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Participation of MAPK, PKA and PP2A in the regulation of MPF activity in Bufo arenarum oocytes

Published online by Cambridge University Press:  30 September 2010

G. Sánchez Toranzo ,
F. Bonilla ,
M.C. Gramajo Bühler  and
M.I. Bühler
G. Sánchez Toranzo
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
F. Bonilla
Affiliation:
Instituto de Biología, Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
M.C. Gramajo Bühler
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
M.I. Bühler*
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina.
*
All correspondence to: Marta I. Bühler. Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina. Fax: +54 381 4247752 intern 7004. e-mail: [email protected]
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Summary

The objectives of the present paper were to study the involvement and possible interactions of both cAMP-PKA and protein phosphatases in Bufo arenarum oocyte maturation and to determine if these pathways are independent or not of the MAP kinase (MAPK) cascade. Our results indicated that the inhibition of PKA by treatment with H-89, an inhibitor of the catalytic subunit of PKA, was capable of inducing GVBD in a dose-dependent manner by a pathway in which Cdc25 phosphatase but not the MAPK cascade is involved. The injection of 50 nl of H-89 10 μM produced GVBD percentages similar to those obtained with treatment with progesterone. In addition, the assays with okadaic acid (OA), a PP2A inhibitor, significantly enhanced the percentage of oocytes that resumed meiosis by a signal transducing pathway in which the activation of the MEK–MAPK pathway is necessary, but in which Cdc25 phosphatase was not involved. Treatment with H-89, was able to overcome the inhibitory effect of PKA on GVBD; however, the inhibition of Cdc25 activity with NaVO3 was able to overcome the induction of GVBD by H-89. Although the connections between PKA and other signalling molecules that regulate oocytes maturation are still unclear, our results suggest that phosphatase Cdc25 may be the direct substrate of PKA. In Xenopus oocytes it was proposed that PP2A, a major Ser/Thr phosphatase present, is a negative regulator of Cdc2 activation. However, in Bufo arenarum oocytes, inhibition of Cdc25 with NaVO3 did not inhibit OA-induced maturation, suggesting that the target of PP2A was not the Cdc25 phosphatase. MAPK activation has been reported to be essential in Xenopus oocytes GVBD. In B. arenarum oocytes we demonstrated that the inhibition of MAPK by PD 98059 prevented the activation of MPF induced by OA, suggesting that the activation of the MAPK cascade produced an inhibition of Myt1 and, in consequence, the activation of MPF without participation of the Cdc25 phosphatase. Our results suggest that in incompetent oocytes of B. arenarum two signal transduction pathways may be involved in the control of MPF activation: (1) the inhibition of phosphatase 2A that through the MEK–MAPK pathway regulates the activity of the Myt1; and (2) the inhibition of AMPc–PKA, which affects the activity of the Cdc25 phosphatase.

Keywords

AmphibianOocyte maturationSignalling pathway
Type
Research Article
Information
Zygote , Volume 19 , Issue 2 , May 2011 , pp. 181 - 189
Copyright
Copyright © Cambridge University Press 2010

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References

Bodart, J.F., Gutierrez, D.V., Nebreda, A.R., Buckner, B.D., Resau, J.R. & Duesbery, N.S. (2002). Characterization of MPF and MAPK activities during meiotic maturation of Xenopus tropicalis oocytes. Dev. Biol. 245, 348–61.CrossRefGoogle ScholarPubMed
Cerdà, J., Petrino, T.R., Landin, A.M. & Lin, W.P. (1997). Effects of isoquinolinesulfonamide H-8 on Fundulus heteroclitus ovarian follicles: role of cyclic nucleotide-dependent protein kinases on steroidogenesis and oocyte maturation in vitro. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 117, 75–81.CrossRefGoogle ScholarPubMed
Clarke, P.R., Hoffmann, I., Draetta, G. & Karsenti, E. (1993). Dephosphorylation of Cdc25-C by a type-2A protein phosphatase: specific regulation during the cell cycle in Xenopus eggs extracts. Mol. Biol. Cell 4, 397–411.CrossRefGoogle Scholar
Dekel, N. (2005). Cellular biochemical and molecular mechanisms regulating oocytes maturation. Mol. Cell. Endocrinol. 29, 19–25.CrossRefGoogle Scholar
Duckworth, B.C., Weaver, J.S. & Rudeman, J.V. (2002). G2 arrest in Xenopus oocytes depends on phosphorylation of Cdc25 by protein kinase A. Proc. Natl. Acad. Sci. USA 99, 16794–9.CrossRefGoogle ScholarPubMed
Ferrell, J.E. (1999). Xenopus oocytes maturation: new lessons from a good egg. Bioessays 21, 833–842, 866–870.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Ferrell, J.E. Jr, Wu, M., Gerhart, J.C. & Martin, G.S. (1991). Cell cycle tyrosine phosphorylation of p34Cdc2 and a microtubule-associated protein kinase homolog in Xenopus oocytes and eggs. Mol. Cell. Biol. 11, 1965–71.Google Scholar
Ferrell, J.E. Jr & Machleder, E.M. (1998). The biochemical basis of an all-or-none cell fate switch in Xenopus oocytes. Science 280, 895–8.CrossRefGoogle ScholarPubMed
Fisher, M., Stirling Meyer, J., Malik, G.M. & Helgason, C.M. (1999). Editorial commentary. J. Stroke Cerebrovasc. Dis. 8, i–ii.CrossRefGoogle ScholarPubMed
Forester, C.M., Maddox, J., Louis, J.V., Goris, J. & Virshup, D.M. (2007). Control of mitotic exit by PP2A regulation of Cdc25C and Cdk1 Proc. Natl. Acad. Sci. USA 104, 19867–72.CrossRefGoogle ScholarPubMed
Gautier, J. & Maller, J.L. (1991). Cyclin B in Xenopus oocytes, implications for the mechanism of pre-MPF activation. EMBO J. 10, 177–82.CrossRefGoogle ScholarPubMed
Goris, J., Hermann, J., Hendrix, P., Ozon, R. & Merlevede, W. (1986). Okadaic acid, a specific protein phosphatase inhibitor, induces maturation and MPF formation in Xenopus laevis oocytes. FEBS Lett. 245, 91–4.CrossRefGoogle Scholar
Haccard, O., Jessus, C., Cayla, X., Goris, J., Merlevede, W. & Ozon, R. (1990). In vivo activation of a microtubule-associated protein kinase during meiotic maturation of the Xenopus oocyte. Eur. J. Biochem. 192, 633–42.CrossRefGoogle ScholarPubMed
Haccard, O., Lewellyn, A., Hartley, R.S., Erikson, E. & Maller, J.L. (1995). Induction of Xenopus oocytes meiotic maturation by MAP kinase. Dev. Biol. 168, 677–82.CrossRefGoogle ScholarPubMed
Haider, S. & Baqri, S.S. (2002). Role of cyclic AMP-dependent protein kinase in oocyte maturation of the catfish, Clarias batrachus. J. Exp. Zool. 292, 587–93.CrossRefGoogle ScholarPubMed
Han, S.J. & Conti, M. (2006). New pathways from PKA to the Cdc2/cyclin B complex in oocytes: Wee1B as a potential PKA substrate. Cell Cycle 5, 227–31.CrossRefGoogle Scholar
Han, S.J., Chen, R., Paronetto, M.P. & Conti, M. (2005). Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr. Biol. 5, 1670–6.CrossRefGoogle Scholar
Hermann, J., Cayla, X., Dumortier, K., Goris, J., Ozon, R. & Merlevede, W. (1988). Modulation of the substrate specificity of the polycation-stimulated protein phosphatase from Xenopus laevis oocytes. Eur. J. Biochem. 173, 17–25.CrossRefGoogle ScholarPubMed
Huchon, D., Ozon, R. & Demaille, J.G. (1981). Protein phosphatase-1 is involved in Xenopus oocyte maturation. Nature 294, 358–9.CrossRefGoogle ScholarPubMed
Izumi, T. & Maller, J.L. (1993). Elimination of Cdc2 phosphorylation sites in the Cdc25 phosphatase blocks initiation of M-phase. Mol. Biol. Cell. 4, 1337–50.CrossRefGoogle ScholarPubMed
Izumi, T., Walker, D.H. & Maller, J.L. (1992). Periodic changes in phosphorylation of the Xenopus Cdc25 phosphatase regulate its activity. Mol. Biol. Cell. 3, 927–39.CrossRefGoogle ScholarPubMed
Karaïskou, A., Jessus, C., Brassac, T. & Ozon, R. (1999). Phosphatase 2A and polo kinase, two antagonistic regulators of Cdc25 activation and MPF auto-amplification. J. Cell Sci. 112, 3747–56.CrossRefGoogle ScholarPubMed
Kishimoto, T. (1998). Cell cycle arrest and release in starfish oocytes and eggs. Semin. Cell Dev. Biol. 9, 549–57.CrossRefGoogle ScholarPubMed
Kwon, H.B. & Lee, W.K. (1991). Involvement of protein kinase C in the regulation of oocyte maturation in amphibians (Rana dybowskii). J. Exp. Zool. 257, 115–23.CrossRefGoogle ScholarPubMed
Lee, T.H., Turk, C. & Kirschner, M.W. (1994). Inhibition of Cdc2 activation by INH/PP2A. Mol. Biol. Cell 5, 323–38.CrossRefGoogle ScholarPubMed
Lin, Y.P. & Schuetz, A.W. (1985). Spontaneous oocyte maturation in Rana pipiens: estrogen and follicle wall involvement. Gamete Res. 12, 11–28.CrossRefGoogle Scholar
Lu, Q., Smith, G.D., Chen, D.Y., Yang, Z., Han, Z., Schatten, H. & Sun, Q. (2001). Phosphorilation of mitogen-activated protein kinase is regulated by protein kinase C, cyclic 3´,5´, adenosine monophosphate, and protein phosphatase modulators during meiosis resumptions in rat oocytes. Biol. Reprod. 64, 1444–50.CrossRefGoogle Scholar
Maller, J.L. & Krebs, E.G. (1977). Progesterone-stimulated meiotic cell division in Xenopus oocytes: induction by regulatory subunit of adenosine 3´5´-monophosphate-dependent protein kinase. J. Biol. Chem. 252, 1712–8.CrossRefGoogle ScholarPubMed
Minshull, J., Murray, A., Colman, A. & Hunt, T. (1991). Xenopus oocytes maturation does not require new cyclin synthesis. J. Cell Biol. 114, 767–72.CrossRefGoogle Scholar
Mishra, A. & Joy, K.P. (2006). Involvement of mitogen-activated protein kinase in 2-hydroxyestradiol-17beta-induced oocyte maturation in the catfish Heteropneustes fossilis and a note on possible interaction with protein phosphatases. Gen. Comp. Endocrinol. 147, 329–35.CrossRefGoogle Scholar
Nebreda, A. & Hunt, T. (1993). The c-mos proto-oncogen protein kinase turns on and maintains the activity of MAP kinase, but not MPF in cell-free extracts of Xenopus oocytes and eggs. EMBO J. 12, 1979–86.CrossRefGoogle Scholar
Pace, M.C. & Thomas, P. (2005). Steroid-induced oocyte maturation in Atlantic croaker (Micropogonias undulatus) is dependent on activation of the phosphatidylinositol 3-kinase/Akt signal transduction pathway. Biol. Reprod. 73, 988–96.CrossRefGoogle ScholarPubMed
Palmer, A., Gavin, A.C. & Nebreda, A.R. (1998). A link between MAP kinase and p34(Cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(Cdc2) inhibitory kinase Myt1. EMBO J. 17, 5037–47.CrossRefGoogle ScholarPubMed
Picard, A., Labbe, J.C., Barakat, H., Cavadore, J.C. & Doree, M. (1991). Okadaic acid mimics a nuclear component required for cyclin B–Cdc2 kinase microinjection to drive starfish oocytes into M phase. J. Cell Biol. 115, 337–44.CrossRefGoogle ScholarPubMed
Picard, A., Galas, S., Peaucellier, G. & Dorée, M. (1996). Newly assembled cyclin B–Cdc2 kinase is required to suppress DNA replication between meiosis I and meiosis II in starfish oocytes. EMBO J. 15, 3590–8.CrossRefGoogle Scholar
Posada, J., Yew, N., Ahn, N.G., Van de Woude, G.F. & Cooper, J.A. (1993). Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol. Cell Biol. 13, 2546–53.Google ScholarPubMed
Qian, Y.W., Erikson, E., Taieb, F.E. & Maller, J.L. (2001). The polo-like kinase Plx1 is required for activation of the phosphatase Cdc25C and cyclin B–Cdc2 in Xenopus oocytes. Mol. Biol. Cell. 12, 1791–9.CrossRefGoogle ScholarPubMed
Rime, H. & Ozon, R. (1990). Protein phosphatase is involved in the in vitro activation of histone H1 kinase in mouse oocytes. Dev. Biol. 141, 115–122.CrossRefGoogle Scholar
Rime, H., Huchon, D., Jessus, C., Goris, J., Merlevede, W. & Ozon, R. (1990). Characterization of MPF activation by okadaic acid in Xenopus oocytes. Cell Differ. Dev. 29, 47–58.CrossRefGoogle Scholar
Sánchez Toranzo, G., Bonilla, F., Zelarayán, L., Oterino, J. & Bühler, M.I. (2006). Activation of maturation promoting factor in Bufo arenarum oocytes: injection of mature cytoplasm and germinal vesicle contents. Zygote 14, 1–12.Google Scholar
Schwartz, D.A. & Schultz, R.M. (1991). Stimulatory effect of okadaic acid, an inhibitor of protein phosphatases, on nuclear envelope breakdown and protein phosphorylation in mouse oocytes and one-cell embryos. Dev. Biol. 145, 119–27.CrossRefGoogle ScholarPubMed
Shibuya, E.K. & Rudeman, J.V. (1993). Mos activates MAP kinase in extracts both quiescent and mitotic cells. Mol. Biol. Cell 4, 781–90.CrossRefGoogle Scholar
Sun, W., Yu, Y., Chiang, H., Fu, Y. & Lu, D. (2002). Exposure to power-frequency magnetic fields can induce activation of P38 mitogen-activated protein kinase.Zhonghua 20, 252–5.Google ScholarPubMed
Tatemoto, H. & Horiuchi, T. (1995). Requirement 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.CrossRefGoogle ScholarPubMed
Verlhac, M.H., de Pennart, H., Maro, B., Cob, 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
Wasserman, W. J. & Masui, Y. (1975). Effects of cycloheximide on a cytoplasmic factor initiating meiotic maturation in Xenopus oocytes. Exp. Cell Res. 91, 381–8.CrossRefGoogle Scholar
Zelarayán, L., Oterino, J. & Bühler, M.I. (1995). Spontaneous maturation in Bufo arenarum oocytes: follicle wall involvement, respiratory activity and seasonal influences. J. Exp. Zool. 272, 356–62.CrossRefGoogle ScholarPubMed
Zelarayán, L., Oterino, J. & Bühler, M.I. (1996). Spontaneous maturation in Bufo arenarum oocytes: participation of protein kinase C. Zygote 4, 257–62.CrossRefGoogle ScholarPubMed
Zelarayán, L., Oterino, J., Sánchez Toranzo, G. & Bühler, M. I. (2000). Involvement of purines and phosphoinositides in spontaneous and progesterone-induced nuclear maturation of Bufo arenarum oocytes. J. Exp. Zool. 287, 151–7.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Zernicka-Goetz, M., Verlhac, M.H., Géraud, G. & Kubiak, J.Z. (1997). Protein phosphatases control MAP kinase activation and microtubule organization during rat oocyte maturation. Eur. J Cell Biol. 72, 30–8.Google ScholarPubMed