Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-06-20T20:34:04.413Z Has data issue: false hasContentIssue false

Participation of inositol trisphosphate and ryanodine receptors in Bufo arenarum oocyte activation

Published online by Cambridge University Press:  30 September 2010

M.T. Ajmat
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
F. Bonilla
Affiliation:
Instituto de Biología, Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
L. Zelarayán
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
M.I. Bühler*
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
*
All correspondence to Marta I. Bühler. Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina. Fax: +54 381 4248025. e-mail: mbuhler@fbqf.unt.edu.ar

Summary

Calcium is considered the most important second messenger at fertilization. Transient release from intracellular stores is modulated through both agonist-gated channels, IP3Rs and RyRs, which can be found individually or together depending on the oocyte species. Using the four commonly used compounds (thimerosal, caffeine, heparin and ruthenium red), we investigated the existence and interdependence of both IP3Rs and RyRs in mature Bufo arenarum oocytes. We found that caffeine, a well known specific RyRs agonist, was able to trigger oocyte activation in a dose-dependent manner. Microinjection of 10 mM caffeine showed 100% of oocytes exhibiting characteristic morphological criteria of egg activation. Ruthenium red, the specific RyR blocker, was able to inhibit oocyte activation induced either by sperm or caffeine. Our present findings provide the first reported evidence of the existence of RyR in frogs. We further explored the relationship between IP3Rs and RyRs in B. arenarum oocytes by exposing them to the agonists of one class after injecting a blocker of the other class of receptor. We found that thimerosal overcame the inhibitory effect of RyR on oocyte activation, indicating that IP3Rs function as independent receptors. In contrast, previous injection of heparin delayed caffeine-induced calcium release, revealing a relative dependence of RyRs on functional IP3Rs, probably through a CICR mechanism. Both receptors play a role in Ca2+ release mechanisms although their relative contribution to the activation process is unclear.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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

Abbott, A.L. & Ducibella, T. (2001). Calcium and the control of mammalian cortical granule exocytosis. Front. Biosci. 6, D792806.Google Scholar
Albrieux, M., Sardet, C. & Villaz, M. (1997). The two intracellular Ca2+ release channels, ryanodine receptor and inositol 1,4,5-trisphosphate receptor, play different roles during fertilization in ascidians. Dev. Biol. 189, 174–85.CrossRefGoogle ScholarPubMed
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
Balakier, H., Dziak, E., Sojecki, A., Librach, C., Michalak, M. & Opas, M. (2002). Calcium-binding proteins and calcium-release channels in human maturing oocytes, pronuclear zygotes and early preimplantation embryos. Hum. Reprod. 17, 2938–47.Google Scholar
Berridge, M.J. (1993). A tale of two messengers. Nature 365, 388–9.Google Scholar
Berridge, M.J. (1996). Microdomains and elemental events in calcium signalling. Cell Calcium 20, 95–6.Google Scholar
Bird, G.S., Burgess, G.M. & Putney, J.W. (1993). Sulfhydryl reagents and cAMP-dependent kinase increase the sensivity of the inositol 1,4,5-trisphosphate receptor in hepatocytes. J. Biol. Chem. 268, 17917–23.CrossRefGoogle Scholar
Bootman, M.D., Taylor, C.W. & Berridge, M.J. (1992). The thiol reagent, thimerosal, evokes Ca2+ spikes in HeLa cells by sensitizing the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 267, 25113–9.Google Scholar
Buck, W.R., Rakow, T.L. & Shen, S.S. (1992). Synergistic release of calcium in the sea urchin egg by caffeine and ryanodine. Exp. Cell Res. 202, 5966.Google Scholar
Buck, W.R., Hoffmann, E.E., Rakow, T.L. & Shen, S.S. (1994). Synergistic calcium release in the sea urchin egg by ryanodine and cyclic ADP ribose. Dev. Biol. 163, 110.Google Scholar
Carroll, J. & Swann, K. (1992). Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes. J. Biol. Chem. 267, 11196–201.Google Scholar
Clapper, D.L. & Lee, H.C. (1985). Inositol trisphosphate induces calcium release from nonmitochondrial stores in sea urchin homogenates. J. Biol. Chem. 260, 13947–54.Google Scholar
Collas, P., Fissore, R., Robl, J.M., Sullivan, E.J. & Barnes, F. (1993). Electrically induced calcium elevation, activation, and parthenogenetic development of bovine oocytes. Mol. Rep. Dev. 34, 212–23.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, 3851–60.Google Scholar
Dekel, N. (2005). Cellular, biochemical and molecular mechanisms regulating oocyte maturation. Mol. Cell. Endocrinol. 234, 1925.Google Scholar
Erickson, E.S., Mooren, O.L., Moore-Nichols, D. & Dunn, R.C. (2004). Activation of ryanodine receptors in the nuclear envelope alters the conformation of the nuclear pore complex. Biophys. Chem. 112, 17.CrossRefGoogle ScholarPubMed
Erlich, B.E., Kaftan, E., Bezprozvannaya, S. & Brezprozvanny, I. (1994). The pharmacology of intracellular Ca 2+ release channels. Trends Pharmacol. Sci. 15, 145–9.Google Scholar
Ferrell, J.E. Jr. (1999). Xenopus oocyte maturation: new lessons from a good egg. Bioessays 10, 833–42.Google Scholar
Fissore, R.A. & Robl, J.M. (1993). Sperm, inositol trisphosphate and thimerosal-induced intracellular calcium elevations in rabbit eggs. Dev. Biol. 159, 122–30.Google Scholar
Fissore, R.A., Dobrinsky, J.R., Balise, J.J., Duby, R.T. & Robl, J.M. (1992). Patterns of intracellular Ca2+ concentrations in fertilized bovine eggs. Biol. Reprod. 47, 960–9.Google Scholar
Galione, A., Lee, H.C. & Busa, W.B. (1991). Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253, 1143–6.Google Scholar
Galione, A., McDougall, A., Busa, W.B., Willmott, N., Gillot, I. & Whitaker, M. (1993a). Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science 261, 348–52.Google Scholar
Galione, A., White, A., Willmott, N., Turner, M., Potter, B.V. & Watson, S.P. (1993b). cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365, 456–9.Google Scholar
Goud, P.T., Goud, A.P., Van Oostveldt, P. & Dhont, M. (1999). Presence and dynamic redistribution of type I inositol 1,4,5-trisphosphate receptors in human oocytes and embryos during in-vitro maturation, fertilization and early cleavage divisions. Mol. Hum. Reprod. 5, 441–51.Google Scholar
Herbert, M., Gillespie, J.I., Murdoch, A.P. (1997). Development of calcium signalling mechanisms during maturation of human oocytes. Mol. Hum. Reprod. 3, 965–73.Google Scholar
Hilly, M., Pietri-Rouxel, F., Coquil, J.F. & Mauger, J.P. (1993). Thiol agents increase the affinity of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 268, 16488–94.Google Scholar
Horner, V.L. & Wolfner, M.F. (2008). Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev. Dynam. 237, 527–44.Google Scholar
Kline, J.T. & Kline, D. (1994). Regulation of intracellular calcium in the mouse egg: evidence for inositol trisphosphate-induced calcium release, but not calcium-induced calcium release. Biol. Reprod. 50, 193203.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
Macháty, Z., Funahashi, H., Day, B.N. & Prather, R.S. (1997). Developmental changes in the intracellular Ca2+ release mechanisms in porcine oocytes. Biol. Reprod. 56, 921–30.Google Scholar
Maes, K., Missiaen, L., Parys, J.B., Sienaert, I., Bultynck, G., Zizi, M., De Smet, P., Casteels, R. & De Smedt, H. (1999). Adenine-nucleotide binding sites on the inositol 1,4,5-trisphosphate receptor bind caffeine, but not adenophostin A or cyclic ADP-ribose. Cell Calcium 25, 143–52.Google Scholar
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.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, 6278.Google Scholar
McPherson, S.M., McPherson, P.S., Mathews, L., Campbell, K.P. & Longo, F.J. (1992). Cortical localization of a calcium release channel in sea urchin eggs. J. Cell Biol. 116, 1111–21.Google Scholar
Nuccitelli, R. (1991). How do sperm activate eggs? Curr. Top. Dev. Biol. 25, 116.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., Valz-Gianinet, J.N. & Bühler, M.I. (2001). Cortical granule exocytosis in Bufo arenarum oocytes matured in vitro. Zygote 9, 251–9.Google Scholar
Parys, J.B., Sernett, S.W., DeLisle, S., Sayder, P.M., Welsh, M.J. & Campbell, K.P. (1992). Isolation, characterization and localization of the inositol 1,4,5-trisphosphate receptor protein in Xenopus laevis oocytes. J. Biol. Chem. 267, 18776–82.Google Scholar
Parys, J.B., McPherson, S.M., Matthews, L., Campbell, K.P. & Longo, F.J. (1994). Presence of inositol 1,4,5-trisphosphate receptor, calreticulin and calsequestrin in eggs of sea urchin and Xenopus laevis. Dev. Biol. 161, 466–76.Google Scholar
Petr, J., Urbánková, D., Tománek, M., Rozinek, J. & Jílek, F. (2002). Activation of in vitro matured pig oocytes using activators of inositol triphosphate or ryanodine receptors. Anim. Reprod. Sci. 70, 235–49.Google Scholar
Rickords, L.F. & White, K.L. (1993). Electroporation of inositol 1,4,5-trisphosphate induces repetitive calcium oscillations in murine oocytes. J. Exp. Zool. 265, 178–84.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
Schultz, R.M. & Kopft, G.S. (1995). Molecular basis of mammalian egg activation. Curr. Topics Dev. Biol. 30, 2162.Google Scholar
Sousa, M., Barros, A. & Tesarik, J. (1996). The role of ryanodine-sensitive Ca2+ stores in the Ca2+ oscillation machine of human oocytes. Mol. Hum. Reprod. 2, 265–72.CrossRefGoogle ScholarPubMed
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. (1992). Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem. J. 287, 7984.Google Scholar
Swann, K. & Ozil, J.P. (1994). Dynamics of the calcium signal that triggers mammalian egg activation. Int. Rev. Cytol. 152, 183215.Google Scholar
Tanaka, Y. & Tashjian, A.H. Jr. (1994). Thimerosal potentiates Ca2+ release mediated by both the inositol 1,4,5-trisphosphate and the ryanodine receptors in sea urchin eggs. Implications for mechanistic studies on Ca2+ signaling. J. Biol. Chem. 269, 11247–53.Google Scholar
Tesarik, J. (2002). Calcium signalling in human oocytes and embryos: two-store model revival. Hum. Reprod. 17, 2948–9.Google Scholar
Wang, L., White, K.L., Reed, W.A. & Campbell, K.D. (2005). Dynamic changes to the inositol 1,4,5-trisphosphate and ryanodine receptors during maturation of bovine oocytes. Cloning Stem Cells 7, 306–20.Google Scholar
Whitaker, M. & Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 112.Google Scholar
White, K.L., Bunch, T.D., Reed, W.A., Wang, S. & Yue, C. (1993). Bovine oocyte activation is mediated by IP3-sensitive intracellular calcium pools. 26th Annual Meeting Society for The Study of Reproduction. Abstract #346.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 121, 2645–54.Google Scholar
Yue, C., White, K.L., Reed, W.A. & King, E. (1998). Localization and regulation of ryanodine receptor in bovine oocytes. Biol. Reprod. 58, 608–14.Google Scholar