of calcium mobilization by guano-sine 5'-O-(2-thiodiphosphate) in Xenopus oocytes. FEBS Letters, 269, 135–138.CrossRefGoogle ScholarPubMed
Shen, S.S. & Steinhardt, R. A., 1984. Time and voltage windows for reversing the electrical block to fertilization. Proceedings of the National Academy of Sciences of the United States of America, 81, 1436–1439.CrossRefGoogle ScholarPubMed
Shilling, F., Chiba, K., Hoshi, M., Kishimoto, T. & Jaffe, L.A., 1989. Pertussis toxin inhibits 1-methyladenine-induced maturation in starfish oocytes. Developmental Biology, 133, 605–608.CrossRefGoogle ScholarPubMed
Shilling, F., Mandel, G. & Jaffe, L.A., 1990. Activation by serotonin of starfish eggs expressing the rat serotonin lc receptor. Cell Regulation, 1, 465–469.CrossRefGoogle Scholar
Steinhardt, R.A., Epel, D., Caroll, E.J. & Yanagimachi, R., 1974. Is calcium ionophore a universal activator for unfertilised eggs? Nature, London, 252, 41–43.CrossRefGoogle ScholarPubMed
Südhof, T.C., Newton, C.L., Archer, B.T. III, Ushkaryov, Y.A. & Mignery, G.A., 1991. Structure of a novel InsP3 receptor. EMBO Journal, 10, 3199–3206.CrossRefGoogle ScholarPubMed
Swann, K., 1990. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development, 110, 1295–1302.CrossRefGoogle ScholarPubMed
Swann, K., 1991. Thimerosal causes calcium oscillations and sensitizes calcium-induced calcium release in unfertilized hamster eggs. FEBS Letters, 278, 175–178.CrossRefGoogle ScholarPubMed
Swann, K., 1992. Different triggers for Ca2+ oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochemical Journal, 287, 79–84.CrossRefGoogle ScholarPubMed
Swann, K., Igusa, I. & Miyazaki, S., 1989. Evidence for an inhibitory effect of protein kinase C on G-protein-mediated repetitive calcium transients in hamster eggs. EMBO Journal, 8, 3711–3718.CrossRefGoogle ScholarPubMed
Swann, K., McCulloh, D.H., McDougall, A., Chambers, E.L. & Whitaker, M.J., 1992. Sperm-induced currents at fertilization in sea urchin eggs injected with EGTA and neomycin. Developmental Biology, 151, 552–563.CrossRefGoogle ScholarPubMed
Swann, K. & Whitaker, M.J., 1986. The part played by inositol trisphosphate and calcium in the propagation of the fertilization wave in sea urchin eggs. Journal of Cell Biology, 103, 2333–2342.CrossRefGoogle ScholarPubMed
Swann, K. & Whitaker, M.J., 1990. Second messengers at fertilization in sea-urchin eggs. Journal of Reproduction and Fertilization, Supplement, 42, 141–153.Google ScholarPubMed
Takeshima, H., et al., 1989. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature, London, 339, 439–445.CrossRefGoogle ScholarPubMed
Terasaki, M., Henson, J., Begg, D., Kaminer, B. & Sardet, C, 1991. Characterization of sea urchin egg endoplasmic reticulum in cortical preparations. Developmental Biology, 148, 398–401.CrossRefGoogle ScholarPubMed
Terasaki, M. & Sardet, C, 1991. Demonstration of calcium uptake and release by sea urchin egg cortical endoplasmic reticulum. Journal of Cell Biology, 115, 1031–1037.CrossRefGoogle ScholarPubMed
Turner, P.R., Jaffe, L.A. & Fein, A., 1986. Regulation of cortical granule exocytosis by inositol 1,4,5-trisphosphate and GTP binding protein. Journal of Cell Biology, 102, 70–76.CrossRefGoogle ScholarPubMed
Turner, P.R., Jaffe, L.A. & Primakoff, P., 1987. A cholera-toxin sensitive G-protein stimulates exocytosis in sea urchin eggs. Developmental Biology, 120, 577–583.CrossRefGoogle ScholarPubMed
Turner, P.R., Sheetz, M.P. & Jaffe, L.A., 1984. Fertilization increases the polyphosphoinositides content of sea urchin eggs. Nature, London, 310, 414–415.CrossRefGoogle ScholarPubMed
Whalley, T., McDougall, A., Crossley, I., Swann, K. & Whitaker, M.J., 1992. Internal calcium release and activation of sea urchin eggs by cGMP are independent of the phosphoinositide signalling pathway. Molecular Biology of the Cell, 3, 373–383.CrossRefGoogle Scholar
Whitaker, M.J. & Aitchison, M.J., 1985. Calcium-dependent polyphosphoinositide hydrolysis is associated with exocytosis in vitro. FEBS Letters, 182, 119–124.CrossRefGoogle ScholarPubMed
Whitaker, M.J. & Irvine, R.F., 1984. Micro-injection of inositol trisphosphate activates sea urchin eggs. Nature, London, 312, 636–638.CrossRefGoogle Scholar
Whitaker, M.J. & Patel, R., 1990. Calcium and cell cycle control. Development, 108, 525–542.CrossRefGoogle ScholarPubMed
Whitaker, M.J. & Steinhardt, R.A., 1982. Ionic regulation of egg activation. Quarterly Reviews of Biophysics, 15, 593–666.CrossRefGoogle ScholarPubMed
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. 159–163. New York: Plenum Press.Google Scholar
Williams, C.J., Schultz, R.M. & Kopf, G.S., 1992. Role of G-proteins in mouse egg activation: stimulatory effects of acetyl choline on the ZP2 to ZP2f conversion and pronuclear formation in eggs expressing a functional ml muscarinic receptor. Developmental Biology, 151, 288–296.CrossRefGoogle Scholar