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Subcellular localization of calcium and Ca-ATPase activity during nuclear maturation in Bufo arenarum oocytes

Published online by Cambridge University Press:  01 August 2009

Inés Ramos ,
Susana B. Cisint ,
Claudia A. Crespo ,
Marcela F. Medina  and
Silvia N. Fernández
Inés Ramos
Affiliation:
Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, (4000) Tucumán, Argentina.
Susana B. Cisint
Affiliation:
Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, (4000) Tucumán, Argentina.
Claudia A. Crespo
Affiliation:
Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, (4000) Tucumán, Argentina.
Marcela F. Medina
Affiliation:
Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, (4000) Tucumán, Argentina.
Silvia N. Fernández*
Affiliation:
Department of Developmental Biology, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina. Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, (4000) Tucumán, Argentina.
*
All correspondence to: Silvia N. Fernández. Department of Developmental Biology, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina. Tel: +51 0381 4247752 (7005). Fax: +51 0381 4107214. e-mail: [email protected]
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Summary

The localization of calcium and Ca-ATPase activity in Bufo arenarum oocytes was investigated by ultracytochemical techniques during progesterone-induced nuclear maturation, under in vitro conditions. No Ca2+ deposits were detected in either control oocytes or progesterone-treated ones for 1–2 h. At the time when nuclear migration started, electron dense deposits of Ca2+ were visible in vesicles, endoplasmic reticulum cisternae and in the space between the annulate lamellae membranes. Furthermore, Ca-ATPase activity was also detected in these membrane structures. As maturation progressed, the cation deposits were observed in the cytomembrane structures, which underwent an important reorganization and redistribution. Thus, they moved from the subcortex and became located predominantly in the oocyte cortex area when nuclear maturation ended. Ca2+ stores were observed in vesicles surrounding or between the cortical granules, which are aligned close to the plasma membrane. The positive Ca-ATPase reaction in these membrane structures could indicate that the calcium deposit is an ATP-dependent process. Our results suggest that during oocyte maturation calcium would be stored in membrane structures where it remains available for release at the time of fertilization. Data obtained under our experimental conditions indicate that calcium from the extracellular medium would be important for the oocyte maturation process.

Keywords

AmphibianCalciumCa-ATPaseOocyte maturation
Type
Research Article
Information
Zygote , Volume 17 , Issue 3 , August 2009 , pp. 253 - 260
Copyright
Copyright © Cambridge University Press 2009

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References

Ando, T., Fujimoto, K., Mayahara, H., Miyajima, H. & Ogawa, K. (1981). A new one-step method for the histochemistry and cytochemistry of Ca2+-ATPase activity. Acta Histochem. Cytochem. 14, 705–26.Google Scholar
Bement, W.M. & Capco, D.G. (1990). Transformation of the amphibian oocyte into the egg: structural and biochemical events. J. Electron Microsc. Tech. 16, 202–34.Google Scholar
Bertout, M., Flament, S., Browaeys-Poly, E. & Vilain, J.P. (1997). Ultrastructural localization of intracellular calcium stores in Xenopus ovarian follicles as revealed by cytochemistry and X-ray microanalysis. Develop. Growth Differ. 39, 249–56.Google Scholar
Boni, R., Cuomo, A. & Tosti, E. (2002). Developmental potential in bovine oocytes is related to cumulus–oocyte complex grade, calcium current activity, and calcium stores. Biol. Reprod. 66, 836–42.CrossRefGoogle ScholarPubMed
Campanella, C., Andreuccetti, P., Taddei, C. & Talevi, R. (1984). The modifications of cortical endoplasmic reticulum during in vitro maturation of Xenopus laevis oocytes and its involvement in cortical granule exocytosis. J. Exp. Zool. 229, 283–93.CrossRefGoogle ScholarPubMed
Cork, R.J., Cicirelli, M.F. & Robinson, K.R. (1987). A rise in cytosolic calcium is not necessary for maturation of Xenopus laevis oocytes. Dev. Biol. 121, 41–7.CrossRefGoogle Scholar
de Romero, I.R., de Atenor, M.B. & Legname, A.H. (1998). Nuclear maturation inhibitors in Bufo arenarum oocytes. Biocell 22, 27–34.Google Scholar
Duesbery, N.S. & Masui, Y. (1996). The role of Ca2+ in progesterone-induced germinal vesicle breakdown of Xenopus laevis oocytes: the synergic effects of microtubule depolymerization and Ca2+. Dev. Genes Evol. 206, 110–24.Google Scholar
Fernández, S.N. & Ramos, I. (2003). Endocrinology of reproduction. In: Reproductive Biology and Phylogeny of Anura (ed. , B.G.M. Jamieson), pp. 73–117. Science Publishers, Inc., Enfield, New Hampshire, USA.Google Scholar
Fortune, J.E. (1983). Steroid production by Xenopus ovarian follicles at different developmental stages. Develop. Biol. 99, 502–9.CrossRefGoogle ScholarPubMed
Fujiwara, T., Nakada, K., Shirakawa, H. & Miyazaki, S. (1993). Development of inositol trisphosphate-induced calcium release mechanism, during maturation of hamster oocytes. Dev. Biol. 156, 69–79.Google Scholar
Homa, S.T. (1995). Calcium and meiotic maturation of the mammalian oocyte. Mol. Reprod. Dev. 40, 122–34.Google Scholar
Jaffe, L.A., Giusti, A.F., Carrol, D.J. & Foltz, K.R. (2001). Ca2+ signaling during fertilization of echinoderm eggs. Semin. Cell Dev. Biol. 12, 45–51.CrossRefGoogle ScholarPubMed
Jalabert, B., Fostier, A., Breton, B. & Weil, C. (1991). Oocyte maturation in vertebrates. In: Vertebrate Endocrinology: Fundamentals and Biochemical Implications (eds Pang, P.K.T. & Schreibman, M.P.), pp. 23–90. San Diego: Academic Press.Google Scholar
Klein, R.L., Yen, S. & Thureson-Klein, A. (1972). Critique on the K-pyroantimonate method for semiquantitative estimation of cations in conjunction with electron microscopy. J. Histochem. Cytochem. 20, 65–78.Google Scholar
Kobrinsky, E.M. & Kirchberger, M.A. (2001). Evidence for a role of the sarcoplasmic/endoplasmic reticulum Ca2+-ATPase in thapsigargin and Bcl-2 induced changes in Xenopus laevis oocyte maturation. Oncogene 20, 933–41.CrossRefGoogle ScholarPubMed
Kume, S., Yamamoto, A., Inoue, T., Muto, A., Okano, H. & Mikoshiba, K. (1997). Developmental expression of the inositol 1,4,5-trisphosphate receptor and structural changes in the endoplasmic reticulum during oogenesis and meiotic maturation of Xenopus laevis. Dev. Biol. 182, 228–39.Google Scholar
Liu, Z. & Patiño, R. (1993). High-affinity binding of progesterone to the plasma membrane of Xenopus oocytes: characteristics of binding and hormonal and developmental control. Biol. Reprod. 49, 980–8.Google Scholar
Maller, J.L. (1985). Regulation of amphibian oocyte maturation. Cell Differ. 16, 211–21.Google Scholar
Medina, M.F., Ramos, I., Crespo, C.A., González, S. & Fernández, S.N. (2004). Changes in serum sex steroid levels throughout the reproductive cycle of Bufo arenarum females. Gen. Comp. Endocrinol. 136, 143–51.Google Scholar
Mehlman, 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.Google Scholar
Mehlman, L.M., Mikoshiba, K. and Kline, D. (1996). Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte. Dev. Biol. 180, 489–98.Google Scholar
Morrison, T., Waggoner, L., Whitworth-Langley, L. & Stith, B.J. (2000). Nongenomic action of progesterone: activation of Xenopus oocyte phospholipase C through a plasma membrane-associated tyrosine kinase. Endocrinology 14, 2145–52.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
Polzonetti-Magni, A.M., Mosconi, G., Carnevali, O., Yamamoto, K., Hanaoka, Y. & Kikuyama, S. (1998). Gonadotropins and reproductive function in the anuran amphibian Rana esculenta. Biol. Reprod. 58, 88–93.CrossRefGoogle ScholarPubMed
Ramos, I., Cisint, S., Alcaide, M.F. & Campos Casal, F. (1998). Morphological and cytochemical changes during nuclear maturation in Bufo arenarum oocytes. Biocell 22, 167–75.Google Scholar
Ramos, I., Winik, B.C., Cisint, S.B., Crespo, C., Medina, M. & Fernández, S. (1999). Ultrastructural changes during nuclear maturation in Bufo arenarum oocytes. Zygote 7, 261–9.Google Scholar
Riabova, L.V. (1990). [The organization of the cortical layer of amphibian ova. 1. The ultrastructure of the cortex of the oocytes and ova of the clawed toad: the effect of divalent cations]. Ontogenez 21, 286–91.Google ScholarPubMed
Sadler, S.E. & Maller, J.L. (1982). Identification of a steroid receptor on the surface of Xenopus oocytes by photoaffinity labeling. J. Biol. Chem. 257, 355–61.Google Scholar
Spicer, S.S., Hardin, J.H. & Greene, W.B. (1968). Nuclear precipitates in pyroantimonate-osmium tetroxide-fixed tissues. J. Cell Biol. 39, 216.Google Scholar
Stricker, S.A. (1999). Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211, 157–76.CrossRefGoogle ScholarPubMed
Stricker, S.A. & Smythe, T.L. (2003). Endoplasmic reticulum reorganizations and Ca2+ signaling in maturing and fertilized oocytes of marine protostome worms: the roles of MAPKs and MPF. Development 130, 2867–79.CrossRefGoogle ScholarPubMed
Sun, L. & Machaca, K. (2004). Ca2+cyt negatively regulate the initiation of oocyte maturation. J. Cell Biol. 165, 63–75.CrossRefGoogle 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
Terasaki, M., Runft, L.L. & Hand, A.R. (2001). Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation. Mol. Biol. Cell 12, 1103–16.Google Scholar
Tosti, E., Boni, R. & Cuomo, A. (2000). Ca2+ current activity decreases during meiotic progression in bovine oocytes. Am. J. Physiol. Cell Physiol. 279, C1795–800.CrossRefGoogle ScholarPubMed
Wasserman, W.J., Pinto, L.H., O'Connor, C.M. & Smith, L.D. (1980). Progesterone induces a rapid increase in Ca of Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA 77, 1534–6.Google Scholar
Yamashita, M., Mita, K., Yoshida, N. & Kondo, T. (2000). Molecular mechanisms of initiation of oocyte maturation: general and species-specific aspects. Prog. Cell Cycle Res. 4, 115–29.CrossRefGoogle ScholarPubMed