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Requirement for a localized, IP3R-generated Ca2+ transient during the furrow positioning process in zebrafish zygotes

Published online by Cambridge University Press:  01 May 2006

Karen W. Lee ,
Sarah E. Webb  and
Andrew L. Miller
Karen W. Lee
Affiliation:
Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, People's Republic of China
Sarah E. Webb
Affiliation:
Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, People's Republic of China
Andrew L. Miller*
Affiliation:
Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, People's Republic of China
*
All correspondence to: A.L. Miller, Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong SAR, PRC. Tel: +852 2358 8631. Fax: +852 2358 1559. e-mail: [email protected]
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Summary

We report that the first localized Ca2+ transient visualized in the blastodisc cortex of post-mitotic zebrafish zygotes has unique features. We confirm that this initial ‘furrow positioning’ Ca2+ transient precedes the physical appearance of the first cleavage furrow at the blastodisc surface and that it has unique dynamics, which distinguish it from the subsequent furrow propagation transients that develop from it. This initial transient displays a distinct rising phase that peaks prior to the initiation of the two linear, subsurface, self-propagating Ca2+ waves that constitute the subsequent furrow propagation transient. Through the carefully timed introduction of the Ca2+ buffer, dibromo-BAPTA, we also demonstrate the absolute requirement of this initial rising phase Ca2+ transient in positioning the furrow at the blastodisc surface: no rising phase transient, no cleavage furrow. Likewise, the introduction of the inositol 1,4,5-trisphosphate receptor (IP3R) antagonist, 2-aminoethoxydiphenyl borate, eliminates both the rising phase transient and the appearance of the furrow at the cell surface. On the other hand, antagonists of the ryanodine receptor and NAADP-sensitive channels, or simply bathing the zygote in Ca2+-free medium, have no effect on the generation of the rising phase positioning transient or the appearance of the furrow at the surface. This suggests that like the subsequent propagation and deepening/zipping Ca2+ transients, the rising phase furrow positioning transient is also generated specifically by Ca2+ released via IP3Rs. We propose, however, that despite being generated by a similar Ca2+ release mechanism, the unique features of this initial transient suggest that it might be a distinct signal with a specific function associated with positioning the cleavage furrow at the blastodisc surface.

Keywords

AequorinCa2+CytokinesisFurrow positioningIP3 receptorZebrafish
Type
Research Article
Information
Zygote , Volume 14 , Issue 2 , May 2006 , pp. 143 - 155
Copyright
Copyright © Cambridge University Press 2006

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References

Alsop, G.B. & Zhang, D. (2004). Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes. J. Cell Sci. 117, 1591–602.CrossRefGoogle ScholarPubMed
Berridge, M.J. (1997). Elementary and global aspects of calcium signalling. J. Exp. Biol. 200, 315–19.CrossRefGoogle ScholarPubMed
Berridge, M.J., Lipp, P. & Bootman, M.D. (2000). The versatility and universality of calcium signalling. Nature Rev. Mol. Cell Biol. 1, 11–21.CrossRefGoogle ScholarPubMed
Berridge, M.J., Bootman, M.D. & Roderick, H.L. (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev. Mol. Cell Biol. 4, 517–29.CrossRefGoogle ScholarPubMed
Bootman, M.D. & Berridge, M.J. (1996). Subcellular Ca2+ signals underlying waves and graded responses in HeLa cells. Curr. Biol. 6, 855–65.CrossRefGoogle ScholarPubMed
Bootman, M., Niggli, E., Berridge, M. & Lipp, P. (1997). Imaging the hierarchical Ca2+ signalling system in HeLa cells. J. Physiol. (Lond.) 499, 307–14.CrossRefGoogle ScholarPubMed
Chang, D.C. & Lu, P. (2000). Multiple types of calcium signals are associated with cell division in zebrafish embryo. Microsc. Res. Tech. 49, 111–22.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Chang, D.C. & Meng, C. (1995). A localized elevation of cytosolic free calcium is associated with cytokinesis in the zebrafish embryo. J. Cell Biol. 131, 1539–45.CrossRefGoogle ScholarPubMed
Créton, R., Speksnijder, J.E. & Jaffe, L.F. (1998). Patterns of free calcium in zebrafish embryos. J. Cell Sci. 111, 1613–22.CrossRefGoogle ScholarPubMed
Ehrlich, B.E., Kaftan, E., Bezprozvannaya, S. & Bezprozvanny, I. (1994). The pharmacology of intracellular Ca2+-release channels. Trends Pharmacol. Sci. 15, 145–9.CrossRefGoogle Scholar
Fluck, R.A., Miller, A.L. & Jaffe, L.F. (1991). Slow calcium waves accompany cytokinesis in medaka fish eggs. J. Cell Biol. 115, 1259–65.CrossRefGoogle ScholarPubMed
Genazzani, A.A., Mezna, M., Dickey, D.M., Michelangeli, F., Walseth, T.F. & Galione, A. (1997). Pharmacological properties of the Ca2+-release mechanism sensitive to NAADP in the sea urchin egg. Br. J. Pharmacol. 121, 1489–95.CrossRefGoogle ScholarPubMed
Jesuthasan, S. (1998). Furrow-associated microtubule arrays are required for the cohesion of zebrafish blastomeres following cytokinesis. J. Cell Sci. 111, 3695–703.CrossRefGoogle ScholarPubMed
Lee, K. W., Baker, R., Galione, A., Gilland, E.H., Hanlon, R.T. & Miller, A.L. (1996). Ionophore-induced calcium waves activate unfertilized zebrafish (Danio rerio) eggs. Biol. Bull. 191, 265–7.CrossRefGoogle Scholar
Lee, K.W., Webb, S.E. & Miller, A.L. (2003). Ca2+ released via IP3 receptors is required for furrow deepening during cytokinesis in zebrafish embryos. Int. J. Dev. Biol. 47, 411–21.Google ScholarPubMed
Lee, K.W., Ho, S.M., Wong, C.H., Webb, S.E. & Miller, A.L. (2004). Characterization of mid-spindle microtubules during furrow positioning in early cleavage period zebrafish embryos. Zygote 12, 221–30.CrossRefGoogle ScholarPubMed
Leung, C.F., Webb, S.E. & Miller, A.L. (1998). Calcium transients accompany ooplasmic segregation in zebrafish embryos. Dev. Growth Differ. 40, 313–26.CrossRefGoogle ScholarPubMed
Mabuchi, I. (1986). Biochemical aspects of cytokinesis. Int. Rev. Cytol. 101,175–213.CrossRefGoogle ScholarPubMed
Mabuchi, I. & Takano-Ohmuro, H. (1990). Effects of inhibitors of myosin light chain kinase and other protein kinases on the first cell division of sea urchin eggs. Dev. Growth Differ. 32, 549–56.CrossRefGoogle ScholarPubMed
Mitsuyama, F. & Sawai, T. (2001). The redistribution of Ca2+ stores with inositol 1,4,5-trisphosphate receptor to the cleavage furrow in a microtubule-dependent manner. Int. J. Dev. Biol. 45, 861–8.Google Scholar
Mitsuyama, F., Sawai, T., Carafoli, E., Furuichi, T. & Mikoshiba, K. (1999). Microinjection of Ca2+ store-enriched microsome fractions to dividing newt eggs induces extra-cleavage furrows via inositol 1,4,5-trisphosphate-induced Ca2+ release. Dev. Biol. 214, 160–7.CrossRefGoogle ScholarPubMed
Muto, A., Kume, S., Inoue, T., Okano, H. & Mikoshiba, K. (1996). Calcium waves along the cleavage furrows in cleavage-stage Xenopus embryos and its inhibition by heparin. J. Cell Biol. 135, 181–90.CrossRefGoogle ScholarPubMed
Noguchi, T. & Mabuchi, I. (2002). Localized calcium signals along the cleavage furrow of the. Xenopus egg are not involved in cytokinesis. Mol. Biol. Cell. 13, 1263–73.CrossRefGoogle Scholar
Parker, I. & Yao, Y. (1996). Ca2+ transients associated with openings of inositol trisphosphate-gated channels in Xenopus oocytes. J. Physiol. (Lond.) 491, 663–8.CrossRefGoogle ScholarPubMed
Shimomura, O. (1995). Luminescence of aequorin is triggered by the binding of two calcium ions. Biochem. Biophys. Res. Commun. 211, 359–63.CrossRefGoogle ScholarPubMed
Shimomura, O., Musicki, B. & Kishi, Y. (1989). Semi-synthetic aequorins with improved sensitivity to Ca2+ ions. Biochem. J. 261, 913–20.CrossRefGoogle ScholarPubMed
Tasaka, K., Mio, M., Fujisawa, K. & Aoki, I. (1991). Role of microtubules on Ca2+ release from the endoplasmic reticulum and associated histamine release from rat peritoneal mast cells. Biochem. Pharmacol. 41, 1031–7.CrossRefGoogle ScholarPubMed
Terasaki, M., Chen, L.B. & Fujiwara, K. (1986). Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol. 103, 1557–68.CrossRefGoogle ScholarPubMed
Webb, S.E., Lee, K.W., Karplus, E. & Miller, A.L. (1997). Localized calcium transients accompany furrow positioning, propagation, and deepening during the early cleavage period of zebrafish embryos. Dev. Biol. 192, 78–92.CrossRefGoogle ScholarPubMed
Westerfield, M. (1994). The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Brachydanio rerio). Eugene, OR: University of Oregon Press.Google Scholar
Yao, Y., Choi, J. & Parker, I. (1995). Quantal puffs of intracellular Ca2+ evoked by inositol trisphosphate in Xenopus oocytes. J. Physiol. (Lond.) 482, 533–53.CrossRefGoogle ScholarPubMed