Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-23T02:27:13.422Z Has data issue: false hasContentIssue false
  • English
  • Français

Mitogen-activated protein kinase activity and microtuble organisation are altered by protein synthesis inhibition in maturing porcine oocytes

Published online by Cambridge University Press:  26 September 2008

Maki Inoue ,
Kunihiko Naito ,
Taisuke Nakayama  and
Eimei Sato
Maki Inoue*
Affiliation:
Department of Reproductive and Developmental Biology, The University of Tokyo, Tokoyo, Japan.
Kunihiko Naito
Affiliation:
Department of Reproductive and Developmental Biology, The University of Tokyo, Tokoyo, Japan.
Taisuke Nakayama
Affiliation:
Department of Reproductive and Developmental Biology, The University of Tokyo, Tokoyo, Japan.
Eimei Sato
Affiliation:
Department of Reproductive and Developmental Biology, The University of Tokyo, Tokoyo, Japan.
*
M.Inoue, Department of Reproductive and Developmental Biology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, 108Japan. Telephone: +81-3-5449-5753. Fax: +81-3-5449-5455. e-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

Previously we have shown that mitogen-activated protein (MAP) kinase activity abruptly increases at the first metaphase (M1) and remains significantly higher than that at the germinal vesicle (GV) stage until the second metaphase (M2) in porcine oocytes cultured in vitro. The present paper describes how the mechanism of the blockage of meiotic maturation by protein sythesis inhibition involves MAP kinase regulation. Cycloheximide arrested both germinal vesicle breakdown (GVBD) and the normal transition from M1 to M2. MAP kinase activation was also reduced in these maturation-inhibited oocytes. By using immunofluorescence microscopy with the monoclonal antibody raised against rat α-tubulin, we showed that cycloheximide caused morphological abnormality in a spindle at M1, but not at M2. All these results indicate that in porcine oocytes: (1) GV blockage by protein synthesis inhibition involves the suppression of both histone H1 kinase and MAP kinase activation, (2) during the transition from M1 to M2, maintenance of a normal metaphasic spindle and high MAP kinase activity require protein synthesis, and (3) once the M2 cytoskeletal structures have been completed, and/or after the ‘critical period’, cytostatic factor activity is independent of protein synthesis.

Keywords

ChromosomesMAP kinaseMicrotubulesOocyte maturationProtein sythesis
Type
Article
Information
Zygote , Volume 4 , Issue 3 , August 1996 , pp. 191 - 198
Copyright
Copyright © Cambridge University Press 1996

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

Davis, R.J. (1993). The mitogen-activated protein kinase signal transduction pathway. Biol. Chem. 268, 14553–6.CrossRefGoogle ScholarPubMed
Downs, S.M. (1989). Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol. Reprod. 41, 371–9.CrossRefGoogle ScholarPubMed
Gille, H., Sharrocks, A.D. & Shaw, P.E. (1992). Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature. 358, 414–17.CrossRefGoogle ScholarPubMed
Gotoh, Y., Nishida, E., Matsuda, S., Shiina, N., Kosako, H., Shiokawa, K., Akiyama, T., Ohta, K. & Sakai, H. (1991). in vitro effect on microtubule dynamics of purified Xenopus M phase-activated MAP kinase. Nature. 349, 251–4.Google Scholar
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
Inoue, M., Naito, K., Aoki, F.Toyoda, Y. & Sato, E. (1995). Activation of mitogen-activated protein kinase during meioteic maturation in porcine oocytes Zygote. 3 265–71.Google Scholar
Jung, Y., Fulka, J. Jr, Lee, C. & Moor, R.M. (1993). Effects of the protein phoshorylation inhibitor genistein on maturation of pig oocytes in vitro. J. Reprod. Fertil. 98, 529–35.CrossRefGoogle Scholar
Kosako, H., Gotoh, Y., Matsuda, S., Ishikawa, M. & Nishida, E. (1992). Xenopus MAP Kinase activator is a serine/tyrosine kinase activated by threonine phosphorylation. EMBo J. 11, 2903–8.CrossRefGoogle Scholar
Kosako, H., Gotoh, Y. & Nishida, E. (1994 a). Requirement for the MAP kinase kinase/map kinase cascade in Xenopus oocyte maturation. EMBO J. 13, 2131–8.CrossRefGoogle ScholarPubMed
Kosaka, H., Gotoh, Y. & Nishida, E. (1994b). Mitogenactivated protein kinase kinase is required for the Mosinduced metaphase atttest. J. Biol. Chem. 269, 28354–8.Google Scholar
Kubelka, M., Motlik, J. Jr, Prochazka, R., Rimkevicova, Z. & Fulka, J. (1988). Time sequence of germinal vesicle breakdown in pig oocytes after cycloheximide and p-aminobenzamidine block. Gamete Res. 19, 423–31.CrossRefGoogle ScholarPubMed
Kubelka, M., Rimkevicova, Z., Guerrier, P. & Motlik, J. (1995). Inhibition of protein synthesis affects histone H1 kinase, but not chromosome condensation activity, during the first meiotic division of pig oocytes. Mol. Reprod. Dev. 41, 63–9.CrossRefGoogle Scholar
Laemmli, U. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227, 680–5.CrossRefGoogle ScholarPubMed
Le Gal, F., Gall, L. & DeSmedt, V. (1992). Changes in protein synthesis pattern during in vitro maturation of goat oocytes. Mol. Reprod. Dev. 32, 1–8.Google Scholar
Matsuda, S., Kosako, H., Takenaka, K., Moriyama, K., Sekai, H., Akiyama, T., Gotoh, Y. & Nishida, E. (1992). Xenopus MAP kinase activator: identification and function as a key intermediate in the phosphorylation cascade. EMDO J. 11, 973–82.Google Scholar
Matsuda, 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
Moor, R.M. & Crosby, I.M. (1986). Protein requirements for germinal vesicle breakdown in ovine oocytes. J. Embryol. Exp. Morphol. 94, 207–20.Google ScholarPubMed
Motlik, J. & Rimekevicova, Z. (1990). Combined effects of protein synthesis and phosphorylation inhibitors on maturation of mouse oocytes in vitro. Mol. Reprod. Dev. 27, 230–4.Google Scholar
Naito, K. & Toyoda, Y. (1991). Fluctuation of histone H1 kinase activity during meiotic maturation in porcine oocytes. J. Reprod. Fertil. 93. 467–73.CrossRefGoogle ScholarPubMed
Naito, K., Fukuda, Y. & Toyoda, Y. (1988). Effects of porcine follicular fluid on male pronucleus formation in porcine oocytes matured in vitro. Gamete Res. 21, 289–95.CrossRefGoogle ScholarPubMed
Naito, E., Hawkins, C., Yamashita, R.M. (1995). Assocition of p34cdc2 and cyclin B1 during meiotic maturation in pig oocytes. Dev. Biol. 168, 627–34.CrossRefGoogle Scholar
Nishida, E. & Gotoh, Y. (1993). The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci. 18, 128–31.CrossRefGoogle ScholarPubMed
Nurse, P. (1990). Universal control mechanism regulating onset of M-phase. Nature. 344, 503–8.CrossRefGoogle ScholarPubMed
Posada, J. & Cooper, J.A. (1992). Requirements for phosphorylation of MAP kinase during meiosis in Xenopus oocytes. Science. 255, 212–15.Google Scholar
Posada, J.Sanghera, J., Pelech, S., Aebersold, R. & Cooper, J.A. (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
Sagata, N., Daar, I., Oskarsson, M., Showalter, S.D.Vande Woude, G.F. (1989). The product of the mos proto-oncogene as a candidate ‘initiator’ for oocyte maturation. Science. 245, 643–6.CrossRefGoogle ScholarPubMed
Sanghera, J.S., McNabb, C.K., Tonks, N. & Pelech, S.L. (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.K., Boulton, T.G., Cobb, M.H. & Ruderman, J.V. (1992). Activation of p42 map kinase and the release of oocytes from cell cycle arrest. EMBO J. 11, 3963–75.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
Sturgill, T.W., Ray, L.B., Erikson, E. & Maller, J.L. (1988). Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature. 334, 715–18.Google Scholar
Szollosi, M.S., Kubiak, J., Debey, P., De, Pennart H & Szollosi, D. (1993). Inhibiton of kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J.Cell Sci. 104, 861–72.CrossRefGoogle Scholar
Tatemoto, H. & Horiuchi, T. (1995). Requirements for protein synthesis during the onset of meiosis in bovine oocytes and its involvement in the autocatalytic amplification of maturation-promoting factor. Mol. Reprod. Dev. 41, 47–53.Google Scholar
Toyoda, Y., Yokoyama, M. & Hosi, T. (1971). Studies on the fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn. Anim. Reprod. 16, 147–51.Google Scholar
Verlhac, M.H., 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
Verlhac, M.H., kubiak, J.Z., Clarke, H.J. & 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
Verlhac, M.H., kubiak, J.Z., Weber, M., Geraud, G., Colledge, W.H., Evans, M.J. & Maro, B. (1996). Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development. 122, 815–22.CrossRefGoogle ScholarPubMed
Yamauchi, N., Sasada, H. & Sugawara, S. (1995). Protein synthesis in porcine follicular oocytes during in vitro meiotic maturation. J. Mamm. Ova Res. 12, 59–63.Google Scholar