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Cyclopiazonic acid induces accelerated progress of meiosis in pig oocytes

Published online by Cambridge University Press:  26 September 2008

Jaroslav Petr ,
Jirří Rozinek  and
František Jílek
Jaroslav Petr*
Affiliation:
Research Institute of Animal Production and Czech University of Agriculture, Prague, Czech Republic
Jirří Rozinek
Affiliation:
Research Institute of Animal Production and Czech University of Agriculture, Prague, Czech Republic
František Jílek
Affiliation:
Research Institute of Animal Production and Czech University of Agriculture, Prague, Czech Republic
*
Ing. Jaroslav Petr DrSc, Research Institute of Animal Production, 104 00 Prague 10–Uhříněves, Czech Republic. Tel: +42 2 67711747. Fax: +42 2 67710779.
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Summary

In mammalian oocytes, calcium plays an important role in the regulation of meiotic maturation. In our study, we used the mycotoxin cyclopiazonic acid (CPA), an inhibitor of calcium-dependent ATPases, to mobilise intracellular calcium deposits during in vitro maturation of pig oocytes. The CPA treatment of maturing oocytes significantly accelerated the progress of their maturation. Oocytes entered the CPA-sensitive period after 21 h of in vitro culture. A very short (5 min) exposure to CPA (100 mM) is sufficient to accelerate maturation and it seems that accelerated maturation can be triggered by a transient elevation of intracellular calcium levels. The effect of CPA is not mediated through the cumulus cells, because maturation is accelerated by CPA treatment even in oocytes devoid of cumulus cells. Culture of oocytes with the calcium channel blocker verapamil (concentrations ranging from 0.01 to 0.04 mM) blocked the progress of oocyte maturation beyond the stage of metaphase I. This block can be overcome by the mobilisation of intracellular calcium deposits after CPA treatment (100 nM). The microinjection of heparin (20 pl, 50.1 mg/;ml), the inhibitor of inositol triphosphate receptors, before CPA treatment prevented the acceleration of oocyte maturation. This indicates that CPA mobilises the release of calcium deposits through inositol trisphosphate receptors. On the other hand, the microinjection of procaine (20 pl, 200 nM) or the microinjection of ruthenium red (20 pl, 50 mM), both inhibitors of ryanodine receptors, did not prevent accelerated maturation in CPA-treated oocytes. If present in pig oocytes, ryanodine receptors evidently play no part in the liberation of calcium from intracellular stores after CPA treatment.

Keywords

CalciumCyclopiazonic acidMaturationOocytePig
Type
Article
Information
Zygote , Volume 5 , Issue 3 , August 1997 , pp. 193 - 205
Copyright
Copyright © Cambridge University Press 1997

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References

Anderson, E. & Albertini, D. F. (1976). Gap-junction between the oocyte and companion follicle cells in the mammalian ovary. J. Cell Biol. 71, 680–6.CrossRefGoogle ScholarPubMed
Bae, I.H. & Channing, C.P. (1985). Effect of calcium ion on the maturation of cumulus-enclosed pig follicular oocytes isolated from medium-sized Graafian follicles. Biol. Reprod. 3, 79–87.CrossRefGoogle Scholar
Berridge, M.J. (1995). Capacitative calcium entry. Biochem. J. 312, 1–11.CrossRefGoogle ScholarPubMed
Borgers, M., Thoné, F. & vanNueten, J.M. (1981). The subcellular distribution of calcium and the effects of calcium-antagonists as evaluated with a combined oxalate– pyroantimonate technique. Acta HistoChem., Suppl. 24, 327–32.Google ScholarPubMed
Carroll, J. & Swann, K. (1992). Spontaneous cytosolic calcium oscillations driven by inositol triphosphate occur during in vitro maturation of mouse oocytes. J. Biol. Chem. 267, 11196–201.CrossRefGoogle Scholar
Carroll, J., Swann, K., Whittingham, D. & Whitaker, M. (1994). Spatiotemporal dynamics of intracellular [Ca2+](i)oscillations during the growth and meiotic maturation of mouse oocytes.Development 120, 3507–17.CrossRefGoogle ScholarPubMed
Cheng, T.C. & Benton, H.P. (1994). The intracellular Ca2+ pump inhibitors thapsigargin and cyclopiazonic acid induce stress proteins in mammalian chondrocytes. Biochem. J. 301, 563–8.CrossRefGoogle ScholarPubMed
Chian, R.C. & Niwa, K. (1994). Completion of first meiosis by sperm penetration in vitro of bovine oocytes inhibited at metaphase-I with dimethylsulphoxide.Theriogenology 42, 55–64.CrossRefGoogle ScholarPubMed
Chian, R.C., Niwa, K. & Nakahara, H. (1992). Effect of sperm penetration in vitro on completion of first meiosis of bovine oocytes arrested at various stages in culture. J. Reprod. Fertil. 96, 73–8.CrossRefGoogle ScholarPubMed
Clapham, D.E. (1995). Calcium signaling. Cell 80, 259–68.CrossRefGoogle ScholarPubMed
Clapper, D.L. & Lee, H.C. (1985). Inisitol triphosphate induces calcium release from nonmitochondrial stores in sea urchin egg homogenates. J. Biol. Chem. 260, 13947–54.CrossRefGoogle Scholar
Collas, P., Chang, T., Long, C. & Robl, J.M. (1995). Inactivation of histone h1 kinase by Ca2+ in rabbit oocytes. Mol. Repord. Dev. 40, 253–8CrossRefGoogle ScholarPubMed
Demaurex, N., Lew, D.P. & Krause, K.H. (1992). Cyclopiazonic acid depletes intracellular Ca2+ stores and activates an influx pathway for divalent cations in HL-60 cells.J. Biol. Chem. 267, 2318–24.CrossRefGoogle ScholarPubMed
Fissore, R.A. & Robl, J.M. (1993). Sperm inositol triphosphate, and thimerosal–induced intracellular calcium elevation in rabbit eggs. Dev. Biol. 159, 122–30.CrossRefGoogle Scholar
Goeger, D.E., Riley, R.T., Dorner, J.W. & Cole, R.J. (1988). Cyclopiazonic acid inhibition of the Ca2+ ATPase in rat skeletal muscle sarcoplasmic reticulum vesicles. Biochem. Pharmacol. 37, 978–81.CrossRefGoogle ScholarPubMed
Hashimoto, N. & Kishimoto, T. (1988). Regulation of meiotic metaphase by a cytoplasmic maturation promoting factor during mouse oocyte maturation. Dev. Biol. 126, 242–52.CrossRefGoogle ScholarPubMed
Hepler, P.K. (1992). Calcium and mitosis. Int. Rev. Cytol. 138, 239–68.CrossRefGoogle ScholarPubMed
Hepler, P.K. (1994). The role of calcium in cell division. Cell Calcium 16, 322–30.CrossRefGoogle ScholarPubMed
Higuchi, Y., Nishimura, J., Kobayashi, S. & Kanaide, H. (1996). CPA induces a sustained increase in [Ca2+] in endothelial cells in situ and relaxes porcine coronary artery. Am. J. Physiol. 39, H2038–49.Google Scholar
Hill, T.D., Berggren, P.O. & Boynton, A.L. (1987). Heparin inhibits inositol triphosphate-induced calcium release from permeabilized rat liver cells. Biochem. Biophys. Res. Commun. 149, 897–901.CrossRefGoogle Scholar
Homa, S.T. (1991). Neomycin, an inhibitor of phosphoinositide hydrolysis, inhibits the resumption of bovine oocyte spontaneous meiotic maturation. J. Exp. Zool. 258, 95–103.CrossRefGoogle ScholarPubMed
Homa, S.T., Carroll, J. & Swann, K. (1993). The role of calcium in mammalian oocyte maturation and egg activation. Hum. Reprod. 8, 1274–81.CrossRefGoogle ScholarPubMed
Hoth, M. & Penner, R. (1992). Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355, 353–6.CrossRefGoogle ScholarPubMed
Hoth, M. & Penner, R. (1993). Calcium release-activated calcium current in rat mast cells. J. Physiol. (Lond.) 465, 359–86.CrossRefGoogle ScholarPubMed
Imaizumi, Y., Suzuki, M., Uyama, Y., Muraki, K. & Watanabe, M. (1992). Effect of cyclopiazonic acid, a novel Ca2+-ATPase inhibitor, on contractile response and an outward current in smooth muscle. Jpn. J. Pharmacol. 58 (Suppl. 2), 401P.CrossRefGoogle Scholar
Isobe, N., Fujihara, M. & Terada, T. (1996). Cumulus cells suppress meiotic progression in pig oocytes cultured in vitro. Theriogenology 45, 1479–89.CrossRefGoogle Scholar
Izant, J.G. (1983). The role of calcium ions during mitosis: calcium participates in the anaphase trigger. Chromosoma 88, 101–7.CrossRefGoogle ScholarPubMed
Jagiello, C., Ducayen, B., Downey, R. & Jonassen, A. (1982). Alterations of mammalian oocyte meiosis I with divalent cations and calmodulin. Cell Calcium 3, 153–62.CrossRefGoogle ScholarPubMed
Kaufman, M.L. & Homa, S.T. (1993). Defining a role for calcium in the resumption and progression of meiosis in the pig oocytes. J. Exp. Zool. 265, 69–76.CrossRefGoogle Scholar
Kline, J.T. & Kline, D. (1994). Regulation of intracellular calcium in the mouse egg: evidence for inositol triphosphate-induced calcium release, but not calcium-induced calcium release. Biol. Reprod. 50, 193–203.CrossRefGoogle Scholar
Kobrinsky, E., Ondrias, K. & Marks, A.R. (1995). Expressed ryanodine receptors can substitute for inositol 1,4,5-triphosphate receptor in Xenopus laevis oocyte during progesterone-induced maturation. Dev. Biol. 172, 531–50.CrossRefGoogle ScholarPubMed
Lefevre, B., Pesty, A. & Testart, J. (1995). Cytoplasmic and nucleic calcium oscillations in immature mouse oocytes: evidence of wave polarization by confocal imaging. Exp. Cell Res. 218, 166–73.CrossRefGoogle ScholarPubMed
Longo, F.J., Cook, S. & Mathews, L. (1991). Pronuclear formation in starfish eggs inseminated at different stages of meiotic maturation: correlation of sperm nuclear transformations and activity of the maternal chromatin. Dev. Biol. 147, 62–72.CrossRefGoogle ScholarPubMed
Mason, M.J., Garcia-Rodriguez, C. & Grinstein, S. (1991). Coupling between intracellular Ca2+ stores and Ca2+ permeability of the plasma membrane: comparison of effect of thapsigargin, 2,5-di-(tert-butyl)-1,4-hydroquinone, and cyclopiazonic acid in rat thymic lymphocytes.J. Biol. Chem. 266, 20856–62.CrossRefGoogle Scholar
Masui, Y. (1991). The role of cytostatic factor (CSF) in the control of oocyte cell cycle: a summary of 20 years' study. Dev. Growth Differ. 33, 543–51.CrossRefGoogle Scholar
Mehlmann, L.M. & Kline, D. (1994). Regulation of intracellular calcium in the mouse egg: calcium release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol. Reprod. 51, 1088–98.CrossRefGoogle ScholarPubMed
Mehlmann, L.M., Terasaki, M., Jaffe, L.A. & Kline, D. (1995). Reorganization of the endoplasmic reticulum during meiotic maturation of the mouse oocyte. Dev. Biol. 170, 607–15.CrossRefGoogle ScholarPubMed
Miyazaki, S. (1991). Repetitive calcium transients in hamster oocytes. Cell Calcium 12, 205–16.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 inositol 1,4,5-triphosphate receptor in fertilized hamster eggs. Science 257, 251–5.CrossRefGoogle ScholarPubMed
Murnane, J.M. & DeFelici, L.J. (1993). Electrical maturation of the murine oocyte: an increase in calcium current coincides with acquisition of meiotic competence. Zygote 1, 49–60.CrossRefGoogle ScholarPubMed
Naito, K.Dean, F.P. & Toyoda, Y. (1992). Comparison of histone H1 kinase activity during meiotic maturation between two types of porcine oocytes matured in different media in vitro. Biol. Reprod. 47, 43–7.CrossRefGoogle ScholarPubMed
Niwa, K., Park, C.K. & Okuda, K. (1991). Penetration in vitro of bovine oocytes during maturation by frozen-thawed spermatozoa. J. Reprod. Fertil. 91, 329–36.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Nurse, P. (1990). Universal control mechanism regulating onset of M-phase. Nature 344, 503–7.CrossRefGoogle ScholarPubMed
Paleos, G.A. & Powers, R.D. (1981). The effect of calcium on the first meiotic division of the mammalian oocyte. J. Exp. Biol. 217, 409–16.Google 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 379, 364–8.CrossRefGoogle ScholarPubMed
Parrish, J.J., Kim, C.I. & Bae, I.H. (1992). Current concepts of cell-cycle regulation to oocyte maturation, fertilization and embryo development. Theriogenology 38, 277–96.CrossRefGoogle ScholarPubMed
Pasyk, E., Inazu, M. & Daniel, E.E. (1995). CPA enhances Ca2+ entry in cultured bovine pulmonary arterial endothelial cells in an IP3-independent manner. Am. J. Physiol. 268, H138–46.Google Scholar
Powers, R.D. & Paleos, G.A. (1982). Combined effect of calcium and dibutyryl cyclic AMP on germinal vesicle breakdown in the mouse oocyte. J. Reprod. Fertil. 66, 1–8.CrossRefGoogle ScholarPubMed
Racowsky, C. (1986). The releasing action of calcium upon cyclic AMP-dependent meiotic arrest in hamster oocytes. J. Exp. Zool. 239, 263–75.CrossRefGoogle ScholarPubMed
Randriamampita, C. & Tsien, R.Y. (1993). Emptying of intracellular Ca2+ stores releases a novel small messenger that stimulates Ca2+ influx. Nature. 364 809–14CrossRefGoogle ScholarPubMed
Ravindranath, N., Papadopoulos, V., Vornberger, W., Zitzmann, D. & Dym, M. (1994). Ultrastructural distribution of calcium in the rat testis. Biol. Reprod. 51, 50–62.CrossRefGoogle ScholarPubMed
Seidler, N.W., Jona, I., Vegh, K. & Martonosi, A. (1989). Cyclopiazonic acid is a specific inhibitor of Ca2+-ATPase of sarcoplasmic reticulum. J. Biol. Chem. 264, 17816–23.CrossRefGoogle ScholarPubMed
Shiraishi, K., Okada, A., Shirakawa, H., Nakanishi, S., Mikoshiba, K. & Miyazaki, S. (1995). Developmental changes in the distribution of the endoplasmic reticulum and inositol 1,4,5-trisphosphate receptors and the spatial pattern of Ca2+ release during maturation of hamster oocytes. Dev. Biol. 170, 594–606.CrossRefGoogle ScholarPubMed
Snedecor, G.W. & Cochran, W.G. (1980). Statistical Methods. Ames, Iowa: Iowa State University Press.Google Scholar
Suprynowicz, F.A., Prusmack, C. & Whalley, T. (1994). Ca2+ triggers premature inactivation of the cdc2 protein kinase in permeabilized sea urchin embryos. Proc. Natl. Acad. Sci. USA 91, 6176–80.CrossRefGoogle ScholarPubMed
Swann, K. (1992). Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem. J. 287, 79–74.CrossRefGoogle ScholarPubMed
Tombes, R.M., Simerly, C., Borisy, G. & Schatten, G. (1992). Meiosis, egg activation, and nuclear envelope breakdown are differentially reliant on Ca2+ whereas germinal vesicle breakdown is Ca2+ independent in the mouse oocyte. J. Cell Biol. 117 799–811.CrossRefGoogle ScholarPubMed
Wassarman, P. M. (1988). The mammalian ovum. In The Physiology of Reproduction, ed. Knobil, E. & Neill, J., pp.69–102. New York: Raven Press.Google Scholar
Wayman, C.P., McFadzean, I., Gibson, A. & Tucker, J.F. (1996). Two distinct membrane currents activated by cyclopiazonic acid-induced calcium store depletion in single smooth muscle cells of the mouse anococcygeus. Br. J. Pharmacol. 117, 566–72.CrossRefGoogle ScholarPubMed
Wilding, M. (1996). Calcium and cell cycle control in early embryos Zygote 4, 1–6.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1988). Mammalian fertilization. In The Physiology of Reproduction, ed. Knobil, E. & Neill, J., pp. 135–85. New York: Raven Press.Google Scholar
Yue, C.P.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.CrossRefGoogle ScholarPubMed
Zernicka-Goetz, M., Ciemerych, M.A., Kubiak, J.Z., Tarkowski, A.K. & Maro, B. (1995). Cytostatic factor inactivation is induced by a calcium-dependent mechanism present until the second cell cycle in fertilized but not in parthenogenetically activated mouse eggs. J. Cell Sci. 108, 469–74.CrossRefGoogle ScholarPubMed