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. 1997 Nov;17(11):6419–6426. doi: 10.1128/mcb.17.11.6419

The Mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes.

C H de Moor 1, J D Richter 1
PMCID: PMC232494  PMID: 9343404

Abstract

Cytoplasmic polyadenylation controls the translation of several maternal mRNAs during Xenopus oocyte maturation and requires two sequences in the 3' untranslated region (UTR), the U-rich cytoplasmic polyadenylation element (CPE), and the hexanucleotide AAUAAA. c-mos mRNA is polyadenylated and translated soon after the induction of maturation, and this protein kinase is necessary for a kinase cascade culminating in cdc2 kinase (MPF) activation. Other mRNAs are polyadenylated later, around the time of cdc2 kinase activation. To determine whether there is a hierarchy in the cytoplasmic polyadenylation of maternal mRNAs, we ablated c-mos mRNA with an antisense oligonucleotide. This prevented histone B4 and cyclin A1 and B1 mRNA polyadenylation, indicating that the polyadenylation of these mRNAs is Mos dependent. To investigate a possible role of cdc2 kinase in this process, cyclin B was injected into oocytes lacking c-mos mRNA. cdc2 kinase was activated, but mitogen-activated protein kinase was not. However, polyadenylation of cyclin B1 and histone B4 mRNA was still observed. This demonstrates that cdc2 kinase can induce cytoplasmic polyadenylation in the absence of Mos. Our data further indicate that although phosphorylation of the CPE binding protein may be involved in the induction of Mos-dependent polyadenylation, it is not required for Mos-independent polyadenylation. We characterized the elements conferring Mos dependence (Mos response elements) in the histone B4 and cyclin B1 mRNAs by mutational analysis. For histone B4 mRNA, the Mos response elements were in the coding region or 5' UTR. For cyclin B1 mRNA, the main Mos response element was a CPE that overlaps with the AAUAAA hexanucleotide. This indicates that the position of the CPE can have a profound influence on the timing of cytoplasmic polyadenylation.

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Selected References

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  1. Bilger A., Fox C. A., Wahle E., Wickens M. Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements. Genes Dev. 1994 May 1;8(9):1106–1116. doi: 10.1101/gad.8.9.1106. [DOI] [PubMed] [Google Scholar]
  2. Cho H., Wolffe A. P. Xenopus laevis B4, an intron-containing oocyte-specific linker histone-encoding gene. Gene. 1994 Jun 10;143(2):233–238. doi: 10.1016/0378-1119(94)90102-3. [DOI] [PubMed] [Google Scholar]
  3. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Curtis D., Lehmann R., Zamore P. D. Translational regulation in development. Cell. 1995 Apr 21;81(2):171–178. doi: 10.1016/0092-8674(95)90325-9. [DOI] [PubMed] [Google Scholar]
  5. Gebauer F., Richter J. D. Synthesis and function of Mos: the control switch of vertebrate oocyte meiosis. Bioessays. 1997 Jan;19(1):23–28. doi: 10.1002/bies.950190106. [DOI] [PubMed] [Google Scholar]
  6. Gebauer F., Xu W., Cooper G. M., Richter J. D. Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 1994 Dec 1;13(23):5712–5720. doi: 10.1002/j.1460-2075.1994.tb06909.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gotoh Y., Masuyama N., Dell K., Shirakabe K., Nishida E. Initiation of Xenopus oocyte maturation by activation of the mitogen-activated protein kinase cascade. J Biol Chem. 1995 Oct 27;270(43):25898–25904. doi: 10.1074/jbc.270.43.25898. [DOI] [PubMed] [Google Scholar]
  8. Hake L. E., Richter J. D. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell. 1994 Nov 18;79(4):617–627. doi: 10.1016/0092-8674(94)90547-9. [DOI] [PubMed] [Google Scholar]
  9. Hake L. E., Richter J. D. Translational regulation of maternal mRNA. Biochim Biophys Acta. 1997 Feb 22;1332(1):M31–M38. doi: 10.1016/s0304-419x(96)00039-x. [DOI] [PubMed] [Google Scholar]
  10. KIRBY K. S. ISOLATION AND CHARACTERIZATION OF RIBOSOMAL RIBONUCLEIC ACID. Biochem J. 1965 Jul;96:266–269. doi: 10.1042/bj0960266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kobayashi H., Minshull J., Ford C., Golsteyn R., Poon R., Hunt T. On the synthesis and destruction of A- and B-type cyclins during oogenesis and meiotic maturation in Xenopus laevis. J Cell Biol. 1991 Aug;114(4):755–765. doi: 10.1083/jcb.114.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kosako H., Gotoh Y., Nishida E. Regulation and function of the MAP kinase cascade in Xenopus oocytes. J Cell Sci Suppl. 1994;18:115–119. doi: 10.1242/jcs.1994.supplement_18.17. [DOI] [PubMed] [Google Scholar]
  13. Kuge H., Richter J. D. Cytoplasmic 3' poly(A) addition induces 5' cap ribose methylation: implications for translational control of maternal mRNA. EMBO J. 1995 Dec 15;14(24):6301–6310. doi: 10.1002/j.1460-2075.1995.tb00320.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lee T. H., Kirschner M. W. An inhibitor of p34cdc2/cyclin B that regulates the G2/M transition in Xenopus extracts. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):352–356. doi: 10.1073/pnas.93.1.352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. MacLachlan T. K., Sang N., Giordano A. Cyclins, cyclin-dependent kinases and cdk inhibitors: implications in cell cycle control and cancer. Crit Rev Eukaryot Gene Expr. 1995;5(2):127–156. doi: 10.1615/critreveukargeneexpr.v5.i2.20. [DOI] [PubMed] [Google Scholar]
  16. Macdonald P. M., Smibert C. A. Translational regulation of maternal mRNAs. Curr Opin Genet Dev. 1996 Aug;6(4):403–407. doi: 10.1016/s0959-437x(96)80060-8. [DOI] [PubMed] [Google Scholar]
  17. Manley J. L. A complex protein assembly catalyzes polyadenylation of mRNA precursors. Curr Opin Genet Dev. 1995 Apr;5(2):222–228. doi: 10.1016/0959-437x(95)80012-3. [DOI] [PubMed] [Google Scholar]
  18. Nebreda A. R., Gannon J. V., Hunt T. Newly synthesized protein(s) must associate with p34cdc2 to activate MAP kinase and MPF during progesterone-induced maturation of Xenopus oocytes. EMBO J. 1995 Nov 15;14(22):5597–5607. doi: 10.1002/j.1460-2075.1995.tb00247.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nebreda A. R., Hunt T. The c-mos proto-oncogene 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. 1993 May;12(5):1979–1986. doi: 10.1002/j.1460-2075.1993.tb05847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nigg E. A. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays. 1995 Jun;17(6):471–480. doi: 10.1002/bies.950170603. [DOI] [PubMed] [Google Scholar]
  21. Paris J., Swenson K., Piwnica-Worms H., Richter J. D. Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein. Genes Dev. 1991 Sep;5(9):1697–1708. doi: 10.1101/gad.5.9.1697. [DOI] [PubMed] [Google Scholar]
  22. Pines J. Cyclins and cyclin-dependent kinases: a biochemical view. Biochem J. 1995 Jun 15;308(Pt 3):697–711. doi: 10.1042/bj3080697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Sagata N. What does Mos do in oocytes and somatic cells? Bioessays. 1997 Jan;19(1):13–21. doi: 10.1002/bies.950190105. [DOI] [PubMed] [Google Scholar]
  25. Sheets M. D., Fox C. A., Hunt T., Vande Woude G., Wickens M. The 3'-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 1994 Apr 15;8(8):926–938. doi: 10.1101/gad.8.8.926. [DOI] [PubMed] [Google Scholar]
  26. Sheets M. D., Wu M., Wickens M. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature. 1995 Apr 6;374(6522):511–516. doi: 10.1038/374511a0. [DOI] [PubMed] [Google Scholar]
  27. Simon R., Tassan J. P., Richter J. D. Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev. 1992 Dec;6(12B):2580–2591. doi: 10.1101/gad.6.12b.2580. [DOI] [PubMed] [Google Scholar]
  28. Smith R. C., Dworkin-Rastl E., Dworkin M. B. Expression of a histone H1-like protein is restricted to early Xenopus development. Genes Dev. 1988 Oct;2(10):1284–1295. doi: 10.1101/gad.2.10.1284. [DOI] [PubMed] [Google Scholar]
  29. St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
  30. Stebbins-Boaz B., Hake L. E., Richter J. D. CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 1996 May 15;15(10):2582–2592. [PMC free article] [PubMed] [Google Scholar]
  31. Stebbins-Boaz B., Richter J. D. Multiple sequence elements and a maternal mRNA product control cdk2 RNA polyadenylation and translation during early Xenopus development. Mol Cell Biol. 1994 Sep;14(9):5870–5880. doi: 10.1128/mcb.14.9.5870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wahle E. 3'-end cleavage and polyadenylation of mRNA precursors. Biochim Biophys Acta. 1995 Apr 4;1261(2):183–194. doi: 10.1016/0167-4781(94)00248-2. [DOI] [PubMed] [Google Scholar]
  33. Wormington M. Preparation of synthetic mRNAs and analyses of translational efficiency in microinjected Xenopus oocytes. Methods Cell Biol. 1991;36:167–183. doi: 10.1016/s0091-679x(08)60277-0. [DOI] [PubMed] [Google Scholar]

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