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. 1991 Sep 1;88(17):7869–7872. doi: 10.1073/pnas.88.17.7869

The c-mos gene product is required for cyclin B accumulation during meiosis of mouse eggs.

S J O'Keefe 1, A A Kiessling 1, G M Cooper 1
PMCID: PMC52405  PMID: 1652768

Abstract

The c-mos protooncogene is expressed as a maternal message that is required for oocyte meiosis. The mechanism of action of c-mos was investigated by analysis of mouse eggs injected with antisense c-mos oligonucleotides. In antisense-injected eggs, maturation-promoting factor was not reactivated after the completion of meiosis I, leading to the formation of nuclei containing decondensed chromatin within 2-3 hr after polar body extrusion. This was correlated with a failure of the injected eggs to accumulate newly synthesized cyclin B. The c-mos protooncogene thus appears to affect the pathway that regulates cyclin B stability during meiosis of mouse eggs.

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Selected References

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

  1. Blair D. G., Oskarsson M., Wood T. G., McClements W. L., Fischinger P. J., Vande Woude G. G. Activation of the transforming potential of a normal cell sequence: a molecular model for oncogenesis. Science. 1981 May 22;212(4497):941–943. doi: 10.1126/science.7233190. [DOI] [PubMed] [Google Scholar]
  2. Clarke H. J., Masui Y. Inhibition by dibutyryl cyclic AMP of the transition to metaphase of mouse oocyte nuclei and its reversal by cell fusion to metaphase oocytes. Dev Biol. 1985 Mar;108(1):32–37. doi: 10.1016/0012-1606(85)90006-5. [DOI] [PubMed] [Google Scholar]
  3. Clarke H. J., Masui Y. The induction of reversible and irreversible chromosome decondensation by protein synthesis inhibition during meiotic maturation of mouse oocytes. Dev Biol. 1983 Jun;97(2):291–301. doi: 10.1016/0012-1606(83)90087-8. [DOI] [PubMed] [Google Scholar]
  4. Clarke H. J., Rossant J., Masui Y. Suppression of chromosome condensation during meiotic maturation induces parthenogenetic development of mouse oocytes. Development. 1988 Sep;104(1):97–103. doi: 10.1242/dev.104.1.97. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Draetta G. Cell cycle control in eukaryotes: molecular mechanisms of cdc2 activation. Trends Biochem Sci. 1990 Oct;15(10):378–383. doi: 10.1016/0968-0004(90)90235-4. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Ford C. C. Maturation promoting factor and cell cycle regulation. J Embryol Exp Morphol. 1985 Nov;89 (Suppl):271–284. [PubMed] [Google Scholar]
  9. Freeman R. S., Ballantyne S. M., Donoghue D. J. Meiotic induction by Xenopus cyclin B is accelerated by coexpression with mosXe. Mol Cell Biol. 1991 Mar;11(3):1713–1717. doi: 10.1128/mcb.11.3.1713. [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. 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]
  12. Glotzer M., Murray A. W., Kirschner M. W. Cyclin is degraded by the ubiquitin pathway. Nature. 1991 Jan 10;349(6305):132–138. doi: 10.1038/349132a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Hadwiger J. A., Wittenberg C., Richardson H. E., de Barros Lopes M., Reed S. I. A family of cyclin homologs that control the G1 phase in yeast. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6255–6259. doi: 10.1073/pnas.86.16.6255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hashimoto N., Kishimoto T. Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Dev Biol. 1988 Apr;126(2):242–252. doi: 10.1016/0012-1606(88)90135-2. [DOI] [PubMed] [Google Scholar]
  16. Jackson K. V., Kiessling A. A. Fertilization and cleavage of mouse oocytes exposed to the conditions of human oocyte retrieval for in vitro fertilization. Fertil Steril. 1989 Apr;51(4):675–681. doi: 10.1016/s0015-0282(16)60620-9. [DOI] [PubMed] [Google Scholar]
  17. Labbé J. C., Capony J. P., Caput D., Cavadore J. C., Derancourt J., Kaghad M., Lelias J. M., Picard A., Dorée M. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J. 1989 Oct;8(10):3053–3058. doi: 10.1002/j.1460-2075.1989.tb08456.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Meijer L., Arion D., Golsteyn R., Pines J., Brizuela L., Hunt T., Beach D. Cyclin is a component of the sea urchin egg M-phase specific histone H1 kinase. EMBO J. 1989 Aug;8(8):2275–2282. doi: 10.1002/j.1460-2075.1989.tb08353.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Newport J. W., Kirschner M. W. Regulation of the cell cycle during early Xenopus development. Cell. 1984 Jul;37(3):731–742. doi: 10.1016/0092-8674(84)90409-4. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. 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. Paules R. S., Buccione R., Moschel R. C., Vande Woude G. F., Eppig J. J. Mouse Mos protooncogene product is present and functions during oogenesis. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5395–5399. doi: 10.1073/pnas.86.14.5395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pines J., Hunter T. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell. 1989 Sep 8;58(5):833–846. doi: 10.1016/0092-8674(89)90936-7. [DOI] [PubMed] [Google Scholar]
  27. Roy L. M., Singh B., Gautier J., Arlinghaus R. B., Nordeen S. K., Maller J. L. The cyclin B2 component of MPF is a substrate for the c-mos(xe) proto-oncogene product. Cell. 1990 Jun 1;61(5):825–831. doi: 10.1016/0092-8674(90)90192-h. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Schmidt M., Oskarsson M. K., Dunn J. K., Blair D. G., Hughes S., Propst F., Vande Woude G. F. Chicken homolog of the mos proto-oncogene. Mol Cell Biol. 1988 Feb;8(2):923–929. doi: 10.1128/mcb.8.2.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Wittenberg C., Sugimoto K., Reed S. I. G1-specific cyclins of S. cerevisiae: cell cycle periodicity, regulation by mating pheromone, and association with the p34CDC28 protein kinase. Cell. 1990 Jul 27;62(2):225–237. doi: 10.1016/0092-8674(90)90361-h. [DOI] [PubMed] [Google Scholar]

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