Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T21:13:06.799Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification of phospholipase activity in Rhinella arenarum sperm extract capable of inducing oocyte activation

Published online by Cambridge University Press:  09 September 2013

Federico Bonilla ,
Carlos Minahk ,
María Teresa Ajmat ,
Graciela Sánchez Toranzo  and
Marta Inés Bühler
Federico Bonilla*
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461–2 ° piso, T4000ILI San Miguel de Tucumán, República Argentina.
Carlos Minahk
Affiliation:
Departamento de Química Biológica - Instituto Superior de Investigaciones Biológicas-INSIBIO. Universidad Nacional de Tucumán, Chacabuco 461 (4000), Tucumán, Argentina.
María Teresa Ajmat
Affiliation:
Departamento de Biología del Desarrollo-INSIBIO. Facultad de Bioquímica, Química y Farmacia. Universidad Nacional de Tucumán, Chacabuco 461 (4000), Tucumán, Argentina.
Graciela Sánchez Toranzo
Affiliation:
Departamento de Biología del Desarrollo-INSIBIO. Facultad de Bioquímica, Química y Farmacia. Universidad Nacional de Tucumán, Chacabuco 461 (4000), Tucumán, Argentina.
Marta Inés Bühler
Affiliation:
Departamento de Biología del Desarrollo-INSIBIO. Facultad de Bioquímica, Química y Farmacia. Universidad Nacional de Tucumán, Chacabuco 461 (4000), Tucumán, Argentina.
*
All correspondence to: Federico Bonilla. Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461–2 ° piso, T4000ILI San Miguel de Tucumán, República Argentina. Tel: +54381 4247752 int. 7093. Fax: +54 381 4247752 int. 7004. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Egg activation, which includes cortical granule exocytosis, resumption and completion of meiosis and pronuclear formation culminates in the first mitotic cleavage. However, the mechanism through which the fertilizing sperm induces this phenomenon is still controversial. We investigated the effect of the microinjection of homologous sperm soluble fractions obtained by fast protein liquid chromatography (FPLC) from reacted sperm (without acrosome) and non-reacted sperm on the activation of Rhinella arenarum oocytes matured in vitro. The FPLC-purified sperm fraction obtained from reacted or non-reacted sperm is able to induce oocyte activation when it is microinjected. This fraction has a 24 kDa protein and showed phospholipase C (PLC) activity in vitro, which was inhibited by D-609 but not by n-butanol or neomycin, suggesting that it is a PLC that is specific for phosphatidylcholine (PC-PLC). The assays conducted using inhibitors of inositol triphosphate (IP3) and ryanodine receptors (RyRs) indicate that the fraction with biological activity would act mainly through the cADPr (cyclic ADP ribose) pathway. Moreover, protein kinase C (PKC) inhibition blocks the activation produced by the same fraction. Immunocytochemical studies indicate that this PC-PLC can be found throughout the sperm head.

Keywords

DiacylglycerolOocyte activationPC-PLCRhinella arenarumSperm factor
Type
Research Article
Information
Zygote , Volume 22 , Issue 4 , November 2014 , pp. 483 - 495
Copyright
Copyright © Cambridge University Press 2013 

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

Ajmat, M.T., Bonilla, F., Zelarayán, L. & Bühler, M.I. (2011). Participation of inositol trisphosphate and ryanodine receptors in Bufo arenarum oocyte activation. Zygote 19, 171–80.Google Scholar
Ajmat, M.T., Bonilla, F, Hermosilla, P.C., Zelarayán, L. & Bühler, M.I. (2013). Role of phospholipase A2 pathway in regulating activation of Bufo arenarum oocytes. Zygote 21, 214–20.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 7, 2233–44.CrossRefGoogle Scholar
Bembenek, J.N., Richie, C.T., Squirrell, J.M., Campbell, J.M., Eliceiri, K.W., Poteryaev, D., Spang, A., Golden, A. & White, J.G. (2007). Cortical granule exocytosis in C. elegans is regulated by cell cycle components including separase. Development 134, 3837–48.CrossRefGoogle Scholar
Bement, W. (1992). Signal transduction by calcium and protein linase C during egg activation. J. Exp. Zool. 263, 382–97.Google Scholar
Bement, W. & Capco, D.G. (1989). Activators of protein kinase C trigger cortical granule exocytosis, cortical contraction, and cleavage furrow formation in Xenopus laevis oocytes and eggs. J. Cell Biol. 108, 885–92.Google Scholar
Berridge, M. (1984). Inositol triphosphate and diacylglycerol as second messengers. Biochem. J. 220, 345–60.Google Scholar
Berridge, M. (1997). Elementary and global aspects of calcium signalling. J. Physiol. 499, 291–306.Google Scholar
Bonilla, F., Ajmat, M.T., Sánchez Toranzo, G., Zelarayán, L., Oterino, J. & Bühler, M.I. (2008). Activation of amphibian oocytes by sperm extracts. Zygote 16, 303–8.Google Scholar
Bühler, M.I., Petrino, T., Zelarayán, L. & Legname, A. (1994). Effects of cytoplasmic components upon sperm aster development in Bufo arenarum eggs. Dev. Biol. 164, 398–401.Google Scholar
Busa, W.B., Ferguson, J.E., Joseph, S.K., Williamson, J.R. & Nuccitelli, R. (1985). Activation of frog (Xenopus laevis) eggs by inositol trisphosphate. Characterization of Ca2+ release from intracellular stores. J. Cell Biol. 101, 677–82.CrossRefGoogle ScholarPubMed
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 Cγ. J. Cell Biol. 138, 1303–11.Google Scholar
Coward, K., Ponting, C.P., Zhang, N., Young, C., Huang, C.J., Chou, C.M., Kashir, J., Fissore, R.A. & Parrington, J. (2011). Identification and functional analysis of an ovarian form of the egg activation factor phospholipase C zeta (PLCζ) in pufferfish. Mol. Reprod. Dev. 78, 48–56.Google Scholar
Cox, L.J., Larman, M.G., Saunders, C.M., Hashimoto, K., Swann, K. & Lai, F.A. (2002). Sperm phospholipase Czeta from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction 124, 611–23.Google Scholar
Dale, B. & DeFelice, L. (2011). Polyspermy prevention: fact and artifacts? J. Ass. Reprod. Genet. 28, 199–207.Google Scholar
Dale, B., DeFelice, L. & Ehrenstein, G. (1985). Injection of a soluble sperm extract into sea urchin eggs triggers the cortical reaction. Experientia 41, 1068–70.CrossRefGoogle Scholar
Dale, B., Wilding, M., Coppola, G. & Tosti, E. (2010). How do spermatozoa activate oocytes? Reprod. Biomed. Online 21, 1–3.Google Scholar
Dong, J.B., Tang, T.S. & Sun, Z.F. (2000). Xenopus and chicken sperm contain a cytosolic soluble protein factor which can trigger calcium oscillations in mouse eggs. Biochem. Biophys. Res. Commun. 268, 947–51.Google Scholar
Douglas, K. & Kline, J.T. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149, 80–9.Google Scholar
Ducibella, T., Huneau, D., Angelichio, E., Xu, Z., Schultz, R.M., Kopf, G.S., Fissore, R., Madoux, S. & Ozil, J.P. (2002). Egg-to-embryo transition is driven by differential responses to Ca2+ oscillation number. Dev. Biol. 250, 280–91.Google Scholar
Evans, J.P. & Kopf, G.S. (1998). Molecular mechanisms of sperm-egg interactions and egg activation. Andrologia 30, 297–307.CrossRefGoogle ScholarPubMed
Folch, J., Lees, M. & Stanley, G.H.S. (1957). A simple method for the isolation and purification of total lipid from animal tissues. J. Biochem. 226, 497–509.Google Scholar
Fujimoto, S., Yoshida, N., Fukui, T., Amanai, M., Isobe, T., Itagaki, C., Izumi, T. & Perry, A.C.F. (2004). Mammalian phospholipase C zeta induces oocyte activation from the sperm perinuclear matrix. Dev. Biol. 274, 370–83.Google Scholar
Galione, A. & Summerhill, R. (1995). Regulation of ryanodine receptors by cyclic ADP-ribose. In Ryanodine Receptors (ed. Sorrentino, V.), pp. 51–70. CRC Press, Boca Raton, FL, USA.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.Google Scholar
Gould, M. & Stephano, J.L. (1991). Peptides from sperm acrosomal protein that initiate development. Dev. Biol. 146, 509–18.Google Scholar
Halet, G., Tunwell, R. & Parkinson, S.J. (2004). Conventional PKCs regulate the temporal pattern of Ca2+ oscillations at fertilization in mouse eggs. J. Cell Biol. 164, 1033–44.CrossRefGoogle ScholarPubMed
Heinecke, J.W. & Shapiro, B.M. (1992). The respiratory burst oxi dase of fertilization. A physiological target for regulation by protein kinase C. J. Biol. Chem. 267, 7959–62.Google Scholar
Hinkovska-Galchev, V. & Srivastava, P.N. (1992). Phosphatidylcholine and phosphatidylinositol-specific phospholipases C of bull and rabbit spermatozoa. Mol. Reprod. Dev. 33, 281–6.Google Scholar
Horner, V. & Wolfner, M. (2008). Transitioning from eg to embryo: triggers and mechanisms of egg activation. Dev. Dyn. 237, 527–44.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
Jones, K.T. (1998). Protein Kinase C action at fertilization overstated or undervalued? Rev. Reprod. 3, 7–12.Google Scholar
Jones, K.T., Cruttwell, C., Parrington, J. & Swann, K. (1998). A mammalian sperm cytosolic phospholipase C activity generates inositol triphosphate and causes Ca2+ release in sea urchin egg homogenates. FEBS Lett. 437, 297–300.Google Scholar
Jones, K.T., Matsuda, M., Parrington, J., Katan, M. & Swann, K. (2000). Different Ca2+ releasing abilities of sperm extracts compared with tissue extracts and phospholipase C isoforms in sea urchin eggs homogenates and mouse eggs. Biochem. J. 346, 743–9.Google Scholar
Kawano, N., Yoshida, K., Miyado, K. & Yoshida, M. (2011). Lipid rafts: keys to sperm maturation, fertilization and early embryogenesis. J. Lipids doi:10.1155/2011/264706Google Scholar
Krapf, D., O'Brien, E.D., Cabada, M.O., Visconti, P.E. & Arranz, S.E. (2009). Egg water from the amphibian Bufo arenarum modulates the ability of homologous sperm to undergo the acrosome reaction in the presence of the vitelline envelope. Biol. Reprod. 2, 311–9.Google Scholar
Kurokawa, M., Sato, K. & Fissore, R.A. (2004). Mammalian fertilization: from sperm factor to phospholipase Cζ. Biol. Cell 96, 37–45.Google Scholar
Kurokawa, M., Sato, K., Wu, H., He, C., Malcuit, C., Black, S.J., Fukami, K. & Fissore, R.A. (2005). Functional, biochemical, and chromatographic characterization of the complete [Ca2+] oscillation-inducing activity of porcine sperm. Dev. Biol. 285, 376–92.Google Scholar
Kurokawa, M., Yoon, S., Alfandari, D., Fukami, K., Sato, K. & Fissore, R.A. (2007). Proteolytic processing of phospholipase Cζ and [Ca2+]i oscillations during mammalian fertilization. Dev. Biol. 312, 407–18.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.Google Scholar
Larman, M.G., Saunders, C.M., Carroll, J., Lai, F.A. & Swann, K. (2004). Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCζ. J. Cell Sci. 117, 2513–21.Google Scholar
Lin, Y.W. & Schuetz, A.W. (1985). Intrafollicular action of estrogen in regulation pituitary-induced ovarian progesterone synthesis and oocyte maturation in Rana pipiens: temporal relationship and locus of action. Gen. Comp. Endocrinol. 58, 421–35.Google Scholar
Machaty, Z., Bonk, A.J., Kuhholzer, B. & Prather, R.S. (2000). Porcine oocyte activation induced by a cytosolic sperm factor. Mol. Reprod. Dev. 57, 290–5.Google Scholar
Malcuit, C., Knott, J.G., He, C., Wainwright, T., Parys, J.B., Robl, J.M. & Fissore, R.A. (2005). Fertilization and inositol 1,4,5-trisphosphate (IP3) induced calcium release in type-1 inositol 1,4,5-trisphosphate receptor down regulated bovine eggs. Biol. Reprod. 73, 2–13.Google Scholar
Martinez, M.L. & Cabada, M.O. (1996). Assessment of the acrosome reaction in Bufo arenarum spermatozoa by immunostaining: comparison with other methods. Zygote 4, 181–90.Google Scholar
Mateos, M.V., Uranga, R.M., Salvador, G.A. & Giusto, N.M. (2008). Activation of phosphatidylcholine signalling during oxidative stress in synaptic endings. Neurochem. Int. 53, 199–206.Google Scholar
Mehlmann, L., Chattopadhyay, A., Carpenter, G. & Jaffe, L. (2001). Evidence that phospholipase C from sperm is not responsible for initiating Ca2+ release at fertilization in mouse eggs. Dev. Biol. 236, 492–501.Google Scholar
Minahk, C., Kim, K.W., Nelson, R., Trigatti, B., Lehner, R. & Vance, D.E. (2008). Conversion of low density lipoprotein-associated phosphatidylcholine to triacylglycerol by primary hepatocytes. J. Biol. Chem. 283, 6449–58.Google Scholar
Miyazaki, S. & Ito, M. (2006). Calcium signals for egg activation in mammals. J. Pharm. Sci. 100, 545–52Google Scholar
Mizote, A., Okamoto, S. & Iwao, Y. (1999). Activation of Xenopus eggs by proteases: possible involvement of a sperm protease in fertilization. Dev. Biol. 208, 79–92.Google Scholar
Nishizuka, Y. (1984). The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308, 393–8.Google Scholar
Nuccitelli, R., Yim, D.L. & Smart, T. (1993). The sperm-induced Ca2+ wave following fertilization of the Xenopus egg requires the production of Ins(1,4,5)P3. Dev. Biol. 158, 200–12.Google Scholar
Oterino, J., Sánchez Toranzo, G., Zelarayán, L. & Bühler, M.I. (1997). Polyspermy in Bufo arenarum oocytes matured in vitro. Zygote 5, 267–71.Google Scholar
Oterino, J., Sánchez Toranzo, G., Zelarayán, L., Valz-Gianinet, J.N. & Bühler, M.I. (2001). Cortical granule exocytosis in Bufo arenarum oocytes matured in vitro. Zygote 9, 251–9.Google Scholar
Parrington, J., Swann, K., Shevchenko, V.I., Sesay, A.K. & Lai, F.A. (1996). Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 25, 364–8.Google Scholar
Parrington, J., Jones, K.T., Lai, F.A. & Swann, K. (1999). The soluble sperm factor that causes Ca2+ release from sea-urchin (Lytechinus pictus) egg homogenates also triggers Ca2+ oscillations after injection into mouse eggs. Biochem. J. 341, 1–4.Google Scholar
Parrington, J., Davis, L.C., Galione, A. & Wessel, G. (2007). Flipping the switch: how a sperm activates the egg at fertilization. Dev. Dyn. 236, 2027–38.Google Scholar
Petcoff, D.W., Holland, W.L. & Stith, B.J. (2008). Lipid levels in sperm, eggs, and during fertilization in Xenopus laevis. J. Lipid Res. 49, 2365–78.Google Scholar
Raisman, J.S., de Cunio, R.W., Cabada, M.O., del Pino, E.J. & Mariano, M.I. (1980). Acrosome breakdown in Leptodactylus chaquensis (Amphibia, Anura) spermatozoa. Dev. Growth Differ. 22, 289–97.Google Scholar
Ramoni, C., Spadaro, F., Menegon, M. & Podo, F. (2001). Cellular localization and functional role of phosphatidylcholine-specific phospholipase C in NK cells. J. Immunol. 167, 2642–50.Google Scholar
Ramoni, C., Spadaro, F., Barletta, B., Dupuis, M.L. & Podo, F. (2004). Phosphatidylcholine-specific phospholipase C in mitogen-stimulated fibroblasts. Exp. Cell Res. 299, 370–82.Google Scholar
Rice, A., Parrington, J., Jones, K.T. & Swann, K. (2000). Mammalian sperm contain a Ca2+ sensitive phospholipase C activity that can generate InsP3 from PIP2 associated with intracellular organelles. Dev. Biol. 227, 125–35.Google Scholar
Richert, S., Luche, S., Chevallet, M., Van Dorsselaer, A., Leize-Wagner, E. & Rabilloud, T. (2004). About the mechanism of interference of silver staining with peptide mass spectrometry. Proteomics 4, 909–16.Google Scholar
Rogers, N.T., Hobson, E., Pickering, S., Lai, F.A., Braude, P. & Swann, K. (2004). Phospholipase Cζ causes Ca2+ oscillations and parthenogenetic activation of human oocytes.Reproduction 128, 697–702.Google Scholar
Roldan, E.R. & Shi, Q.X. (2007). Sperm phospholipases and acrosomal exocytosis. Front Biosci. 1, 89–104.CrossRefGoogle 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
Runft, L.L., Carroll, D.J., Gillett, J., Giusti, A. F., O'Neill, F.J. & Foltz, K.R. (2004). Identification of a starfish egg PLCγ that regulates Ca2+ release at fertilization. Dev. Biol. 269, 220–36.Google Scholar
Sánchez Toranzo, G., Oterino, J., Zelarayán, L., Bonilla, F. & Bühler, M.I. (2007). Spontaneous and LH-induced maturation in Bufo arenarum oocytes: importance of gap junctions. Zygote 15, 65–80.Google Scholar
Sato, K., Tokmakov, A.A., Iwasaki, T. & Fukami, Y. (2000). Tyrosine kinase-dependent activation of phospholipase Cɣ is required for calcium transient in Xenopus egg fertilization. Dev. Biol. 224, 453–69.Google Scholar
Sato, K., Fukami, Y. & Stith, B.J. (2006). Signal transduction pathways leading to Ca2+ release in a vertebrate model system: lessons from Xenopus eggs. Semin. Cell. Dev. Biol. 17, 285–92.CrossRefGoogle 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
Sheikhnejad, R.G. & Srivastava, P.N. (1986). Isolation and properties of a phosphatidylcholine-specific phospholipase C from bull seminal plasma. J. Biol. Chem. 261, 7544–9.CrossRefGoogle ScholarPubMed
Singer, W.D., Brown, H.A. & Sternweis, P.C. (1997). Regulation of eukaryotic phosphatidylinositol-specific phospholipase C and phospholipase D. Annu. Rev. Biochem. 66, 475–509.Google Scholar
Snow, P., Yim, D.L., Leibow, J.D., Saini, S. & Nuccitelli, R. (1996). Fertilization stimulates an increase in inositol trisphosphate and inositol lipid levels in Xenopus eggs. Dev. Biol. 180, 108–18.Google Scholar
Spadaro, F., Cecchetti, S., Sanchez, M., Ausiello, C.M., Podo, F. & Ramoni, C. (2006). Expression and role of phosphatidylcholine-specific phospholipase C in human NK and T lymphocyte subsets. Eur. J. Immunol. 36, 3277–87.Google Scholar
Stephens, S., Beyer, B., Balthazar-Stablein, U., Duncan, R., Kostacos, M., Lukoma, M., Green, G.R. & Poccia, D. (2002). Two kinase activities are sufficient for sea urchin sperm chromatin decondensation in vitro. Mol. Reprod. 62, 496–503.Google Scholar
Stith, B.J., Goalstone, M., Silva, S. & Jaynes, C. (1993). Inositol 1,4,5-trisphosphate mass changes from fertilization through first cleavage in Xenopus laevis. Mol. Biol. Cell 4, 435–43.Google Scholar
Stith, B.J., Woronoff, K., Espinoza, R. & Smart, T. (1997). sn-1,2-diacylglycerol and choline increase after fertilization in Xenopus laevis. Mol. Biol. Cell 4, 755–65.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., Larman, M.G., Saunders, C.M. & Lai, F. (2004). The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCζ. Reproduction 127, 431–9.Google Scholar
Szumiło, M. & Rahden-Staroń, I. (2008). Biol. role of phosphatidylcholine-specific phospholipase C in mammalian cells. Postepy. Hig. Med. Dosw. (Online) 62, 593–8.Google Scholar
Talevi, R., Dale, B. & Campanella, C. (1985). Fertilization and activation potentials in Discoglossus pictus (Anura) eggs: A delayed response to activation by pricking. Dev. Biol. 111, 316–23.Google Scholar
Whitaker, M.J. & Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 1–12.Google Scholar
Whitaker, M. & Zimmerberg, J. (1987). Inhibition of secretory granule discharge during exocytosis in sea urchin eggs by polymer solutions. J. Physiol. (London) 389, 527–39.Google Scholar
Wilding, M. & Dale, B. (1998). Soluble extracts from ascidian spermatozoa trigger intracellular calcium release independently of the activation of the ADP ribose channel. Zygote 6, 149–55.Google Scholar
Wilding, M., Kyozuka, K., Ruso, G.L., Tosti, E. & Dale, B. (1997). A soluble extract from human spermatozoa activates ascidian oocytes. Dev. Growth Differ. 39, 329–36.Google Scholar
Wolny, Y.M., Fissore, R.A., Wu, H., Reis, M.M., Colombero, L.T., Ergün, B., Rosenwaks, Z. & Palermo, G.D. (1999). Human glucosamine-6-phosphate isomerase, a homologue of hamster oscillin, does not appear to be involved in Ca2+ release in mammalian oocytes. Gamete Biol. 53, 277–87.Google Scholar
Wu, H., Smyth, J., Luzzi, V., Fukami, K., Takenawa, T., Black, S.L., Allbritton, N.L. & Fissore, R. (2001). Sperm factor induces intracellular free calcium oscillations by stimulating the phosphoinositide pathway. Biol. Reprod. 64, 1338–49.Google Scholar
Wu, X., Zhang, X., Li, W., Cheng, H., Kuai, Y., Wang, S. & Guo, Y.-L. (2006). Translocation of classical PKC and cortical granule exocytosis of human oocyte in germinal vesicle and metaphase II stage. Acta Pharmacologica Sinica 27, 1353–8.Google Scholar
Yamaga, M., Kawai, K., Kiyota, M., Homma, Y. & Yagisawa, H. (2007). Recruitment and activation of phospholipase C (PLC)-d1 in lipid rafts by muscarinic stimulation of PC12 cells: contribution of p122RhoGAP/DLC1, a tumor-suppressing PLCd1 binding protein. Adv. Enzyme Regul. 48, 41–54.Google Scholar
Yue, C., White, K.L., Reed, W.A. & Bunch, T.D. (1995). The existence of inositol 1,4,5-trisphosphate and ryanodine receptors in mature bovine oocytes. Development 8, 2645–54.Google Scholar