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Activation of mitogen-activated protein kinase during meiotic maturation in porcine oocytes

Published online by Cambridge University Press:  26 September 2008

Maki Inoue*
Affiliation:
Institute of Medical Science and Faculty of Agriculture, University of Tokyo, Tokyo, Tokyo, Japan.
Kunihiko Naito
Affiliation:
Institute of Medical Science and Faculty of Agriculture, University of Tokyo, Tokyo, Tokyo, Japan.
Fugaku Aoki
Affiliation:
Institute of Medical Science and Faculty of Agriculture, University of Tokyo, Tokyo, Tokyo, Japan.
Yutaka Toyoda
Affiliation:
Institute of Medical Science and Faculty of Agriculture, University of Tokyo, Tokyo, Tokyo, Japan.
Eimei Sato
Affiliation:
Institute of Medical Science and Faculty of Agriculture, University of Tokyo, Tokyo, Tokyo, Japan.
*
Maki Inoue, Department of Reproductive and Developmental Biology, Institute of Medical Science, University of Tokyo, 4-6-1, Shirokanedai, Minato-ku Tokyo, Japan, 108. Telephone: + 81-3-5449-5332. Fax: + 81-3-5449-5451.
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To investigate the involvement of mitogen-activated protein kinase(MAP kinase) in meiotic maturation of porcine oocytes, we assayed MAP kinase activity using basic protein(MBP) as a substrate. MAP kinase activity was low during the germinal vesicle stage, 0–20 h of culture. An abrupt increase was observed at metaphase I(30 h of culture), and activity remained significantly higher than that at 0 h until 50 h of culture, with a transient slight decrease at the time of first polar body extrusion (40 h). Detection of the kinase activity by an in-gel phosphorylation assay confirmed that the 42 and 44 kDa MAP kinases were significantly activated in 45 h cultured oocytes but not in 0 h oocytes, and just slightly in 20 h oocytes. In immunoblotting, however, the 42 and 44 kDa bands were detected in 0, 20 and 45 h cultured oocytes. Furthermore, the signal strength of the two bands did not change during the period of culture, but shifted up to 45 h, indicating that the activation of MAP kinase depended not on the synthesis but on the phosphorylation of this enzyme. These results suggest that the activation of MAP kinase is involved in the regulation of meiotic maturation of porcine oocytes, and especially in the regulation after germinal vesicle breakdown.

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Article
Copyright
Copyright © Cambridge University Press 1995

References

references

Albertini, D. (1992). Regulation of meiotic maturation in the mammalian oocyte: interplay between exogenous cues and the microtubule cytoskeleton. BioEssays 14, 97103.CrossRefGoogle ScholarPubMed
Davis, R. (1993). The mitogen-activated protein kinase signal transduction pathway. J. Biol Chem. 268, 14553–6.CrossRefGoogle ScholarPubMed
Erickson, A., Payne, D., Martino, P., Rossomando, A., Shabanowitz, J., Weber, M., Hunt, D. & Sturgill, T.(1990). Identification by mass spectrometry of threonine 97 in bovine myelin basic protein as a specific phosphorylation site for mitogen-activated protein kinase.J. Biol. Chem. 265, 19728–35.CrossRefGoogle ScholarPubMed
Gotoh, Y., Nishida, E., Yamashita, T., Hoshi, M., Kawakami, M. & Sakai, H. (1990). Microtubule-associated protein(MAP) kinase activated by nerve growth factor and epidermal growth factor in PC12 cells.Eur.J.Biochem. 193, 661–9.CrossRefGoogle ScholarPubMed
Gotoh, Y., Nishida, E., Matsuda, S., Shiina, N., Kosako, H., Shiokawa, K., Akiyama, T., Ohta, K. & Sakai, H. (1991a). in vitro effect on microtubule dynamics of purified xenopus M phase-activated MAP kinase. Nature 349, 251–4.CrossRefGoogle ScholarPubMed
Gotoh, Y., Moriyama, K., Matsuda, S., Okumura, E., Kishimoto, T., Kawasaki, H., Suzuki, K., Yahara, I., Sakai, H. & Nishida, E. (1991b). Xenopus M phase MAP kinase:isolation of its cDNA and activation by MPF. EMBO J. 10, 2661–8.CrossRefGoogle ScholarPubMed
Haccard, O., Sarcevic, B., Lewellyn, A., Haetly, R., Roy, L., Izumi, T., Erikson, E. & Maller, J.L. (1993). Induction of metaphase arrest in cleaving xenopus embryos by MAP kinase. Science 262, 1262–4.CrossRefGoogle ScholarPubMed
Hattori, S., Fukuda, S., Yamashita, T., Nakamura, S., Gotoh, Y. & Nishida, E. (1992). Activation of mitogen-activated protein kinases and its activator by ras in intact cells and in a cell-free system. J. Biol. Chem. 267, 20346–51.CrossRefGoogle Scholar
Jung, T., Fulka, J. Jr, Lee, C. & Moor, M. (1993). Effect of the protein phosphorylation inhibitor genistein on maturation of pig oocytes in vitro. J. Reprod. Fertil, 98, 529–35.CrossRefGoogle ScholarPubMed
Kosako, H., Gotoh, Y., Matsuda, S., Ishikawa, M. & Nishida, E. (1992). Xenopus MAP kinase activator is a serne/threonine/tyrosine kinase activated by threonine phosphorylation. EMBO J. 11, 2903–8.CrossRefGoogle Scholar
Kosako, H., Gotoh, Y. &Nishida, E. (1994a).Requirement for the MAP kinase kinase/MAP kinase cascade in xenopus oocyte maturation. EMBO J. 13, 2131–8.CrossRefGoogle ScholarPubMed
Kosako, H., Gotoh, Y. & Nishida, E. (1994b). Mitogen-activated protein kinase is required for the Mos-induced metaphase arrest. J. Biol. Chem. 269, 28354–8.CrossRefGoogle ScholarPubMed
Kubiak, J., Weber, M., Geraud, G. & Maro, B. (1992). Cell cycle modification during the transition between meiotic M-phases in mouse oocytes. J. Cell Sci. 102, 457–67.CrossRefGoogle ScholarPubMed
Laemmli, U. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.CrossRefGoogle ScholarPubMed
Matsuda, S., Kosako, H., Takenaka, K., Moriyama, K., Sakai, H., Akiyama, T., Gotoh, Y. & Nishida, E. (1992). Xenopus MAP kinase activator:identification and function as a key intermediate in the phosphorylation casade. EMBO J. 11, 973–82.CrossRefGoogle Scholar
Mastuda, S., Gotoh, Y. & Nishida, E. (1993). Phosphorylation of xenopus mitogen-activated protein (MAP)kinase kinase by MAP kinase kinase kinase and MAP kinase. J. Biol. Chem. 268, 3277–81.Google Scholar
Naito, K., Fukuda, Y. & Toyoda, Y. (1988). Effect of porcine follicular fluid on male pronucleus formation in porcine oocytes matured in vitro. Gamete Res. 21, 289–95.CrossRefGoogle ScholarPubMed
Naito, K. & Toyoda, Y. (1991). Fluctuation of histine H1 kinase activity during meiotic maturation in porcine oocytes. J. Reprod. Fertil. 93, 467–73.CrossRefGoogle Scholar
Naito, K., Fukuda, Y. & Toyoda, Y. (1989). Developmental ability of porcine ova matured in porcine follicular fluid in vitro and fertilized in vitro. Theriogenology 31, 1049–57.CrossRefGoogle ScholarPubMed
Naito, K., Daen, F.P. & Toyoda, Y. (1992). Comparison of histone H1 kinase activity during meiotic maturation in different media in vitro. Biol. Reprod. 47, 43–7.CrossRefGoogle ScholarPubMed
Nebreda, A. & Hunt, T. (1993). The c-mos proto-oncogene protein kinase turns on and maintains the activity of MAP kinase, but not MPF, in cell-free extracts of xenopus occytes and eggs. EMBO J. 12, 1979–86.CrossRefGoogle ScholarPubMed
Nishida, E. & Gotoh, Y. (1993). The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci. 4, 128–31.CrossRefGoogle Scholar
Pearson, R. & Kemp, B. (1991). Protein phosphorylation siti sequences and consensus specificity motif: tabulations. Methods Enzymol. 200, 6281.CrossRefGoogle Scholar
Posada, J., Sanghera, J., Pelech, S., Aebersold, R. & Cooper, J. (1991). Tyrosine phosphorylation and activation of homologous protein kinases during oocyte maturation and mitogenic activation of fibroblasts. Mol. Cell Biol. 11, 2517–28.Google ScholarPubMed
Posada, J., Yew, N., Ahn, N., Woude, G.V. & Cooper, J. (1993). Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol. Cell Biol. 13, 2546–53.Google ScholarPubMed
Ray, L. & Sturgill, T. (1988). Characterization of insulinstimulated microtubule-associted protein kinase. J. Biol. Chem. 263, 12721–7.CrossRefGoogle ScholarPubMed
Sanghera, J., McNabb, C., Tonks, N. & Pelech, S. (1991). Tyrosyl phosphorylation and activation of the myelin basic protein kinase p44mpk during sea star oocyte maturation. Biochim.Biophys. Acta 1095, 153–60.CrossRefGoogle ScholarPubMed
Shibuya, E. & Ruderman, J. (1993). Mos induces the in vitro activation of mitogen-activated protein kinases in lysate of frog oocytes and mammalian somatic cells. Mol. Biol. Cell 4, 781–90.CrossRefGoogle ScholarPubMed
Shibuya, E., Boulton, T., Cobb, M. & Ruderman, J. (1992a). Activation of p42 MAP kinase and the release of oocytes from cell cycle arrest. EMBO J. 11, 3963–75.CrossRefGoogle ScholarPubMed
Shibuya, E., Polverino, A., Chang, E., Wigler, M. & Ruderman, J. (1992b). Oncogenic Ras triggers the activation of 42-kDa mitogen-activated protein kinase in extracts of quiescent xenopus oocytes. Proc. Natl. Acad. Sci. USA 89, 9831–5.CrossRefGoogle ScholarPubMed
Sobajima, T., Aoki, F. & kohmoto, K.(1993). Activation of mitogen-activated protein kinase during meiotic maturation in mouse oocytes. J. Reprod. Fertil. 97, 389–94.CrossRefGoogle ScholarPubMed
Toyoda, Y., Yokoyama, M. & Hoshi, T.(1971). Studies on the fertilization of mouse eggs in vitro I.In vitro fertilization of eggs by fresh epididymal sperm. J. Anim. Reprod. 16 147–51.Google Scholar
Verlhac, M., pennart, H., Maro, B., Cobb, M. & Clarke, H.(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
Verlhac, M., Kubiak, J., Clarke, H. & Maro, B.(1994).Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes.Development. 120, 1017–25.CrossRefGoogle Scholar