Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-26T15:14:16.058Z Has data issue: false hasContentIssue false
  • English
  • Français

Cortical granule exocytosis is triggered by different thresholds of calcium during fertilisation in sea urchin eggs

Published online by Cambridge University Press:  15 January 2010

John C. Matese  and
David R. McClay
John C. Matese
Affiliation:
Zoology Department, Duke University, Durham, North Carolina, USA
David R. McClay*
Affiliation:
Zoology Department, Duke University, Durham, North Carolina, USA
*
D.R. McClay, Developmental, Cell and Molecular Biology Program, Zoology Department, Box 91000, Levine Science Research Building, Duke University, Durham, North Carolina 27708-1000, USA. Telephone: +1 (919) 613-8188. Fax: +1 (919) 613-8177. e-mail: dmcclay@duke.edu.
Get access Rights & Permissions [Opens in a new window]

Summary

In sea urchin eggs, fertilisation is followed by a calcium wave, cortical granule exocytosis and fertilisation envelope elevation. Both the calcium wave and cortical granule exocytosis sweep across the egg in a wave initiated at the point of sperm entry. Using differential interference contrast (DIC) microscopy combined with laser scanning confocal microscopy, populations of cortical granules undergoing calcium-induced exocytosis were observed in living urchin eggs. Calcium imaging using the indicator Calcium Green-dextran was combined with an image subtraction technique for visual isolation of individual exocytotic events. Relative fluorescence levels of the calcium indicator during the fertilisation wave were compared with cortical fusion events. In localised regions of the egg, there is a 6s delay between the detection of calcium release and fusion of cortical granules. The rate of calcium accumulation was altered experimentally to ask whether this delay was necessary to achieve a threshold concentration of calcium to trigger fusion, or was a time-dependent activation of the cortical granule fusion apparatus after the ‘triggering’ event. Calcium release rate was attenuated by blocking inositol 1,4,5-triphospate (InsP3)-gated channels with heparin. Heparin extended the time necessary to achieve a minimum concentration of calcium at the sites of cortical granule exocytosis. The data are consistent with the conclusion that much of the delay observed normally is necessary to reach threshold concentration of calcium. Cortical granules then fuse with the plasma membrane. Further, once the minimum threshold calcium concentration is reached, cortical granule fusion with the plasma membrane occurs in a pattern suggesting that cortical granules are non-uniform in their calcium sensitivity threshold.

Keywords

CalciumCortical granulesExocytosisFertilisation reactionUrchin
Type
Research Article
Information
Zygote , Volume 6 , Issue 1 , February 1998 , pp. 55 - 63
Copyright
Copyright © Cambridge University Press 1998

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

Anderson, E. (1968). Oocyte differentiation in the sea urchin, Arbacia punctulata, with particular reference to the origin of cortical granules and their participation in the cortical reaction. J. Cell Biol. 37, 514–39.CrossRefGoogle Scholar
Augustine, G.J., Burns, M.E., De Bello, W.M., Pettit, D.L. & Schweizer, F.E. (1996). Exocytosis: proteins and pertubations. Annu Rev. Pharmacol. Toxicol. 36, 659–701.CrossRefGoogle Scholar
Baker, P.F. & Whitaker, M.J. (1978). Influence of ATP and calcium on the cortical reaction in sea urchin eggs. Nature, 276, 513–15.CrossRefGoogle ScholarPubMed
Berg, L.K. & Wessel, G.M. (1997). Cortical granules of the sea urchin translocate early in oocyte maturation. Development 124, 1845–50.CrossRefGoogle ScholarPubMed
Bi, G.Q., Alderton, J.M. & Steinhardt, R.A. (1995). Calcium-regulated exocytosis is required for cell membrane resealing. J. Cell Biol. 131, 1747–58.CrossRefGoogle ScholarPubMed
Buck, W.R., Hoffmann, E.E., Rakow, T.L. & Shen, S.S. (1994). Synergistic calcium release in the sea urchin egg by ryanodine and cyclic ADP ribose. Dev. Biol. 163, 1–10.CrossRefGoogle ScholarPubMed
Calakos, N. & Scheller, R.H. (1996). Synaptic vesicle biogenesis, docking, and fusion: a molecular description. Physiol. Rev. 76, 1–29.CrossRefGoogle ScholarPubMed
Conner, S., Leaf, D. & Wessel, G. (1997). Members of the snare hypothesis are associated with cortical granule exocytosis in the sea urchin egg. Mol. Reprod. Dev. 48, 106–118.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
De Bello, W.M., Betz, H. & Augustine, G.J. (1993). Synapto-tagmin and neurotransmitter release. Cell 74, 947–50.CrossRefGoogle ScholarPubMed
Eisen, A., Kiehart, D.P., Wieland, S.J. & Reynolds, G.T. (1984). Temporal sequence and spatial distribution of early events of fertilization in single sea urchin eggs. J. Cell Biol. 99, 1647–54.CrossRefGoogle ScholarPubMed
Gallone, 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
Galione, A., McDougall, A., Busa, W.B., Willmott, N., Gillot, 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
Hafner, M., Petzelt, C., Nobiling, R., Pawley, J.B., Kramp, D. & Schatten, G. (1988). Wave of free calcium at fertilization in the sea urchin egg visualized with fura-2. Cell Motil. Cytoskel. 9, 271–7.CrossRefGoogle ScholarPubMed
Hamaguchi, Y. & Hamaguchi, M.S. (1990). Simultaneous investigation of intiacellular Ca2+ increase and morphological events upon fertilization in the sand dollar egg. Cell Struct. Fund. 15, 159–62.CrossRefGoogle ScholarPubMed
Hamaguchi, Y. & Hiramoto, Y. (1981). Activation of sea urchin eggs by microinjection of calcium buffers. Exp. Cell Res. 134, 171–9.CrossRefGoogle ScholarPubMed
Horne, J.H. & Meyer, T. (1997). Elementary calcium-release units induced by inositol trisphosphate. Science 276, 1690–3.CrossRefGoogle ScholarPubMed
Kreimer, D.I. & Khotimchenko, Y.S. (1995). Cytoplasm calcium-binding proteins of germ cells and embryos of the sea urchin. Comp. Biochem. Physiol. Physiol. 110, 95–105.CrossRefGoogle ScholarPubMed
Laidlaw, M. & Wessel, G.M. (1994). Cortical granule biogenesis is active throughout oogénesis in sea urchins. Development 120, 1325–33.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
Llinas, R., Sugimori, M. & Silver, R.B. (1992). Microdomains of high calcium concentration in a presynaptic terminal. Science 256, 677–9.CrossRefGoogle Scholar
Lucio, J., D'Brot, J., Guo, D.B., Abraham, W.M., Lichtenstein, L.M., Kagey-Sobotka, A. & Ahmed, T. (1992). Immunologie mast cell-mediated responses and histamine release are attenuated by heparin. J. Appl. Physiol. 73, 1093–101.CrossRefGoogle ScholarPubMed
Matese, J.C. & McClay, D.R. (1994). Dynamics of cortical granule fusion and their relationship to the calcium wave following fertilization of sea urchin eggs. Mol. Biol. Cell 5 (Suppl.), 445A.Google Scholar
Matese, J.C. & McClay, D.R. (1996). Heparin modulation of the post-fertilization calcium release changes cortical granule exocytosis dynamics. Mol. Biol. Cell 7 (Suppl.), 609A.Google Scholar
Matese, J.C., Black, S. & McClay, D.R. (1997). Regulated exocytosis and sequential construction of the extracellular matrix surrounding the sea urchin zygote. Dev. Biol. 186, 16–26.CrossRefGoogle ScholarPubMed
Matthews, G. (1996). Neurotransmitter release. Annu. Rev. Neurol. 19, 219–33.CrossRefGoogle ScholarPubMed
Mazia, D. (1937). The release of calcium in Arbacia eggs on fertilization, J. Cell Comp. Physiol. 10, 291–304.CrossRefGoogle Scholar
McPherson, S.M., McPherson, P.S., Mathews, L., Campbell, K.P. & Longo, F.J. (1992). Cortical localization of a calcium release channel in sea urchin eggs. J. Cell Biol. 116, 1111–21.CrossRefGoogle ScholarPubMed
Mohri, T. & Hamaguchi, Y. (1990). Quantitative analysis of the process and propagation of cortical granule breakdown in sea urchin eggs. Cell Struct. Funct. 15, 309–15.CrossRefGoogle ScholarPubMed
Mohri, T. & Hamaguchi, Y. (1991). Propagation of transient Ca2+ increase in sea urchin eggs upon fertilization and its regulation by microinjecting EGTA solution. Cell Struct. Funct. 16, 157–65.CrossRefGoogle ScholarPubMed
Mohri, T., Ivonnet, P.I. & Chambers, E.L. (1995). Effect on sperm-induced activation current and increase of cytosolic Ca2+ by agents that modify the mobilization of [Ca2+]. I. Heparin and pentosan polysulfate. Dev Biol 172, 139–57.CrossRefGoogle ScholarPubMed
Moser, F. (1939). Studies on a cortical layer response to stimulating agents in the Arbacia egg. I. Response to insemination, J. Exp. Zool. 80, 423–71.CrossRefGoogle Scholar
Moy, G.W., Kopf, G.S., Gache, C. & Vacquier, V.D. (1983). Calcium-mediated release of glucanase activity from cortical granules of sea urchin eggs. Dev. Biol. 100, 267–74.CrossRefGoogle ScholarPubMed
Rakow, T.L., & Shen, S.S. (1990). Multiple stores of calcium are released in the sea urchin egg during fertilization. Proc. Nati. Acad. Sci. USA 87, 9285–9.CrossRefGoogle ScholarPubMed
Sasaki, H. (1984). Modulation of calcium sensitivity by a specific cortical protein during sea urchin egg cortical vesicle exocytosis. Dev. Biol. 101, 125–35.CrossRefGoogle ScholarPubMed
Schweizer, F.E., Betz, H. & Augustine, G.J. (1995). From vesicle docking to endocytosis: intermediate reactions of exocytosis. Neuron 14, 689–96.CrossRefGoogle ScholarPubMed
Shen, S.S. (1995). Mechanisms of calcium regulation in sea urchin eggs and their activities during fertilization. Curr. Topics Dev. Biol. 30, 63–101.CrossRefGoogle ScholarPubMed
Shen, S.S. & Buck, W.R. (1993). Sources of calcium in sea urchin eggs during the fertilization response. Dev. Biol. 157, 157–69.CrossRefGoogle ScholarPubMed
Sollner, T., Bennett, M.K., Whiteheart, S.W., Scheller, R.H. & Rothman, J.E. (1993). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activption, and fusion. Cell 75, 409–18.CrossRefGoogle ScholarPubMed
Steinhardt, R., Zucker, R. & Schatten, G. (1977). Intracellular calcium release at fertilization in the sea urchin egg. Dev. Biol. 58, 185–96.CrossRefGoogle ScholarPubMed
Steinhardt, R.A., Bi, G. & Alderton, J.M. (1994). Cell membrane, resealing by a vesicular mechanism similar to neurotransmitter release. Science 263, 390–3.CrossRefGoogle ScholarPubMed
Strieker, S.A. (1995). Time-lapse confocal imaging of calcium dynamics in starfish embryos. Dev. Biol. 170, 496–518.CrossRefGoogle Scholar
Strieker, S.A., Centonze, V.E., Paddock, S.W. & Schatten, G. (1992). Confocal microscopy of fertilization-induced calcium dynamics in sea urchin eggs. Dev. Biol. 149, 370–80.CrossRefGoogle Scholar
Suzuki, K., Tanaka, Y., Nakajima, Y., Hirano, K., Itoh, H., Miyata, H., Hayakawa, T. & Kinosita, K. Jr, (1995). Spatiotemporal relationships among early events of fertilization in sea urchin eggs revealed by multiview microscopy. Biophys. J. 68, 739–48.CrossRefGoogle ScholarPubMed
Swann, K. & Whitaker, M. (1986). The part played by inosital trisphosphate and calcium in the propagation of the fertilization wave in sea urchin eggs. J. Cell Biol. 103, 2333–42.CrossRefGoogle Scholar
Swann, K. & Whitaker, M.J. (1990). Second messengers at fertilization in sea-urchin eggs. J. Reprod. Fertil. Suppl. 42, 141–53.Google ScholarPubMed
Terasaki, M. (1995). Visualization of exocytosis during sea urchin egg fertilization using confocal microscopy, J. Cell Sci. 108, 2293–300.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
Terasaki, M., Henson, J., Begg, D., Kaminer, B. & Sardet, C. (1991). Characterization of sea urchin egg endoplasmic reticulum in cortical preparations. Dev. Biol. 148, 398–401.CrossRefGoogle ScholarPubMed
Trimmer, J.S. & Vacquier, V.D. (1986). Activation of sea urchin gametes. Annu. Rev. Cell Biol. 2, 1–26.CrossRefGoogle ScholarPubMed
Turner, P.R., Sheetz, M.P. & Jaffe, L.A. (1984). Fertilization increases the phosphoinositide content of sea urchin eggs. Nature 310, 414–15.CrossRefGoogle ScholarPubMed
Vacquier, V.D. (1975). The isolation of intact cortical granules from sea urchin eggs: calcium ions trigger granule discharge. Dev. Biol. 43, 62–74.CrossRefGoogle Scholar
Vogel, S.S., Blank, P.S. & Zimmerberg, J. (1996). Poisson-distributed active fusion complexes underlie the control of the rate and extent of exocytosis by calcium, J. Cell Biol. 134, 329–38.CrossRefGoogle ScholarPubMed
Whitaker, M.J. & Baker, P.F. (1983). Calcium-dependent exocytosis in an in vitro secretory granule plasma membrane preparation from sea urchin eggs and the effects of some inhibitors of cytoskeletal function. Proc. R. Soc. Lond. B 218, 397–413.Google Scholar
Whitaker, M. & Irvine, R.F. (1984). Inositol 1, 4,5-triphosphate microinjection activates sea urchin eggs. Nature 312, 636–9.CrossRefGoogle Scholar
Whitaker, M. & Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 1–12.CrossRefGoogle Scholar
Zucker, R.S. & Steinhardt, R.A. (1978). Prevention of the cortical reaction in fertilized sea urchin eggs by injection of calcium-chelating ligands. Biochim. Biophys. Acta 541, 459–66.CrossRefGoogle ScholarPubMed