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. 1990 Jan;10(1):310–315. doi: 10.1128/mcb.10.1.310

Ha-rasVal-12,Thr-59 activates S6 kinase and p34cdc2 kinase in Xenopus oocytes: evidence for c-mosxe-dependent and -independent pathways.

C B Barrett 1, R M Schroetke 1, F A Van der Hoorn 1, S K Nordeen 1, J L Maller 1
PMCID: PMC360742  PMID: 2152963

Abstract

Treatment with insulin or progesterone or microinjection of the transforming protein product of Ha-rasVal-12,Thr-59 (p21) is known to induce germinal vesicle breakdown in Xenopus oocytes. We have investigated the effect of p21 on S6 kinase and the H1 histone kinase of maturation-promoting factor in the presence and absence of antisense oligonucleotides against the c-mosxe proto-oncogene. Injection of p21 led to a rapid increase in S6 phosphorylation, with kinetics similar to those previously observed with insulin. Microinjection of c-mosxe antisense oligonucleotides inhibited germinal vesicle breakdown induced by p21 and totally abolished S6 kinase activation by insulin or progesterone but only partially inhibited activation by p21. However, the activation of p34cdc2 protein kinase by all three stimuli was blocked by antisense oligonucleotides. The results suggest that in oocyte maturation c-mosxe functions downstream of p21 but upstream of p34cdc2 and S6 kinase activation, although not all p21-induced events require c-mosxe.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allende C. C., Hinrichs M. V., Santos E., Allende J. E. Oncogenic ras protein induces meiotic maturation of amphibian oocytes in the presence of protein synthesis inhibitors. FEBS Lett. 1988 Jul 18;234(2):426–430. doi: 10.1016/0014-5793(88)80130-3. [DOI] [PubMed] [Google Scholar]
  2. Birchmeier C., Broek D., Wigler M. ras proteins can induce meiosis in Xenopus oocytes. Cell. 1985 Dec;43(3 Pt 2):615–621. doi: 10.1016/0092-8674(85)90233-8. [DOI] [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  4. Cicirelli M. F., Pelech S. L., Krebs E. G. Activation of multiple protein kinases during the burst in protein phosphorylation that precedes the first meiotic cell division in Xenopus oocytes. J Biol Chem. 1988 Feb 5;263(4):2009–2019. [PubMed] [Google Scholar]
  5. Deshpande A. K., Kung H. F. Insulin induction of Xenopus laevis oocyte maturation is inhibited by monoclonal antibody against p21 ras proteins. Mol Cell Biol. 1987 Mar;7(3):1285–1288. doi: 10.1128/mcb.7.3.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dunphy W. G., Brizuela L., Beach D., Newport J. The Xenopus cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis. Cell. 1988 Jul 29;54(3):423–431. doi: 10.1016/0092-8674(88)90205-x. [DOI] [PubMed] [Google Scholar]
  7. El-Etr M., Schorderet-Slatkine S., Baulieu E. E. Meiotic maturation in Xenopus laevis oocytes initiated by insulin. Science. 1979 Sep 28;205(4413):1397–1399. doi: 10.1126/science.472755. [DOI] [PubMed] [Google Scholar]
  8. Erikson E., Maller J. L. A protein kinase from Xenopus eggs specific for ribosomal protein S6. Proc Natl Acad Sci U S A. 1985 Feb;82(3):742–746. doi: 10.1073/pnas.82.3.742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Erikson E., Maller J. L. Purification and characterization of a protein kinase from Xenopus eggs highly specific for ribosomal protein S6. J Biol Chem. 1986 Jan 5;261(1):350–355. [PubMed] [Google Scholar]
  10. Erikson E., Stefanovic D., Blenis J., Erikson R. L., Maller J. L. Antibodies to Xenopus egg S6 kinase II recognize S6 kinase from progesterone- and insulin-stimulated Xenopus oocytes and from proliferating chicken embryo fibroblasts. Mol Cell Biol. 1987 Sep;7(9):3147–3155. doi: 10.1128/mcb.7.9.3147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Finidori-Lepicard J., Schorderet-Slatkine S., Hanoune J., Baulieu E. E. Progesterone inhibits membrane-bound adenylate cyclase in Xenopus laevis oocytes. Nature. 1981 Jul 16;292(5820):255–257. doi: 10.1038/292255a0. [DOI] [PubMed] [Google Scholar]
  12. Gautier J., Matsukawa T., Nurse P., Maller J. Dephosphorylation and activation of Xenopus p34cdc2 protein kinase during the cell cycle. Nature. 1989 Jun 22;339(6226):626–629. doi: 10.1038/339626a0. [DOI] [PubMed] [Google Scholar]
  13. Gautier J., Norbury C., Lohka M., Nurse P., Maller J. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+. Cell. 1988 Jul 29;54(3):433–439. doi: 10.1016/0092-8674(88)90206-1. [DOI] [PubMed] [Google Scholar]
  14. Gerhart J., Wu M., Kirschner M. Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J Cell Biol. 1984 Apr;98(4):1247–1255. doi: 10.1083/jcb.98.4.1247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gibbs J. B., Sigal I. S., Poe M., Scolnick E. M. Intrinsic GTPase activity distinguishes normal and oncogenic ras p21 molecules. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5704–5708. doi: 10.1073/pnas.81.18.5704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Glass D. B., Masaracchia R. A., Feramisco J. R., Kemp B. E. Isolation of phosphorylated peptides and proteins on ion exchange papers. Anal Biochem. 1978 Jul 1;87(2):566–575. doi: 10.1016/0003-2697(78)90707-8. [DOI] [PubMed] [Google Scholar]
  17. Goldman D. S., Kiessling A. A., Millette C. F., Cooper G. M. Expression of c-mos RNA in germ cells of male and female mice. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4509–4513. doi: 10.1073/pnas.84.13.4509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hanocq-Quertier J., Baltus E. Phosphorylation of ribosomal proteins during maturation of Xenopus laevis oocytes. Eur J Biochem. 1981 Nov;120(2):351–355. doi: 10.1111/j.1432-1033.1981.tb05711.x. [DOI] [PubMed] [Google Scholar]
  19. Keshet E., Rosenberg M. P., Mercer J. A., Propst F., Vande Woude G. F., Jenkins N. A., Copeland N. G. Developmental regulation of ovarian-specific Mos expression. Oncogene. 1988 Mar;2(3):235–240. [PubMed] [Google Scholar]
  20. Kishimoto T., Kuriyama R., Kondo H., Kanatani H. Generality of the action of various maturation-promoting factors. Exp Cell Res. 1982 Jan;137(1):121–126. doi: 10.1016/0014-4827(82)90014-3. [DOI] [PubMed] [Google Scholar]
  21. Korn L. J., Siebel C. W., McCormick F., Roth R. A. Ras p21 as a potential mediator of insulin action in Xenopus oocytes. Science. 1987 May 15;236(4803):840–843. doi: 10.1126/science.3554510. [DOI] [PubMed] [Google Scholar]
  22. Kruppa J., Darmer D., Kalthoff H., Richter D. The phosphorylation of ribosomal protein S6 from progesterone-stimulated Xenopus laevis oocytes. Kinetic studies and phosphopeptide analysis. Eur J Biochem. 1983 Jan 1;129(3):537–542. doi: 10.1111/j.1432-1033.1983.tb07082.x. [DOI] [PubMed] [Google Scholar]
  23. Lacal J. C., de la Peña P., Moscat J., Garcia-Barreno P., Anderson P. S., Aaronson S. A. Rapid stimulation of diacylglycerol production in Xenopus oocytes by microinjection of H-ras p21. Science. 1987 Oct 23;238(4826):533–536. doi: 10.1126/science.2821623. [DOI] [PubMed] [Google Scholar]
  24. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  25. Lohka M. J., Hayes M. K., Maller J. L. Purification of maturation-promoting factor, an intracellular regulator of early mitotic events. Proc Natl Acad Sci U S A. 1988 May;85(9):3009–3013. doi: 10.1073/pnas.85.9.3009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maller J. L., Butcher F. R., Krebs E. G. Early effect of progesterone on levels of cyclic adenosine 3':5'-monophosphate in Xenopus oocytes. J Biol Chem. 1979 Feb 10;254(3):579–582. [PubMed] [Google Scholar]
  27. Maller J., Wu M., Gerhart J. C. Changes in protein phosphorylation accompanying maturation of Xenopus laevis oocytes. Dev Biol. 1977 Jul 15;58(2):295–312. doi: 10.1016/0012-1606(77)90093-8. [DOI] [PubMed] [Google Scholar]
  28. Maxwell S. A., Arlinghaus R. B. Serine kinase activity associated with Maloney murine sarcoma virus-124-encoded p37mos. Virology. 1985 May;143(1):321–333. doi: 10.1016/0042-6822(85)90119-9. [DOI] [PubMed] [Google Scholar]
  29. Mutter G. L., Wolgemuth D. J. Distinct developmental patterns of c-mos protooncogene expression in female and male mouse germ cells. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5301–5305. doi: 10.1073/pnas.84.15.5301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nielsen P. J., Thomas G., Maller J. L. Increased phosphorylation of ribosomal protein S6 during meiotic maturation of Xenopus oocytes. Proc Natl Acad Sci U S A. 1982 May;79(9):2937–2941. doi: 10.1073/pnas.79.9.2937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Noda M., Selinger Z., Scolnick E. M., Bassin R. H. Flat revertants isolated from Kirsten sarcoma virus-transformed cells are resistant to the action of specific oncogenes. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5602–5606. doi: 10.1073/pnas.80.18.5602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Propst F., Rosenberg M. P., Iyer A., Kaul K., Vande Woude G. F. c-mos proto-oncogene RNA transcripts in mouse tissues: structural features, developmental regulation, and localization in specific cell types. Mol Cell Biol. 1987 May;7(5):1629–1637. doi: 10.1128/mcb.7.5.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ray L. B., Sturgill T. W. Insulin-stimulated microtubule-associated protein kinase is phosphorylated on tyrosine and threonine in vivo. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3753–3757. doi: 10.1073/pnas.85.11.3753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Reynhout J. K., Smith L. D. Studies on the appearance and nature of a maturation-inducing factor in the cytoplasm of amphibian oocytes exposed to progesterone. Dev Biol. 1974 Jun;38(2):394–400. doi: 10.1016/0012-1606(74)90016-5. [DOI] [PubMed] [Google Scholar]
  35. Sadler S. E., Maller J. L. A similar pool of cyclic AMP phosphodiesterase in Xenopus oocytes is stimulated by insulin, insulin-like growth factor 1, and [Val12,Thr59]Ha-ras protein. J Biol Chem. 1989 Jan 15;264(2):856–861. [PubMed] [Google Scholar]
  36. Sagata N., Daar I., Oskarsson M., Showalter S. D., Vande Woude G. F. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation. Science. 1989 Aug 11;245(4918):643–646. doi: 10.1126/science.2474853. [DOI] [PubMed] [Google Scholar]
  37. Sagata N., Oskarsson M., Copeland T., Brumbaugh J., Vande Woude G. F. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature. 1988 Oct 6;335(6190):519–525. doi: 10.1038/335519a0. [DOI] [PubMed] [Google Scholar]
  38. Smith M. R., DeGudicibus S. J., Stacey D. W. Requirement for c-ras proteins during viral oncogene transformation. Nature. 1986 Apr 10;320(6062):540–543. doi: 10.1038/320540a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stefanovic D., Maller J. L. Post-transcriptional regulation by insulin of Xenopus ribosomal protein S6 kinase. Exp Cell Res. 1988 Nov;179(1):104–114. doi: 10.1016/0014-4827(88)90352-7. [DOI] [PubMed] [Google Scholar]
  40. Stith B. J., Maller J. L. Induction of meiotic maturation in Xenopus oocytes by 12-O-tetradecanoylphorbol 13-acetate. Exp Cell Res. 1987 Apr;169(2):514–523. doi: 10.1016/0014-4827(87)90211-4. [DOI] [PubMed] [Google Scholar]
  41. Stith B. J., Maller J. L. The effect of insulin on intracellular ph and ribosomal protein S6 phosphorylation in oocytes of Xenopus laevis. Dev Biol. 1984 Mar;102(1):79–89. doi: 10.1016/0012-1606(84)90176-3. [DOI] [PubMed] [Google Scholar]
  42. Sturgill T. W., Ray L. B., Erikson E., Maller J. L. Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature. 1988 Aug 25;334(6184):715–718. doi: 10.1038/334715a0. [DOI] [PubMed] [Google Scholar]
  43. Tachibana K., Yanagishima N., Kishimoto T. Preliminary characterization of maturation-promoting factor from yeast Saccharomyces cerevisiae. J Cell Sci. 1987 Oct;88(Pt 3):273–281. doi: 10.1242/jcs.88.3.273. [DOI] [PubMed] [Google Scholar]
  44. Wasserman W. J., Richter J. D., Smith L. D. Protein synthesis during maturation promoting factor- and progesterone-induced maturation in Xenopus oocytes. Dev Biol. 1982 Jan;89(1):152–158. doi: 10.1016/0012-1606(82)90303-7. [DOI] [PubMed] [Google Scholar]

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