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Activation of amphibian oocytes by sperm extracts

Published online by Cambridge University Press:  01 November 2008

F. Bonilla ,
M. T. Ajmat ,
G. Sánchez Toranzo ,
L. Zelarayán ,
J. Oterino  and
M. I. Bühler
F. Bonilla
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
M. T. Ajmat
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
G. Sánchez Toranzo
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
L. Zelarayán
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
J. Oterino
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
M. I. Bühler*
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
*
All correspondence to: Marta I. Bühler. Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina, Fax: +54 381 4248025. e-mail: [email protected]
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Summary

In the fertilization of most animals, egg activation is accompanied by an increase in cytoplasmatic Ca2+; however, the mechanism through which the fertilizing sperm induce this phenomenon is still controversial. An increase in intracellular free Ca2+ is required to trigger egg activation events, a process that includes cortical granule exocytosis, resumption and completion of meiosis and DNA replication, and culminates in the first mitotic cleavage. In this work, we investigated the effect of microinjection and incubation of different fractions of homologous sperm extract on the activation of Bufo arenarum oocytes matured in vitro. Two heat treatment-sensitive fractions obtained by chromatography were able to induce oocyte activation. The sperm fraction, which contained a 24 kDa protein, induced 90% activation when it was microinjected into the oocytes. Whilst the sperm fraction, which contained a 36 kDa protein, was able to induce about 70% activation only when it was applied on the oocyte surface.

Keywords

Bufo arenarumOocyte activationSperm extracts
Type
Research Article
Information
Zygote , Volume 16 , Issue 4 , November 2008 , pp. 303 - 308
Copyright
Copyright © Cambridge University Press 2008

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References

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. & De Felice, L.J. (1990) Soluble sperm factors, electrical events and egg activation. In Mechanisms of fertilization (ed. Dale, B.) NATO ASI Series Vol. H 45. Berlin: Springer–Verlag.Google Scholar
Dong, J.B., Tang, T.S. & Sun, F.Z. (2000). Xenopus and Chiquen sperm contain a cytosolic soluble protein factor which can trigger calcium oscillations in mouse eggs. Biochem. Biophys. Res. Com. 268, 947–51.CrossRefGoogle ScholarPubMed
Gómez, M.I.. Santolaya, R.C. & Cabada, M.O. (1984). Exocytosis of cortical granules from activated oocytes of the toad, Bufo arenarum. Cell. Tissue Res. 237, 191–4.CrossRefGoogle ScholarPubMed
Iwamatsu, T., Yoshimoto, Y. & Hiramoto, Y. (1988). Mechanisms of Ca2+ release in medaka eggs microinjected with inositol 1,4,5-trisphosphate and Ca2+. Dev. Biol. 129, 191–7.CrossRefGoogle ScholarPubMed
Iwao, Y. (2000). Mechanism of eggs activation and polyspermy block in amphibians and comparative aspects with fertilization in other vertebrates. Zool. Sci. 17, 699–709.CrossRefGoogle Scholar
Iwao, Y., Kobayashi, M., Miki, A., Kubota, H.Y. & Yoshimoto, Y. (1995). Activation of Xenopus egg by Cynops sperm extract is dependent upon both extra- and inter-cellular Ca activities. Zool. Sci. 12, 572–81.CrossRefGoogle Scholar
Iwao, Y. & Fujimura, T. (1996). Activation of Xenopus eggs by RGD-containing peptides accompanied by intracellular Ca2+ release. Dev. Biol. 177, 558–67.CrossRefGoogle ScholarPubMed
Jaffe, L.A., Giusti, A.F., Carroll, D.J. & Foltz, K.R. (2001). Ca2+ signaling during fertilization of equinoderm eggs. Cell. Dev. Biol. Vol. 12, pp. 45–51.Google ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Kanner, S.B., Grosmaire, L.S., Ledbetter, J.A. & Damle, N.K. (1993). Beta2-integrin LFA-1 signaling through phospholipase C-gamma 1 activation. Proc. Natl. Acad. Sci. U. S. A. 190 (15), 7099–103.CrossRefGoogle Scholar
Kimura, Y., Yanagimachi, R., Kuretake, S., Bortkiewiez, H., Perry, A.C. & Yanagimachi, H. (1998). Analysis of mouse oocyte activation suggests the involvement of sperm perinuclear material. Biol. Reprod. 58, 1407–15.CrossRefGoogle ScholarPubMed
Kouchi, Z., Fukami, K., Shikano, T., Oda, S., Nakamura, Y., Takenawa, T. & Miyazaki, S. (2004). Recombinant phospholipase Cζ has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse eggs. J. Biol. Chem. 279, 10408–12.CrossRefGoogle ScholarPubMed
Kuretake, S., Kimura, Y., Hoshi, K. & Yanagimachi, R. (1996). Fertilization and development of mouse oocytes inject with isolated sperm heads. Biol. Reprod. 55, 789–95.CrossRefGoogle ScholarPubMed
Kurokawa, M., Sato, K. & Fissore, R.A. (2004). Mammalian fertilization: from sperm factor to phospholipase Czeta. Biol. Cell. 96, 37–45.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.CrossRefGoogle ScholarPubMed
Lin, Y.P. & Schuetz, A.W. (1985). Spontaneous oocyte maturation in Rana pipiens: estrogen and follicle wall involvement. Gamete Res. 12, 11–28l.CrossRefGoogle Scholar
Llanos, R.J, Whitacre, C. & Miceli, D.C. (2000). Potential involvement of C3 complement factor in amphibian fertilization. Comp. Biochem. Physiol. 127, 29–38.CrossRefGoogle ScholarPubMed
Machaty, Z., Bonk, A.J., Kühholzer, B. & Prather, R.S. (2000) Porcine oocyte activation induced by a cytosolic sperm factor. Mol. Reprod. Dev. 57, 290–5.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Miyazaki, S., Yuzaki, M., Nakada, K., Shirakawa, H., Nakanishi, S., Nakade, S. & Mikoshiba, K. (1992). Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5- trisphosphate receptor in fertilized hamster eggs. Science 257, 251–5.CrossRefGoogle 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
Nuccitelli, R., Yim, D.L. & Smarta, 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.CrossRefGoogle ScholarPubMed
Oterino, J., Sanchez Toranzo, G., Zelarayan, L., Valz-Gianinet, J.N. & Bühler, M.I. (2001). Cortical granule exocytosis in Bufo arenarum oocytes matured in vitro. Zygote 9, 251–9.CrossRefGoogle ScholarPubMed
Oterino, J., Sanchez Toranzo, G., Zelarayan, L., Ajmat, M.T., Bonilla, F. & Buhler, M.I. (2006). Behaviour of the vitelline envelope in Bufo arenarum oocytes matured in vitro in blockade to polyspermy. Zygote 14 (2), 97–106.CrossRefGoogle ScholarPubMed
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 25.379 (6563), 364–8.CrossRefGoogle Scholar
Rice, A., Parrington, J., Jones, K. & 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.CrossRefGoogle Scholar
Runft, L.L., Watras, J. & Jaffe, L.A. (1999). Calcium release at fertilization of Xenopus eggs requires type I IP3 receptors, but not SH2 domain-mediated activation of PLCgamma or G(q)-mediated activation of PLCbeta. Dev. Biol. 223, 399–411.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Saunders, C.M., Larman, M.G., Parrington, J., Cox, L.J., Royse, J., Blayney, L.M., Swann, K. & Lai, F.A. (2002). PLCzeta: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–44.CrossRefGoogle Scholar
Shilling, F., Craig, M. & Nuccitelli, R. (1998). Voltage-dependent activation of frog eggs by a sperm surface disintegrin peptide. Dev. Biol. 202, 113–24.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 (4), 435–43.CrossRefGoogle ScholarPubMed
Stricker, S.A. (1999) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211, 157–76.CrossRefGoogle ScholarPubMed
Swann, K. & Lai, F.A. (1997) A novel signaling mechanism for generating Ca2+ oscillations at fertilization in mammals. BioEssays 19, 371–8.CrossRefGoogle ScholarPubMed
Whitaker, M.J. & Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 1–12.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Wolny, Y., Fissore, R.A., Wu, H., Reis, M.M., Colombero, R.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. Mol. Reprod. Dev. 52, 277–87.3.0.CO;2-0>CrossRefGoogle Scholar
Wu, H., Smyth, J., Luzzi, V., Fukami, K., Takenawa, T., Black, S.L., Allbritton, N.L. & Fissore, R.A. (2001). Sperm factor induces intracellular free calcium oscillations by stimulating the phosphoinositide pathway. Biol. Reprod. 64, 1338–49.CrossRefGoogle ScholarPubMed