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Soluble sperm extract specifically recapitulates the initial phase of the Ca2+ response in the fertilized oocyte of P. occelata following a G-protein/ PLCβ signaling pathway

Published online by Cambridge University Press:  16 October 2014

Takeshi Nakano  and
Keiichiro Kyozuka
Takeshi Nakano
Affiliation:
Research Center for Marine Biology, Graduate School of Life Sciences, Tohoku University, Asamushi, Aomori, 039–3501, Japan.
Keiichiro Kyozuka*
Affiliation:
Research Center for Marine Biology, Graduate School of Life Sciences, Tohoku University, Asamushi, Aomori, 039–3501, Japan.
*
All correspondence to: Keiichiro Kyozuka. Research Center for Marine Biology, Graduate School of Life Sciences, Tohoku University, Asamushi, Aomori, 039–3501, Japan. Tel: +81 17 752 3397. Fax: +81 17 752 2765. E-mail: [email protected]
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Summary

Matured oocytes of the annelidan worm Pseudopotamilla occelata are fertilized at the first metaphase of the meiotic division. During the activation by fertilizing spermatozoa, the mature oocyte shows a two-step intracellular Ca2+ increase. Whereas the first Ca2+ increase is localized and appears to utilize the inositol 1,4,5-trisphosphate (IP3)-sensitive Ca2+ stores, the second Ca2+ increase is global and involves Ca2+ influx via voltage-gated Ca2+ channels on the entire surface of the oocyte. To study how sperm trigger the Ca2+ increases during fertilization, we prepared soluble sperm extract (SE) and examined its ability to induce Ca2+ increases in the oocyte. The SE could evoke a Ca2+ increase in the oocyte when it was added to the medium, but not when it was delivered by microinjection. However, the second-step Ca2+ increase leading to the resumption of meiosis did not follow in these eggs. Local application of SE induced a non-propagating Ca2+ increase and formed a cytoplasmic protrusion that was similar to that created by the fertilizing sperm at the first stage of the Ca2+ response, important for sperm incorporation into the oocyte. Our results suggest that the fertilizing spermatozoon may trigger the first-step Ca2+ increase before it fuses with the oocyte in a pathway that involves the G-protein-coupled receptor and phospholipase C. Thus, the first phase of the Ca2+ response in the fertilized egg of this species is independent of the second phase of the Ca2+ increase for egg activation.

Keywords

Annelida oocyteCa2+ functionCa2+ increaseEgg activationInositol 1,4,5-trisphosphate (IP3)Sperm extract
Type
Research Article
Information
Zygote , Volume 23 , Issue 6 , December 2015 , pp. 821 - 835
Copyright
Copyright © Cambridge University Press 2014 

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References

Abassi, Y.A., Carroll, D.J., Giusti, A.F., Belton, R.J. Jr. & Foltz, K.R. (2000). Evidence that Src-type tyrosine kinase activity is necessary for initiation of calcium release at fertilization in sea urchin eggs. Dev. Biol. 218, 206–19.Google Scholar
Anderson, W.A. & Eckberg, W.R. (1983). A cytological analysis of fertilization in Chaetopterus pergamentaceus . Biol. Bull. 165, 110–18.Google Scholar
Berridge, M.J. (1993) Inositol trisphosphate and calcium signaling. Nature 361, 315–25.Google Scholar
Carroll, D.J. & Jaffe, L.A. (1995). Protease stimulate fertilization-like responses in starfish eggs. Dev. Biol. 170, 690–700.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 second messenger: NAADP. Curr. Biol. 13, 125–8.Google Scholar
Colas, P. & Dube, F. (1998). Meiotic maturation in mollusc oocytes. Semin. Cell Dev. Biol. 9, 539–48.Google Scholar
Cuomo, A., Silvestre, F., De Santis, R. & Tosti, E. (2006). Ca2+ and Na+ current patterns during oocyte maturation, fertilization, and early developmental stages of Ciona intestinalis . Mol. Reprod. Dev. 73, 501–11.CrossRefGoogle ScholarPubMed
Dale, B., Marino, M., & Wilding, M. (1999). Sperm-induced calcium oscillations. Soluble factor, factors or receptors? Mol. Hum. Reprod. 5, 1–4.CrossRefGoogle ScholarPubMed
Dale, B., Wilding, M., Coppola, G.F. & Tosti, E. (2010). How spermatozoa activate oocytes? Reprod. Biomed. Online 21, 1–3.CrossRefGoogle ScholarPubMed
Dale, B. & DeFelice, L. (2011). Polyspermy prevention: facts and artifacts? J. Assist. Reprod. Genet. 28, 199–207.Google Scholar
Dale, B. (2014). Is the idea of a first block to polyspermy based on artifact? Biochem. Biophys. Res. Commun. 450, 1159–65.Google Scholar
Deguchi, R., Shirakawa, H., Oda, S., Mohri, T. & Miyazaki, S. (2000). Spatiotemporal analysis of Ca2+ waves in relation to the sperm entry site and animal-vegetal axis during Ca2+ oscillations in fertilized mouse eggs. Dev. Biol. 218, 299–313.Google Scholar
Deguchi, R. & Morisawa, M. (2003). External Ca2+ is predominantly used for cytoplasmic and nuclear Ca2+ increases in fertilized oocytes of the marine bivalve Mactra chinensis . J. Cell Sci. 116, 367–76.Google Scholar
Deguchi, R., Kondoh, E. & Itoh, J. (2005). Spatiotemporal characteristics and mechanisms of intracellular Ca2+ increase at fertilization in eggs of jellyfish (Phylum Cnidaria, Class Hydrozoa). Dev. Biol. 279, 291–307.Google Scholar
Deguchi, R. (2007). Fertilization causes a single Ca2+ increase that fully depends on Ca2+ influx in oocytes of limpets (Phylum Mollusca, Class Gastropoda). Dev. Biol. 304, 652–63.Google Scholar
Dupont, G., McGuinness, O.M., Johnson, M.H., Berridge, M.J. & Borgese, F. (1996). Phospholipase C in mouse oocytes: characterization of β and γ isoforms and their possible involvement in sperm-induced Ca2+ spiking. Biochem. J. 316, 583–91.CrossRefGoogle ScholarPubMed
Harada, Y., Matsumoto, T., Hirahara, S., Nakashima, A., Ueno, S., Oda, S., Miyazaki, S. & Iwao, Y. (2007). Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster . Dev. Biol. 306, 797–808.CrossRefGoogle ScholarPubMed
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
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. (1998). Cell cycle arrest and release in starfish oocytes and eggs. Semin. Cell Dev. Biol. 9, 549–57.Google Scholar
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. 241, 464–7.Google Scholar
Kyozuka, K., Deguchi, R., Mohri, T. & Miyazaki, S. (1998). Injection of sperm extract mimics spatiotemporal dynamics of Ca2+ responses and progression of meiosis at fertilization of ascidian oocytes. Development 125, 4099–105.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
Kyozuka, K, Chun, J.T., Puppo, A., Gragnaniello, G., Garante, E. & Santella, L. (2009) Guanine nucleotides in the meiotic maturation of starfish oocytes: regulation of the actin cytoskeleton and of Ca2+ signaling. PLoS One 20, e6296.Google Scholar
Mehlmann, L.M., Carpenter, G., Rhee, S.G. & Jaffe, L.A. (1998). SH2 domain-mediated activation of phospholipase Cγ is not required to initiate Ca2+ release at fertilization of mouse eggs. Dev. Biol. 203, 221–32.CrossRefGoogle Scholar
Mehlmann, L.M. & Jaffe, L.A. (2005). SH2 domain-mediated activation of an SRC family kinase is not required to initiate Ca2+ release at fertilization in mouse eggs. Reproduction 129, 557–64.Google Scholar
Miyazaki, S. (2006). Thirty years of calcium signals at fertilization. Semin. Cell Dev. Biol. 17, 233–43.Google Scholar
Mizote, A., Okamoto, S. & Iwao, Y. (1999). Activation of Xenopus eggs by protease: possible involvement of a sperm protease in fertilization. Dev. Biol. 208, 79–92.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.Google Scholar
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., Kyozuka, K. & Deguchi, R. (2008). Novel two-step Ca2+ increase and its mechanisms and functions at fertilization oocytes of the annelidan worm Pseudopotamilla occelata . Dev. Growth Differ. 50, 365–79.Google Scholar
Noda, M., Higashida, H., Aoki, S. & Wada, K. (2004). Multiple signal transduction pathways mediated by 5-HT receptors. Mol. Neurobiol. 29, 31–9.Google Scholar
Novikoff, A.B. (1939). Surface changes in unfertilized and fertilized eggs of Sabellaria vulgaris . J. Exp. Zool. 82, 217–37.Google Scholar
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
Rhee, S.G. (2001). Regulation of phosphoinositide-specific phospholipase C. Annu. Rev. Biochem. 70, 281–312.Google Scholar
Runft, L.L. & Jaffe, L.A. (2000). Sperm extract injection into ascidian eggs signals Ca2+ release by the same pathway as fertilization. Development 127, 3227–36.Google Scholar
Runft, L.L., Jaffe, L.A. & Mehlmann, L.M. (2002). Egg activation at fertilization: where it all begins. Dev. Biol. 245, 237–54.Google Scholar
Russo, G.L., Kyozuka, K., Antonazzo, L., Tosti, E. & Dale, B. (1996). Maturation promoting factor in ascidian oocytes is regulated by different intracellular signals at meiosis I and II. Development 122, 1995–2003.Google Scholar
Santella, L., Ercolano, E., Lim, D., Nusco, G.A. & Moccia, F. (2003). Activated M-phase-promoting factor (MPF) is exported from the nucleus of starfish oocytes to increase the sensitivity of the ins(1,4,5)P3 receptors. Biochem. Soc. Trans. 31, 79–82.Google Scholar
Sato, M.S., Yoshimoto, M., Mohri, T. & Miyazaki, S. (1999). Spatiotemporal analysis of [Ca2+]i rises in mouse eggs after intracytoplasmic sperm injection (ICSI). Cell Calcium 26, 49–58.Google Scholar
Sato, K., Tokmakov, A.A., Iwasaki, T. & Fukami, Y. (2000). Tyrosine kinase-dependent activation of phospholipase Cγ is required for calcium transient in Xenopus egg fertilization. Dev. Biol. 224, 453–69.Google Scholar
Sato, M. & Osanai, K. (1983). Sperm reception by an egg microvillus in the polychaete, Tylorrhynchus heterochaetus . J. Exp. Zool. 227, 459–69.Google Scholar
Sato, M. & Osanai, K. (1986). Morphological identification of sperm receptors above egg microvilli in the polychaete. Neanthes japonica. Dev. Biol. 113, 263–70.Google Scholar
Sato, K., Iwasaki, T., Tamaki, I., Aoto, M., Tokmakov, A.A. & Fukami, Y. (1998). Involvement of protein-tyrosine phosphorylation and dephosphorylation in sperm-induced Xenopus egg activation. FEBS Lett. 424, 113–8.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
Shen, S.S., Kinsey, W.H. & Lee, S.-J. (1999). Protein tyrosine kinase-dependent release of intracellular calcium in the sea urchin egg. Dev. Growth Differ. 41, 345–55.Google Scholar
Shimizu, T. (1999). Cytoskeletal mechanisms of ooplasmic segregation in annelid eggs. Int. J. Dev. Biol. 43, 11–18.Google Scholar
Stricker, S.A. (1997). Intracellular injections of a soluble sperm factor trigger calcium oscillations and meiotic maturation in unfertilized oocytes of a marine worm. Dev. Biol. 186, 185–201.Google Scholar
Stricker, S. A. (1999). Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211, 157–76.Google Scholar
Swann, K. & Parrington, J. (1999). Mechanism of Ca2+ release at fertilization in mammals. J. Exp. Zool. 285, 267–75.Google Scholar
Swann, K. & Yu, Y. (2008). The dynamics of calcium oscillations that activate mammalian eggs. Int. J. Dev. Biol. 52, 585–94.Google Scholar
Terasaki, M. & Sardet, C. (1991). Demonstration of calcium uptake and release by sea urchin egg cortical endoplasmic reticulum. J. Cell Biol. 115, 1031–7.Google Scholar
Tosti, E., Gallo, A. & Silvestre, F. (2011). Ion current involved in oocyte maturation, fertilization and early developmental stages of the ascidian Ciona intestinalis . Mol. Reprod. Dev. 78, 854–60.Google Scholar
Ueki, K. & Yokosawa, H. (1997). Evidence for an erbstatin-sensitive tyrosine kinase functioning in ascidian egg activation. Biochem. Biophys. Res. Comm. 238, 130–3.Google Scholar
Yin, X. & Eckberg, W.R. (2009). Characterization of phospholipases C β and γ and their possible roles in Chaetopterus egg activation. Mol. Reprod. Dev. 76, 460–70.Google Scholar
Yoon, S.-Y. & Fissore, R.A. (2007). Release of phospholipase Cζ and [Ca2+]i oscillation-inducing activity during mammalian fertilization. Reproduction 134, 695–704.Google Scholar
Whitaker, M. (2006). Calcium at fertilization and in early development. Physiol. Rev. 86, 25–88.Google Scholar