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. 1991 Jul 1;88(13):5794–5798. doi: 10.1073/pnas.88.13.5794

Progression from meiosis I to meiosis II in Xenopus oocytes requires de novo translation of the mosxe protooncogene.

J P Kanki 1, D J Donoghue 1
PMCID: PMC51964  PMID: 1648231

Abstract

The meiotic maturation of Xenopus oocytes exhibits an early requirement for expression of the mosxe protooncogene. The mosxe protein has also been shown to be a component of cytostatic factor (CSF), which is responsible for arrest at metaphase of meiosis II. In this study, we have assayed the appearance of CSF activity in oocytes induced to mature either by progesterone treatment or by overexpression of mosxe. Progesterone-stimulated oocytes did not exhibit CSF activity until 30-60 min after germinal vesicle breakdown (GVBD). Both the appearance of CSF activity and the progression from meiosis I to meiosis II were inhibited by microinjection of mosxe antisense oligonucleotides just prior to GVBD. These results demonstrate a translational requirement for mosxe, which is temporally distinct from the requirement for mosxe expression at the onset of meiotic maturation. In contrast to progesterone-treated oocytes, oocytes that were induced to mature by overexpression of mosxe exhibited CSF activity at least 3 hr prior to GVBD. Despite the early appearance of CSF, these oocytes were not arrested at meiosis I. These results indicate that, although CSF activity is capable of stabilizing maturation-promoting factor (MPF) at meiosis II and in cleaving embryos, it is incapable of stabilizing MPF prior to or at meiosis I. These studies show that the complex regulation of the cell cycle during meiosis differs significantly from the regulation of the cell cycle during mitosis.

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Selected References

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

  1. Arion D., Meijer L., Brizuela L., Beach D. cdc2 is a component of the M phase-specific histone H1 kinase: evidence for identity with MPF. Cell. 1988 Oct 21;55(2):371–378. doi: 10.1016/0092-8674(88)90060-8. [DOI] [PubMed] [Google Scholar]
  2. Cyert M. S., Kirschner M. W. Regulation of MPF activity in vitro. Cell. 1988 Apr 22;53(2):185–195. doi: 10.1016/0092-8674(88)90380-7. [DOI] [PubMed] [Google Scholar]
  3. Draetta G., Beach D. Activation of cdc2 protein kinase during mitosis in human cells: cell cycle-dependent phosphorylation and subunit rearrangement. Cell. 1988 Jul 1;54(1):17–26. doi: 10.1016/0092-8674(88)90175-4. [DOI] [PubMed] [Google Scholar]
  4. Draetta G., Luca F., Westendorf J., Brizuela L., Ruderman J., Beach D. Cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF. Cell. 1989 Mar 10;56(5):829–838. doi: 10.1016/0092-8674(89)90687-9. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Evans T., Rosenthal E. T., Youngblom J., Distel D., Hunt T. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell. 1983 Jun;33(2):389–396. doi: 10.1016/0092-8674(83)90420-8. [DOI] [PubMed] [Google Scholar]
  7. Freeman R. S., Donoghue D. J. Protein kinases and protooncogenes: biochemical regulators of the eukaryotic cell cycle. Biochemistry. 1991 Mar 5;30(9):2293–2302. doi: 10.1021/bi00223a001. [DOI] [PubMed] [Google Scholar]
  8. Freeman R. S., Kanki J. P., Ballantyne S. M., Pickham K. M., Donoghue D. J. Effects of the v-mos oncogene on Xenopus development: meiotic induction in oocytes and mitotic arrest in cleaving embryos. J Cell Biol. 1990 Aug;111(2):533–541. doi: 10.1083/jcb.111.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Freeman R. S., Pickham K. M., Kanki J. P., Lee B. A., Pena S. V., Donoghue D. J. Xenopus homolog of the mos protooncogene transforms mammalian fibroblasts and induces maturation of Xenopus oocytes. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5805–5809. doi: 10.1073/pnas.86.15.5805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gautier J., Minshull J., Lohka M., Glotzer M., Hunt T., Maller J. L. Cyclin is a component of maturation-promoting factor from Xenopus. Cell. 1990 Feb 9;60(3):487–494. doi: 10.1016/0092-8674(90)90599-a. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Labbe J. C., Lee M. G., Nurse P., Picard A., Doree M. Activation at M-phase of a protein kinase encoded by a starfish homologue of the cell cycle control gene cdc2+. Nature. 1988 Sep 15;335(6187):251–254. doi: 10.1038/335251a0. [DOI] [PubMed] [Google Scholar]
  14. Maller J. L. Xenopus oocytes and the biochemistry of cell division. Biochemistry. 1990 Apr 3;29(13):3157–3166. doi: 10.1021/bi00465a001. [DOI] [PubMed] [Google Scholar]
  15. Masui Y., Markert C. L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool. 1971 Jun;177(2):129–145. doi: 10.1002/jez.1401770202. [DOI] [PubMed] [Google Scholar]
  16. Meyerhof P. G., Masui Y. Ca and Mg control of cytostatic factors from Rana pipiens oocytes which cause metaphase and cleavage arrest. Dev Biol. 1977 Dec;61(2):214–229. doi: 10.1016/0012-1606(77)90293-7. [DOI] [PubMed] [Google Scholar]
  17. Meyerhof P. G., Masui Y. Properties of a cytostatic factor from Xenopus laevis eggs. Dev Biol. 1979 Sep;72(1):182–187. doi: 10.1016/0012-1606(79)90108-8. [DOI] [PubMed] [Google Scholar]
  18. Minshull J., Blow J. J., Hunt T. Translation of cyclin mRNA is necessary for extracts of activated xenopus eggs to enter mitosis. Cell. 1989 Mar 24;56(6):947–956. doi: 10.1016/0092-8674(89)90628-4. [DOI] [PubMed] [Google Scholar]
  19. Moreno S., Nurse P. Substrates for p34cdc2: in vivo veritas? Cell. 1990 May 18;61(4):549–551. doi: 10.1016/0092-8674(90)90463-o. [DOI] [PubMed] [Google Scholar]
  20. Murray A. W., Kirschner M. W. Cyclin synthesis drives the early embryonic cell cycle. Nature. 1989 May 25;339(6222):275–280. doi: 10.1038/339275a0. [DOI] [PubMed] [Google Scholar]
  21. Murray A. W., Solomon M. J., Kirschner M. W. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature. 1989 May 25;339(6222):280–286. doi: 10.1038/339280a0. [DOI] [PubMed] [Google Scholar]
  22. Nurse P. Universal control mechanism regulating onset of M-phase. Nature. 1990 Apr 5;344(6266):503–508. doi: 10.1038/344503a0. [DOI] [PubMed] [Google Scholar]
  23. O'Keefe S. J., Wolfes H., Kiessling A. A., Cooper G. M. Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7038–7042. doi: 10.1073/pnas.86.18.7038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pines J., Hunter T. p34cdc2: the S and M kinase? New Biol. 1990 May;2(5):389–401. [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Sagata N., Watanabe N., Vande Woude G. F., Ikawa Y. The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs. Nature. 1989 Nov 30;342(6249):512–518. doi: 10.1038/342512a0. [DOI] [PubMed] [Google Scholar]
  29. Smith L. D., Ecker R. E. The interaction of steroids with Rana pipiens Oocytes in the induction of maturation. Dev Biol. 1971 Jun;25(2):232–247. doi: 10.1016/0012-1606(71)90029-7. [DOI] [PubMed] [Google Scholar]
  30. Solomon M. J., Glotzer M., Lee T. H., Philippe M., Kirschner M. W. Cyclin activation of p34cdc2. Cell. 1990 Nov 30;63(5):1013–1024. doi: 10.1016/0092-8674(90)90504-8. [DOI] [PubMed] [Google Scholar]
  31. Wasserman W. J., Masui Y. A cytoplasmic factor promoting oocyte maturation: its extraction and preliminary characterization. Science. 1976 Mar 26;191(4233):1266–1268. doi: 10.1126/science.1083070. [DOI] [PubMed] [Google Scholar]
  32. Wasserman W. J., Masui Y. Effects of cyclohexamide on a cytoplasmic factor initiating meiotic naturation in Xenopus oocytes. Exp Cell Res. 1975 Mar 15;91(2):381–388. doi: 10.1016/0014-4827(75)90118-4. [DOI] [PubMed] [Google Scholar]
  33. Wasserman W. J., Smith L. D. The cyclic behavior of a cytoplasmic factor controlling nuclear membrane breakdown. J Cell Biol. 1978 Jul;78(1):R15–R22. doi: 10.1083/jcb.78.1.r15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Watanabe N., Vande Woude G. F., Ikawa Y., Sagata N. Specific proteolysis of the c-mos proto-oncogene product by calpain on fertilization of Xenopus eggs. Nature. 1989 Nov 30;342(6249):505–511. doi: 10.1038/342505a0. [DOI] [PubMed] [Google Scholar]
  35. Westendorf J. M., Swenson K. I., Ruderman J. V. The role of cyclin B in meiosis I. J Cell Biol. 1989 Apr;108(4):1431–1444. doi: 10.1083/jcb.108.4.1431. [DOI] [PMC free article] [PubMed] [Google Scholar]

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