Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T09:13:59.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Oocyte maturation in rabbits: effects of calmodulin inhibitors

Published online by Cambridge University Press:  26 September 2008

Michael A. Henry ,
Richard G. Rawlins ,
Ewa Radwanska  and
Mary M. Fahy
Michael A. Henry*
Affiliation:
Section of Reproductive Endocrinology, Department of OB/GYN, Rush-Presbyterian-St. Luke's Medical Center, Chicago, IL 60612, USA
Richard G. Rawlins
Affiliation:
Section of Reproductive Endocrinology, Department of OB/GYN, Rush-Presbyterian-St. Luke's Medical Center, Chicago, IL 60612, USA
Ewa Radwanska
Affiliation:
Section of Reproductive Endocrinology, Department of OB/GYN, Rush-Presbyterian-St. Luke's Medical Center, Chicago, IL 60612, USA
Mary M. Fahy
Affiliation:
Section of Reproductive Endocrinology, Department of OB/GYN, Rush-Presbyterian-St. Luke's Medical Center, Chicago, IL 60612, USA
*
Michael A. Henry, MD. Present address: Advanced Fertility Group, 201 Pennsylvania Parkway - Suite 205, Indianapolis, IN 46280, USA. Tel: +1 (317) 817-1300. Fax: +1 (317) 817-1306.
Get access Rights & Permissions [Opens in a new window]

Summary

Oocyte maturation in mammals follows a highly conserved pattern of release from arrest through to the extrusion of the first polar body and formation of the second metaphase spindle. Oscillations in cytoplasmic calcium concentration precede the events of maturation in many species. These calcium ions interact with and activate calcium-binding proteins, including calmodulin, within the cell. Thus, it was of interest to us to examine whether calcium acted through calmodulin in the initial stages of maturation in rabbit oocytes or whether calmodulin was required for continuation through metaphase I on to metaphase II. Using the calmodulin inhibitor W-7 we found a significant (p < 0.05) decrease in the percentage of oocytes that underwent germinal vesicle breakdown. Calmidazolium did not prevent germinal vesicle breakdown; however, it caused a significant (p < 0.05) decrease in the proportion of oocytes with fully elaborated spindles and taxol-induced cytoplasmic asters. Both inhibitors caused a significant (p < 0.05) reduction in the proportion of oocytes that extruded their first polar bodies. The kinase inhibitor 6-DMAP caused a significant reduction in the proportion of oocytes with spindles and condensed chromatin, indicating the necessity for phosphorylation events in the resumption of meiosis. In rabbit oocytes calmodulin may play a role in the release from prophase arrest, and it is necessary for spindle preservation and continuation through metaphase I to metaphase II. The varying effects of the two inhibitor stems from their different binding sites on the calmodulin molecule thus causing a differential effect on its downstream effectors.

Keywords

CalmodulinOocyte maturationRabbitSpindle
Type
Article
Information
Zygote , Volume 5 , Issue 3 , August 1997 , pp. 255 - 260
Copyright
Copyright © Cambridge University Press 1997

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

Abdelmajid, H., Leclerc-David, C., Moreau, M., Guerrier, P., & Ryazanov, A. (1993). Release from the metaphase I Ryazanov, block in invertebrate oocytes: possible involvement of Ca2+/calmodulin-dependent kinase III. Int. J. Dev. Biol. 37 279–90.Google 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. 33 79–87.CrossRefGoogle ScholarPubMed
Crtaud, A., Ozon, R., Walsh, M.P., Haiech, J., Demaille, J.G. (1980). Xenopus laevis oocyte calmodulin in the process of meiotic maturation. J. Biol. Chem. 255 9404–8.CrossRefGoogle Scholar
Channing, C.P., Hillensjo, T., & Schaerf, F.W. 1978 Hormonal control of oocyte meiosis, ovulation and luteinization in mammals [reivew]. Clin. Endocrinol. Metab. 7 601–24.CrossRefGoogle ScholarPubMed
Chesnel, F., & Eppig, J.J. (1995). Synthesis and accumulation of p34cdc2 and cyclin B in mouse oocytes during acquisition of competence to resume meiosis. Mol. Reprod. Dev. 40 503–8.CrossRefGoogle ScholarPubMed
Courtot, A.J., Feinberg, J.M., Schoevaert, D.A., & Rainteau, D.R. 1994 Calmodulin during human sperm incorporation into hamster oocyte: an immunogold electron microscope study. Mol. Reprod. Dev. 38 170–7.CrossRefGoogle ScholarPubMed
Davis, T.N. (1992). A temperature-sensitive calmodulinmutant loses viability during mitosis. J. Cell Biol. 118 607–17.CrossRefGoogle Scholar
De Brabander, M., Geuens, G., Nuydens, R., Willebrords, R., & De Mey, J. (1981). Taxol induces the assembly of free microtubules in living cells and blocks the organizing living capacity of the centrosomes and kinetochores. Proc Natl. Acad. Sci. USA 78, 5608–12.CrossRefGoogle ScholarPubMed
De Mey, J., Moeremans, M., Geuens, G. et al. (1980). Immunocytochemical evidence for the association of calmodulin with microtubules of the mitotic apparatus. In Microtubules and Microtubule Inhibitors, ed. De Brabander, M. & De Mey, J., pp. 227–41. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Fellous, A., Kubelka, M., Thibier, C., Taieb, F., Haccard, O., & Jessus, C. (1994). Association of p34Cacdc2+ kinase and MAP kinase with microtubules during the meiotic maturation of Xenopus oocytes. Int. J. Dev. Biol. 38, 651–9.Google ScholarPubMed
Geiser, J.R., Sundberg, H.A., Chang, B.H., Muller, E.G., & Davis, T.N. (1993). The essential mitotic target of calmodulin is the 110-kilodalton competent of the spindle pole body in Saccharomyces cerevisiae. Mol. Cell Biol. 13 7913–24.Google Scholar
Golsteyn, R.M., Schultz, S.J., Bartek, J., Zeimiecki, A., Ried, T., & Nigg, E.A. (1994). Cell cycle analysis and chromosomal localization of human Plk1, a putative homologue of the mitotic kinases Drosophila polo and Saccharomyces cerevisiae Cdc5. J. Cell Sci. 107 1509–17.CrossRefGoogle ScholarPubMed
Golsteyn, R.M., Mundt, K.E., Fry, A.M., & Nigg, E.A. (1995). Cell cycle regulation of the activity and subcellular localization of Plkl, a human protein kinase implicated in mitotic spindle function. J. Cell Biol. 129 1617–28.CrossRefGoogle Scholar
Hidaka, H., Yamaki, T., Naka, M., Tanaka, T., Hayashi, H., & Kobayashi, R. (1980). Calcium-regulated modulator protein interacting agents inhibit smooth muscle calcium-stimulated protein kinase and ATPase. Mol. Pharmacol. 17, 66–72.Google ScholarPubMed
Hidaka, H., Asano, M., & Tanaka, T. (1981). Activity-structure relationship of calmodulin antagonists, naphthalene sulfonamide derivatives. Mol. Pharmacol. 20 571–8.Google Scholar
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
Jagiello, G., 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
Jung, T., Lee, C., & Moor, R.M. (1992). Effects of protein kinase inhibitors on pig oocyte maturation in vitro. Reprod. Nutr. Dev. 32 461–73.CrossRefGoogle ScholarPubMed
Kaufman, M.L., & Homa, S.T. (1993). Defining a role for calcium in the resumption and progression of meiosis in the pig oocyte. J. Exp. Zool. 265 69–76.CrossRefGoogle ScholarPubMed
Kuang, J. & Ashorn, C.L. (1993). At least two kinases phosphorliate the MPM-2 epitope during Xenopus oocyte maturation. J. Cell Biol. 123 859–68.CrossRefGoogle ScholarPubMed
Kumagai, A., & Dunphy, W.G. (1996). Purification and molecular cloning of Plxl, a Cdc-25-regulatory kinase from Xenopus egg extracts. Science 273 1377– 80.CrossRefGoogle Scholar
Llamazares, S., Moreira, A., Tavares, A., Girdham, C., Spruce, B.A., Gonzalez, C., Karess, R.E., Glover, D.M., & Sunkel, C.E. (1991). polo encodes a protein kinase homolog required for mitosis in Drosophila. Genes Dev. 5, 2153–65.CrossRefGoogle ScholarPubMed
Lorca, T., Galas, S., Fesquet, D., Devault, A., Cavadore, J.C. & Doree, M. (1991). Degradation of the proto-oncogene produce p39mos is not necessary for cyclin proteolysis and exit from meiotic metaphase: requirement for a Ca2+ calmodulin dependent event. EMBO J. 10 2087–93.CrossRefGoogle Scholar
Mills, J.S., Bailey, B.L., & Johnson, J.D. (1985). Cooperativity among calmodulin's drug binding sites. Biochemistry 24, 4897–902.CrossRefGoogle ScholarPubMed
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 [review]. Dev. Biol. 158, 62–78.CrossRefGoogle ScholarPubMed
Ohta, H. (1990). Possible involvement of protein kinase C in early development of mouse. Mie Igaku 34 79–86.Google Scholar
Ohta, K., Shiina, N., Okumura, E., Hisanaga, S., Kishimoto, T., Endo, S., Gotoh, Y., Nishida, E., & Sakai, H. (1993). Microtubule nucleating activity of centrosomes in cell-free extracts from Xenopus eggs: involvement of phosphorylation and accumulation of pericentriolar material. J. Cell Sci., 104 125–37.CrossRefGoogle ScholarPubMed
Ohya, T., & Botstein, D. (1994). Diverse essential functions revealed by complementing yeast calmodulin mutants. Science 263 963–6.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
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
Simerly, C., & Schatten, G. (1993). Techniques for localization of specific molecules in oocytes and embryos. Methods Enzymol. 225 516–53.CrossRefGoogle ScholarPubMed
Spang, A., Grein, K. & Schiebel, E. (1996). The spacer protein Spc11p targets calmodulin to the central plaque of the yeast spindle pole body. J. Cell Sci. 109 2229–37.CrossRefGoogle Scholar
Stirling, D.A., Welch, K.A., & Stark, M.J.R. (1994). Interaction with calmodulin is required for the function of Spc110p, an essential component of the yeast spindle pole body. EMBO J. 13 4329–42.CrossRefGoogle ScholarPubMed
Sun, G., Hirata, A., Ohya, Y., & Anraku, Y. (1992). Mutations in yeast calmodulin cause defects in spindle pole body functions and nuclear integrity. J. Cell Biol. 119 1625–39.CrossRefGoogle ScholarPubMed
Sundberg, H.A., Goetsch, L., Byers, B. & Davis, T.N. (1996). Role of calmodulin and Spc110p interaction in the proper assembly of spindle pole body components. J. Cell Biol. 133 111–24.CrossRefGoogle Scholar
Takuwa, N., Zhou, W., & Takuwa, Y. (1995). Calcium, calmodulin and cell cycle progression [reivew] Cell Signal 7 93–104.CrossRefGoogle ScholarPubMed
Thayer, S.A., & Fairhurst, A.S. (1983). The interaction of dihydropyridine calcium channel blockers with calmodulin and calmodulin inhibitors. Mol. Pharmacol. 24 6–9.Google ScholarPubMed
Verde, F., Berrez, J., Antony, C., & Karsenti, E. (1991). Taxol induced microtubule asters in mitotic extracts of Xenopus eggs: requirement of phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112 1177–87.CrossRefGoogle ScholarPubMed
Verlhac, M.H., de Pennart, H., Maro, B., Cobb, M.H., & Clarke, H.J. (1993). MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev. Biol. 158 330–40.CrossRefGoogle ScholarPubMed
Vogel, H.J. (1994). The Merck Frost Award Lecture 1994. Calmodulin: a versatile calcium mediator protein [review]. Biochem. Cell Biol. 72 357–76.CrossRefGoogle Scholar
Wasserman, W.J. & Smith, L.D. (1981). Calmodulin triggers the resumption of meiosis in amphibian oocytes. J. Cell Biol. 89 389–94.CrossRefGoogle ScholarPubMed
Welsh, M.J., Dedman, J.R., Brinkley, B.R. & Means, A.R. (1996). Tubulin and calmodulin effects of microtubule and microfilament inhibitors on localization in the mitotic apparatus. J. Cell Biol. 81 624–34.CrossRefGoogle Scholar
Wickramasinghe, D., & Albertini, D.F. (1992). Centrosomephosphorylation and the developmental expression of meiotic competence in mouse oocytes. Dev. Biol. 152 62–74CrossRefGoogle ScholarPubMed
Wickramasinghe, D., & Albertini, D.F. (1993). Cell cycle control during mammalian oogenesis [review]. Curr. Top. Dev. Biol. 28, 125–53.CrossRefGoogle ScholarPubMed
Wickramasinghe, D., Ebert, K.M., & Albertini, D.F. (1991). Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes [published erratum appears in Dev. Biol. 1991; 144: 220]. Dev. Biol. 143, 162–72.CrossRefGoogle ScholarPubMed
Zavortink, M., Welsh, M.J., & McIntosh, J.R. (1983). The distribution of calmodulin in living mitotic cells. Exp. Cell Res. 149, 375–85.CrossRefGoogle ScholarPubMed