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Tyrosine Phosphorylation of MPF and Membrane Proteins During Meiotic Maturation of Starfish Oocytes

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Mechanism of Fertilization: Plants to Humans

Part of the book series: NATO ASI Series ((ASIH,volume 45))

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Summary

It has been reported that the starfish homolog of the fission yeast cdc2 protein is a component of maturation promoting factor (MPF) that controls entry of eukaryotic cells into M-phase. The p34cdc2 protein is phosphorylated during interphase and dephosphorylated during M-phase. We show that starfish p34cdc2 is phosphorylated in vivo on tyrosine, threonine and serine in G2 (prophase I) and Gl (after completion of meiotic divisions). Rephosphorylation of p34cdc2 is not prevented or modified by inhibition of protein synthesis during M-phase.

Tyrosine phosphorylation was found to occur in proteins from oocytes cortices, by immunoprecipitations with an antibody specific for phosphotyrosine. In 32P-preloaded oocytes, labeled phosphotyrosine containing proteins were noticeable only after hormonal induction of meiotic divisions. Labeling increased in five major phosphoproteins of 195, 155, 100, 45 and 35 kDa until first polar body emission, then decreased upon completion of meiosis. Endogenous in vitro phosphorylation of cortices showed a high tyrosine kinase activity towards a 68-kDa protein but no difference between cortices from oocytes treated or not with the hormone.

These findings suggest that tyrosine phosphorylation contributes both to the transduction of the hormonal signal for meiosis resumption and to several steps of the ensuing divisions.

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References

  • Arion D, Meijer L, Brizuela L and Beach D (1988) cdc2 is a component of the M phase-specific histone H1 kinase: evidence for identity with MPF. Cell 55:371–378

    Article  PubMed  CAS  Google Scholar 

  • Bourassa C, Chapdelaine A, Roberts K D and Chevalier S (1988) Enhancement of the detection of alkali-resistant phosphoproteins in Polyacrylamide gels. Anal. Biochem. 169:356–362

    Article  PubMed  CAS  Google Scholar 

  • Brizuela L, Draetta G and Beach D (1987) pl3sucl acts in the fission yeast cell division cycle as a component of the p34cdc2 protein kinase. EMBO J. 6:3507–3514

    PubMed  CAS  Google Scholar 

  • Brizuela L, Draetta G and Beach D (1989) Activation of cdc2 protein as a histone H1 kinase is associated with complex formation with the p62 subunit. Proc. Natl. Acad. Sci. U.S.A. 86:4362–4366

    Article  PubMed  CAS  Google Scholar 

  • Capony J-P, Picard A, Peaucellier G, Labbé J-C and Dorée M (1986) Changes in the activity of the maturation-promoting factor during meiotic maturation and following activation of amphibian and starfish oocytes: their correlation with protein phosphorylation. Dev. Biol. 117:1–12

    Article  CAS  Google Scholar 

  • Chen WS, Lazar CS, Poenie M, Tsien RY, Gill GN and Rosenfeld MG (1987) Requirement for intrinsic protein tyrosine kinase in the immediate and late actions of the EGF receptor. Nature 328:820–823

    Article  PubMed  CAS  Google Scholar 

  • Chou CK, Dull TJ, Russell DS, Gherzi R, Lebwohl D, Ulrich U and Rosen OM (1987) Human insulin receptors mutated at the ATP-binding site lack protein tyrosine kinase activity and fail to mediate postreceptor effects of insulin. J. Biol. Chem. 262:1842–1847

    PubMed  CAS  Google Scholar 

  • Cooper JA, Sefton BM and Hunter T (1983) Detection and quantification of phosphotyrosine in proteins. Methods Enzymol. 99:387–401

    Article  PubMed  CAS  Google Scholar 

  • Dasgrupta JD and Garbers DL (1983) Tyrosine protein kinase activity during embryogenesis. J. Biol. Chem. 258:6174–6178

    Google Scholar 

  • Detering NK, Decker GL, Schmell ED and Lennarz WJ (1977) Isolation and characterization of plasma membrane-associated cortical granules from sea urchin eggs. J. Cell Biol. 75:899–914

    Article  PubMed  CAS  Google Scholar 

  • Dorée M and Guerrier P (1975) Site of action of 1-methyladenine in inducing oocyte maturation in starfishes: Kinetical evidences for receptors localized on the cell surface. Exp. Cell Res. 91:296–300

    Article  PubMed  Google Scholar 

  • Dorée M, Peaucellier G and Picard A (1983) Activity of the maturation-promoting factor and the extent of protein phosphorylation oscillate simultaneously during meiotic maturation of starfish oocytes. Dev. Biol. 99:489–501

    Article  PubMed  Google Scholar 

  • Dunphy WG and Newport JW (1988) Unraveling of mitotic control mechanisms. Cell 55:925–928

    Article  PubMed  CAS  Google Scholar 

  • Dunphy WG and Newport JW (1989) Fission yeast pl3 blocks mitotic activation and tyrosine dephosphorylation of the Xenopus cdc2 protein kinase. Cell 58:181–191

    Article  PubMed  CAS  Google Scholar 

  • Draetta G, Piwnica-Worms H, Morrison D, Druker B, Roberts T and Beach D (1988) Human cdc2 protein kinase is a major cell-cycle regulated tyrosine kinase substrate. Nature 336:738–743

    Article  PubMed  CAS  Google Scholar 

  • Gautier J, Matsukawa T, Nurse P and Maller J (1989) Dephosphorylation and activation of “Xenopus” p34cdc2 protein kinase during the cell cycle. Nature 339:626–628

    Article  PubMed  CAS  Google Scholar 

  • Guerrier P and Dorée M (1975) Hormonal control of reinitiation of meiosis in starfish. The requirement of 1-methyladenine during nuclear maturation. Dev. Biol. 47:341–348

    Article  PubMed  CAS  Google Scholar 

  • Heldin CH and Westermark B (1984) Growth factors: mechanism of action and relation to oncogenes. Cell 37:9–20

    Article  PubMed  CAS  Google Scholar 

  • Hunter T and Cooper J.A. (1985) Protein-tyrosine kinases. Annu. Rev. Biochem. 54:897–930

    Article  PubMed  CAS  Google Scholar 

  • Kamel C, Veno PA and Kinsey WH (1986) Quantitation of a src-like tyrosine protein kinase during fertilization of the sea urchin egg. Biochem. Biophys. Res. Commun. 138:349–355

    Article  PubMed  CAS  Google Scholar 

  • Kamps MP and Sefton BM (1988) Identification of multiple novel polypeptide substrates of the v-src, v-yes, v-fps, v-ros, and v-erb-B oncogenic protein kinases utilizing antisera against phosphotyrosine. Oncogene 2:305–315

    PubMed  CAS  Google Scholar 

  • Kinsey WH (1984) Regulation of tyrosine-specific kinase activity at fertilization. Dev. Biol. 105:137–143

    Article  PubMed  CAS  Google Scholar 

  • Kinsey WH, Decker GL and Lennarz WJ (1980) Isolation and partial characterization of the plasma membrane of the sea urchin egg. J. Cell Biol. 87:248–254

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto T, Kuriyama R, Kondo H and Kanatani H (1982) Generality of the action of various maturation-promoting factors. Exptl. Cell Res. 137: 121–126

    Article  PubMed  CAS  Google Scholar 

  • Labbé J-C, Capony J-P, Caput D, Cavadore J-C, Derancourt J, Kaghad M, Lelias J-M, Picard A and Dorée M (1989) MPF from starfish oocytes at first meiotic metaphase is an heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J. 8:3053–3058

    PubMed  Google Scholar 

  • Labbé J-C, Lee MG, Nurse P, Picard A and Dorée M (1988) Activation at M-phase of a protein kinase encoded by a starfish homologue of the cell cycle control gene cdc2+. Nature 335:251–253

    Article  PubMed  Google Scholar 

  • Labbé JC, Picard A, Peaucellier G, Lee M, Nurse P and Dorée M (1989) Purification of MPF from starfish: identification as the H1 histone kinase p34cdc2 and a possible mechanism for its periodic activation. Cell 57:253–263

    Article  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lee M and Nurse P (1988) Cell cycle control genes in fission yeast and mammalian cells. Trends Genet. 4:287

    Article  PubMed  CAS  Google Scholar 

  • Meijer L, Arion D, Goldstein R, Pines J, Brizuela L, Hunt T and Beach D (1989) Cyclin is a component of the sea urchin egg M-phase specific histone H1 kinase. EMBO J. 8:2275–2282

    PubMed  CAS  Google Scholar 

  • Moria AO, Draetta G, Beach D and Wang JY (1989) Reversible tyrosine phosphorylation of cdc2: dephosphorylation accompanies activation during entry into mitosis. Cell 58:193–203)

    Article  Google Scholar 

  • Peaucellier G, Veno PA and Einsey WH (1988) Protein tyrosine phosphorylation in response to fertilization. J. Biol. Chem. 263:3806–13811

    Google Scholar 

  • Picard A, Peaucellier G, Le Bouffant F, Le Peuch C and Dorée M (1985) Role of protein synthesis and proteases in production and inactivation of maturation-promoting activity during meiotic maturation of starfish oocytes. Dev. Biol. 109:311–320

    Article  PubMed  CAS  Google Scholar 

  • Pondaven P, Meijer L and Pelech SL (1987) Protein phosphorylation in starfish oocyte meiotic divisions and sea urchin egg mitotic divisions. Adv. Protein Phosphatases 4:229–251

    CAS  Google Scholar 

  • Ribot HD, Eisenman EA and Kinsey WH (1984) Fertilization results in increased tyrosine phosphorylation of egg proteins. J. Biol. Chem. 259:5333–5338

    PubMed  CAS  Google Scholar 

  • Ross AH, Baltimore D and Eisen HN (1981) Phosphotyrosine-containing proteins isolated by affinity chromatography with antibodies to a synthetic hapten. Nature 294:654–656

    Article  PubMed  CAS  Google Scholar 

  • Sakanoue Y, Hashimoto E, Nakamura S-I and Yamamura H (1988) Insulin-stimulated serine kinase in Xenopus oocyte plasma membrane. Biochem. Biophys. Res. Commun. 150:1176–1184

    Article  PubMed  CAS  Google Scholar 

  • Satoh N and Garbers DL (1985) Protein tyrosine kinase activity of eggs of the sea urchin Strongylocentrotus purpuratus: The regulation of its increase after fertilization. Dev. Biol. 111:515–519

    Article  PubMed  CAS  Google Scholar 

  • Spivack JG, Erikson RL and Mailer JL (1984) Microinjection of pp60v-src into Xenopus oocytes increases phosphorylation of ribosomal protein S6 and accelerates the rate of progesterone-induced meiotic maturation. Mol. Cell Biol. 4:1631–1634

    PubMed  CAS  Google Scholar 

  • Wang JYJ (1988) Antibodies for phosphotyrosine: analytical and preparative tool for tyrosyl-phosphorylated proteins. Anal. Biochem. 172:1–7

    Article  PubMed  CAS  Google Scholar 

  • Yarden Y and Ullrich A (1988) Growth factor receptor tyrosine kinases. Ann. Rev. Biochem. 57:443–478

    Article  PubMed  CAS  Google Scholar 

  • Yoshikuni M, Ishikawa K, Isobe M, Goto T and Nagahama Y (1988b) Characterization of 1-methyladenine binding in starfish oocyte cortices. Proc. Natl. Acad. Sci. U.S.A. 85:1874–1877

    Article  PubMed  CAS  Google Scholar 

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© 1990 Springer-Verlag Berlin Heidelberg

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Peaucellier, G., Andersen, A.C., Kinsey, W.H., Dorée, M. (1990). Tyrosine Phosphorylation of MPF and Membrane Proteins During Meiotic Maturation of Starfish Oocytes. In: Dale, B. (eds) Mechanism of Fertilization: Plants to Humans. NATO ASI Series, vol 45. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-83965-8_6

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  • DOI: https://doi.org/10.1007/978-3-642-83965-8_6

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-83967-2

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