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Development of Ca2+-release mechanisms during oocyte maturation of the starfish Asterina pectinifera

Published online by Cambridge University Press:  03 October 2016

Isao Takahashi  and
Keiichiro Kyozuka
Isao Takahashi
Affiliation:
Research Center for Marine Biology, Asamushi, Graduate School of Life Science, Tohoku University, Asamushi, Aomori 039–3501, Japan.
Keiichiro Kyozuka*
Affiliation:
Research Center for Marine Biology, Asamushi, Graduate School of Life Science, Tohoku University, Asamushi, Aomori 039–3501, Japan Research Center for Marine Biology, Asamushi, Graduate School of Life Science, Tohoku University, Asamushi, Aomori 039–3501, Japan.
*
All correspondence to Keiichiro Kyozuka. Research Center for Marine Biology, Asamushi, Graduate School of Life Science, Tohoku University, Asamushi, Aomori 039–3501, Japan. Tel: +81 17 752 3397. Fax: +81 17 752 2765. E-mail: kkyozuka@m.tohoku.ac.jp
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Summary

An important step for successful fertilization and further development is the increase in intracellular Ca2+ in the activated oocyte. It has been known that starfish oocytes become increasingly sensitive to inositol 1,4,5-trisphosphate (IP3) during meiotic maturation to exhibit highly efficient IP3-induced Ca2+ release (IICR) by the time of germinal vesicle breakdown (GVBD). However, we noted that the peak level of intracellular Ca2+ increase after insemination is already high in the maturing oocytes before GVBD. Using maturing oocytes before GVBD, we investigated Ca2+ release mechanisms other than IICR. We report here that Ca2+-release mechanisms dependent on nicotinic acid adenine dinucleotide phosphate (NAADP) and nicotinamide adenine dinucleotide (NADP), the precursor of NAADP, became functional prior to the development of IICR mechanisms. As with IP3, but unlike NAADP, the Ca2+ stores responsive to NADP are sensitized during the meiotic maturation induced by 1-methyladenine (1-MA). This suggests that the process may represent a physiological response to the maturation hormone. NADP-dependent Ca2+ release in immature oocytes, however, did not induce oocyte maturation by itself, but was enhanced by the conditions mimicking the increases of intracellular Ca2+ and pH that take place in the maturing oocytes of starfish.

Keywords

Maturing oocyteInositol 1,4,5-trisphosphate (IP3)Nicotinamide adenine dinucleotide (NADP)Nicotinic acid adenine dinucleotide phosphate (NAADP)Intracellular Ca2+ and pH
Type
Research Article
Information
Zygote , Volume 24 , Issue 6 , December 2016 , pp. 857 - 868
Copyright
Copyright © Cambridge University Press 2016 

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References

Aarhus, R., Graeff, R.M., Dickey, D.M., Walseth, T.F. & Lee, H.C. (1995). ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium mobilizing metabolite from NADP. J. Biol. Chem. 270, 30327–33.Google Scholar
Ayabe, T., Kopf, G.S. & Schultz, R.M. (1995). Regulation of mouse egg activation: presence of ryanodine receptors and effects of microinjected ryanodine and cyclic ADP ribose on uninseminated and inseminated eggs. Development 121, 2233–44.Google Scholar
Berridge, M.J. (2009). Inositol trisphosphate and calcium signalling mechanisms. Biochim. Biophys. Acta 793, 933–40.Google Scholar
Billington, R.A., Ho, A. & Genazzani, A.A. (2002). Nicotinic acid adenine dinucleotide phosphate (NAADP) is present at micromolar concentrations in sea urchin spermatozoa. J. Physiol. 544, 107–12.Google Scholar
Carroll, D.J., Ramarao, C.S., Mehlmann, L.M., Roche, S., Terasaki, M. & Jaffe, L.A. (1997). Calcium release at fertilization in starfish eggs is mediated by phospholipase C gamma. J. Cell Biol. 138, 1303–11.Google Scholar
Chiba, K., Kado, R.T. & Jaffe, L.A. (1990). Development of calcium release mechanisms during starfish oocyte maturation. Dev. Biol. 140, 300–6.CrossRefGoogle ScholarPubMed
Chun, J.T. & Santella, L. (2009). The actin cytoskeleton in meiotic maturation and fertilization of starfish eggs. Biochem. Biophys. Res. Commun. 384, 141–3.Google Scholar
Chun, J.T., Limatola, N., Vasilev, F. & Santella, L. (2014). Early events of fertilization in sea urchin eggs are sensitive to actin-binding organic molecules. Biochem. Biophys. Res. Commun. 450, 1166–74.Google Scholar
Churchill, G.C., O'Neill, J.S., Masgrau, R., Patel, S., Thomas, J.M., Genazzani, A.A. & Galione, A. (2003). Sperm deliver a new messenger: NAADP. Curr. Biol. 13, 125–8.Google 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. Biol. Chem. 262, 9561–8.Google Scholar
Costache, V., McDougall, A. & Dumollard, R. (2014). Cell cycle arrest and activation of development in marine invertebrate deuterostomes. Biochem. Biophys. Res. Commun. 450, 1175–81.Google Scholar
Crossley, I., Whalley, T. & Whitaker, M. (1991). Guanosine 5′-thiotriphosphate may stimulate phosphoinositide messenger production in sea urchin eggs by a different route than the fertilizing sperm. Cell. Regul. 2, 121–33.CrossRefGoogle Scholar
Deguchi, R. & Osanai, K. (1994). Repetitive intracellular Ca2+ increases at fertilization and the role of Ca2+ in meiosis reinitiation from the first metaphase in oocytes of marine bivalves. Dev. Biol. 163, 62–74.Google Scholar
Deguchi, R., Osanai, K. & Morisawa, M. (1996). Extracellular Ca2+ entry and Ca2+ release from inositol 1,4,5-trisphosphate-sensitive stores function at fertilization in oocytes of the marine bivalve Mytilus edulis. Development 122, 3651–60.CrossRefGoogle ScholarPubMed
El-Jouni, W., Jang, B., Haun, S. & Machaca, K. (2005). Calcium signaling differentiation during Xenopus oocyte maturation. Dev. Biol. 288, 514–25.CrossRefGoogle ScholarPubMed
Epel, D., Patton, C., Wallace, R.W. & Cheung, W.Y. (1981). Calmodulin activates NAD kinase of sea urchin eggs: an early event of fertilization. Cell 23, 543–9.Google Scholar
Epel, D. (1990). The initiation of development at fertilization. Cell. Differ. Dev. 29, 1–12.Google Scholar
Fujimori, F. & Hirai, S. (1979). Differences in starfish oocyte susceptibility to polyspermy during the course of maturation. Biol. Bull. 157, 249–57.Google 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
Guerrier, P. & Doree, M. (1975). Hormonal control of reinitiation of meiosis in starfish. The requirement of 1-methyladenine during nuclear maturation. Dev. Biol. 47, 341–8.Google Scholar
Giusti, A.F., Xu, W., Hinkle, B., Terasaki, M. & Jaffe, L.A. (2000). Evidence that fertilization activates starfish eggs by sequential activation of a Src-like kinase and phospholipase C gamma. J. Biol. Chem. 275, 16788–94.Google Scholar
Harada, K., Oita, E. & Chiba, K. (2003). Metaphase I arrest of starfish oocytes induced via the MAP kinase pathway is released by an increase of intracellular pH. Development 130, 4581–6.Google Scholar
Harada, Y., Kawazoe, M., Eto, Y., Ueno, S. & Iwao, Y. (2011). The Ca2+ increase by the sperm factor in physiologically polyspermic newt fertilization: its signaling mechanism in egg cytoplasm and the species-specificity. Dev. Biol. 351, 266–76.Google Scholar
Hirohashi, N., Harada, K. & Chiba, K. (2008). Hormone-induced cortical maturation ensures the slow block to polyspermy and does not couple with meiotic maturation in starfish. Dev. Biol. 318, 194–202.Google Scholar
Iwasaki, H., Chiba, K., Uchiyama, T., Yoshikawa, F., Suzuki, F., Ikeda, M., Furuichi, T. & Mikoshiba, K. (2002). Molecular characterization of the starfish inositol 1,4,5-trisphosphate receptor and its role during oocyte maturation and fertilization. J. Biol. Chem. 277, 2763–72.Google Scholar
Jaffe, L.A., Giusti, A.F., Carroll, D.J. & Foltz, K.R. (2001). Ca2+ signalling during fertilization of echinoderm eggs. Semin. Cell. Dev. Biol. 12, 45–51.Google Scholar
Kanatani, H., Shirai, H., Nakanishi, K. & Kurokawa, T. (1969). Isolation and identification of meiosis inducing substance in starfish. Nature 221, 273–4.CrossRefGoogle Scholar
Kashir, J., Deguchi, R., Jones, C., Coward, K. & Stricker, S.A. (2013). Comparative biology of sperm factors and fertilization-induced calcium signals across the animal kingdom. Mol. Reprod. Dev. 80, 787–815.CrossRefGoogle ScholarPubMed
Kishimoto, T. (1986). Microinjection and cytoplasmic transfer in starfish oocytes. Methods Cell. Biol. 27, 379–94.Google Scholar
Kyozuka, K., Chun, J.T., Puppo, A., Gragnaniello, G., Garante, E. & Santella, L. (2008) Actin cytoskeleton modulates calcium signaling during maturation of starfish oocytes. Dev. Biol. 320, 426–35.Google Scholar
Lange, K. (1999). Microvillar Ca++ signaling: a new view of an old problem. J. Cell. Physiol. 180, 19–34.Google Scholar
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.Google Scholar
Lee, H.C., Aarhus, R. & Walseth, T.F. (1993). Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261, 352–5.Google Scholar
Lee, H.C. & Aarhus, R. (1995). A derivative of NADP mobilizes calcium stores insensitive to trisphosphate and cyclic ADP-ribose. J. Biol. Chem. 270, 2152–7.Google Scholar
Lim, D., Kyozuka, K., Gragnaniello, G., Carafoli, E. & Santella, L. (2001). NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J. 15, 2257–67.Google Scholar
Lim, D., Lange, K. & Santella, L. (2002) Activation of oocytes by latrunculin A. FASEB J. 16, 1050–6.Google Scholar
Lim, D., Ercolano, E., Kyozuka, K., Nusco, G.A., Moccia, F., Lange, K. & Santella, L. (2003). The M-phase-promoting factor modulates the sensitivity of the Ca2+ stores to inositol 1,4,5-trisphosphate via the actin cytoskeleton. J. Biol. Chem. 278, 42505–14.Google Scholar
Limatola, N., Chun, J.T., Kyozuka, K. & Santella, L. (2015). Novel Ca2+ increases in the maturing oocytes of starfish during the germinal vesicle breakdown. Cell. Calcium 58, 500–10.CrossRefGoogle ScholarPubMed
McCulloh, D.H., Ivonnet, P.I., Landowne, D. & Chambers, E.L. (2000). Calcium influx mediates the voltage-dependence of sperm entry into sea urchin eggs. Dev. Biol. 223, 449–62.Google Scholar
Matsumoto, M., Solzin, J., Helbig, A., Hagen, V., Ueno, S., Kawase, O., Maruyama, Y., Ogiso, M., Godde, M., Minakata, H., Kaupp, U.B., Hoshi, M. & Weyand, I. (2003). A sperm-activating peptide controls a cGMP-signaling pathway in starfish sperm. Dev. Biol. 260, 314–24.Google Scholar
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. Dev. Biol. 158, 62–78.CrossRefGoogle ScholarPubMed
Miyazaki, S. (2006). Thirty years of calcium signals at fertilization. Dev. Biol. 17, 233–243.Google Scholar
Moccia, F., Lim, D., Nusco, G.A., Ercolano, E. & Santella, L. (2003) NAADP activates a Ca2+ current that is dependent on F-actin cytoskeleton. FASEB J. 17,1907–9.CrossRefGoogle ScholarPubMed
Moccia, F., Nusco, G.A., Lim, D., Kyozuka, K. & Santella, L. (2006). NAADP and InsP3 play distinct roles at fertilization in starfish oocytes. Dev. Biol. 294, 24–38.Google Scholar
Nakano, T., Deguchi, R. & Kyozuka, K. (2014). Intracellular calcium signaling in the fertilized eggs of Annelida. Biochem. Biophys. Res. Commun. 450, 1188–94.CrossRefGoogle ScholarPubMed
Nemoto, S.I. (1982). Nature of the 1-methyladenine-requiring phase in maturation of starfish oocytes. Dev. Growth Differ. 24, 429–42.Google Scholar
Nusco, G.A., Lim, D., Sabala, P. & Santella, L. (2002). Ca2+ response to cADPr during maturation and fertilization of starfish oocytes. Biochem. Biophys. Res. Commun. 290, 1015–21.CrossRefGoogle ScholarPubMed
Puppo, A., Chun, J.T., Gragnaniello, G., Garante, E. & Santella, L. (2008) Alteration of the cortical actin cytoskeleton deregulates Ca2+ signaling, monospermic fertilization, and sperm entry. PLoS One 3, e3588.Google Scholar
Santella, L. & Kyozuka, K. (1994). Reinitiation of meiosis in starfish oocytes requires an increase in nuclear Ca2+ . Biochem. Biophys. Res. Commun. 203, 674–80.Google Scholar
Santella, L., De Riso, L., Gragnaniello, G. & Kyozuka, K. (1998) Separate activation of the cytoplasmic and nuclear calcium pools in maturing starfish oocytes. Biochem. Biophys. Res. Commun. 252, 1–4.CrossRefGoogle ScholarPubMed
Santella, L., De Riso, L., Gragnaniello, G. & Kyozuka, K. (1999). Cortical granule translocation during maturation of starfish oocytes requires cytoskeletal rearrangement triggered by InsP3-mediated Ca2+ release. Exp. Cell Res. 248, 567–74.Google Scholar
Santella, L., Kyozuka, K., Genazzani, A.A., De Riso, L. & Carafoli, E. (2000). Nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release. Interactions among distinct Ca2+ mobilizing mechanisms in starfish oocytes. J. Biol. Chem. 275, 8301–6.Google Scholar
Santella, L., Lim, D. & Moccia, F. (2004). Calcium and fertilization: the beginning of life. Trends Biochem. Sci. 29, 400–8.Google Scholar
Santella, L., Vasilev, F. & Chun, J.T. (2012). Fertilization in echinoderms. Biochem. Biophys. Res. Commun. 425, 588–94.Google Scholar
Santella, L., Limatola, N. & Chun, J. T. (2015). Calcium and actin in the saga of awakening oocytes. Biochem. Biophys. Res. Commun. 460, 104–13.Google Scholar
Saunders, C.M., Larman, M.G., Parrington, J., Cox, L.J., Royse, J., Blayney, L.M., Swann, K. & Lai, F.A. (2002). PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–44.Google Scholar
Schroeder, T.E. & Stricker, S.A. (1983). Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev. Biol. 98, 373–84.Google Scholar
Shen, S.S. & Buck, W.R. (1993). Sources of calcium in sea urchin eggs during the fertilization response. Dev. Biol. 157, 157–69.Google Scholar
Steinhardt, R.A. & Epel, D. (1974). Activation of sea-urchin eggs by a calcium ionophore. Proc. Natl. Acad. Sci. USA 71, 1915–9.Google Scholar
Stricker, S.A., Centonze, V.E. & Melendez, R.F. (1994). Calcium dynamics during starfish oocyte maturation and fertilization. Dev. Biol. 166, 34–58.Google Scholar
Stricker, S.A. (1995). Time-lapse confocal imaging of calcium dynamics in starfish embryos. Dev. Biol. 170, 496–518.Google Scholar
Stricker, S.A. (1996). Repetitive calcium waves induced by fertilization in the nemertean worm Cerebratulus lacteus . Dev. Biol. 176, 243–63.Google Scholar
Vacquier, V.D. (1975). The isolation of intact cortical granules from sea urchin eggs: calcium ions trigger granule discharge. Dev. Biol. 43, 62–74.Google Scholar
Vasilev, F., Chun, J.T., Gragnaniello, G., Garante, E. & Santella, L. (2012). Effects of ionomycin on egg activation and early development in starfish. PLoS One 7, e39231.Google Scholar
Whalley, T., McDougall, A., Crossley, I., Swann, K. & Whitaker, M. (1992). Internal calcium release and activation of sea urchin eggs by cGMP are independent of the phosphoinositide signaling pathway. Mol. Biol. Cell. 3, 373–83.Google Scholar
Whitaker, M. (2006). Calcium at fertilization and in early development. Physiol. Rev. 86, 25–88.CrossRefGoogle ScholarPubMed
Wilding, M., Russo, G.L., Marino, M., Grumetto, L., De Simone, M.L., Tosti, E. & Dale, B. (1998a). Activation of Ciona intestinalis at fertilization is controlled by nicotinamide nucleotide metabolism, pp. 121–3. New York: Plenum Press.Google Scholar
Wilding, M., Russo, G.L., Galione, A., Marino, M. & Dale, B. (1998b). ADP-ribose gates the fertilization channel in ascidian oocytes. Am. J. Physiol. 275, 1277–83.Google Scholar
Yoshida, M., Sensui, N., Inoue, T., Morisawa, M. & Mikoshiba, K. (1998). Role of two series of Ca2+ oscillations in activation of ascidian eggs. Dev. Biol. 203, 122–33.Google Scholar
Zucker, R.S., Steinhardt, R.A. & Winkler, M.M. (1978). Intracellular calcium release and the mechanisms of parthenogenetic activation of the sea urchin egg. Dev. Biol. 65, 285–95.Google Scholar