Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Aug 20;93(17):9027–9032. doi: 10.1073/pnas.93.17.9027

Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylylation.

A C Verrotti 1, S R Thompson 1, C Wreden 1, S Strickland 1, M Wickens 1
PMCID: PMC38589  PMID: 8799148

Abstract

Cytoplasmic polyadenylylation is an evolutionarily conserved mechanism involved in the translational activation of a set of maternal messenger RNAs (mRNAs) during early development. In this report, we show by interspecies injections that Xenopus and mouse use the same regulatory sequences to control cytoplasmic poly(A) addition during meiotic maturation. Similarly, Xenopus and Drosophila embryos exploit functionally conserved signals to regulate polyadenylylation during early post-fertilization development. These experiments demonstrate that the sequence elements that govern cytoplasmic polyadenylylation, and hence one form of translational activation, function across species. We infer that the requisite regulatory sequence elements, and likely the trans-acting components with which they interact, have been conserved since the divergence of vertebrates and arthropods.

Full text

PDF
9027

Images in this article

9029Fig. 1
on p.9029
9030Fig. 2
on p.9030
9031Fig. 3
on p.9031

Selected References

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

  1. Bachvarova R. F. A maternal tail of poly(A): the long and the short of it. Cell. 1992 Jun 12;69(6):895–897. doi: 10.1016/0092-8674(92)90606-d. [DOI] [PubMed] [Google Scholar]
  2. Ballantyne S., Bilger A., Astrom J., Virtanen A., Wickens M. Poly (A) polymerases in the nucleus and cytoplasm of frog oocytes: dynamic changes during oocyte maturation and early development. RNA. 1995 Mar;1(1):64–78. [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  5. Christerson L. B., McKearin D. M. orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev. 1994 Mar 1;8(5):614–628. doi: 10.1101/gad.8.5.614. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Driever W., Nüsslein-Volhard C. A gradient of bicoid protein in Drosophila embryos. Cell. 1988 Jul 1;54(1):83–93. doi: 10.1016/0092-8674(88)90182-1. [DOI] [PubMed] [Google Scholar]
  8. Driever W., Siegel V., Nüsslein-Volhard C. Autonomous determination of anterior structures in the early Drosophila embryo by the bicoid morphogen. Development. 1990 Aug;109(4):811–820. doi: 10.1242/dev.109.4.811. [DOI] [PubMed] [Google Scholar]
  9. Fox C. A., Sheets M. D., Wahle E., Wickens M. Polyadenylation of maternal mRNA during oocyte maturation: poly(A) addition in vitro requires a regulated RNA binding activity and a poly(A) polymerase. EMBO J. 1992 Dec;11(13):5021–5032. doi: 10.1002/j.1460-2075.1992.tb05609.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fox C. A., Sheets M. D., Wickens M. P. Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev. 1989 Dec;3(12B):2151–2162. doi: 10.1101/gad.3.12b.2151. [DOI] [PubMed] [Google Scholar]
  11. Fox C. A., Wickens M. Poly(A) removal during oocyte maturation: a default reaction selectively prevented by specific sequences in the 3' UTR of certain maternal mRNAs. Genes Dev. 1990 Dec;4(12B):2287–2298. doi: 10.1101/gad.4.12b.2287. [DOI] [PubMed] [Google Scholar]
  12. Gebauer F., Richter J. D. Cloning and characterization of a Xenopus poly(A) polymerase. Mol Cell Biol. 1995 Mar;15(3):1422–1430. doi: 10.1128/mcb.15.3.1422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Gottlieb E. The 3' untranslated region of localized maternal messages contains a conserved motif involved in mRNA localization. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7164–7168. doi: 10.1073/pnas.89.15.7164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Huarte J., Belin D., Vassalli A., Strickland S., Vassalli J. D. Meiotic maturation of mouse oocytes triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA. Genes Dev. 1987 Dec;1(10):1201–1211. doi: 10.1101/gad.1.10.1201. [DOI] [PubMed] [Google Scholar]
  17. Huarte J., Belin D., Vassalli J. D. Plasminogen activator in mouse and rat oocytes: induction during meiotic maturation. Cell. 1985 Dec;43(2 Pt 1):551–558. doi: 10.1016/0092-8674(85)90184-9. [DOI] [PubMed] [Google Scholar]
  18. Huarte J., Stutz A., O'Connell M. L., Gubler P., Belin D., Darrow A. L., Strickland S., Vassalli J. D. Transient translational silencing by reversible mRNA deadenylation. Cell. 1992 Jun 12;69(6):1021–1030. doi: 10.1016/0092-8674(92)90620-r. [DOI] [PubMed] [Google Scholar]
  19. Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lantz V., Chang J. S., Horabin J. I., Bopp D., Schedl P. The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev. 1994 Mar 1;8(5):598–613. doi: 10.1101/gad.8.5.598. [DOI] [PubMed] [Google Scholar]
  21. McGrew L. L., Dworkin-Rastl E., Dworkin M. B., Richter J. D. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 1989 Jun;3(6):803–815. doi: 10.1101/gad.3.6.803. [DOI] [PubMed] [Google Scholar]
  22. McGrew L. L., Richter J. D. Translational control by cytoplasmic polyadenylation during Xenopus oocyte maturation: characterization of cis and trans elements and regulation by cyclin/MPF. EMBO J. 1990 Nov;9(11):3743–3751. doi: 10.1002/j.1460-2075.1990.tb07587.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982 Oct;30(3):675–686. doi: 10.1016/0092-8674(82)90272-0. [DOI] [PubMed] [Google Scholar]
  24. Osborne H. B., Duval C., Ghoda L., Omilli F., Bassez T., Coffino P. Expression and post-transcriptional regulation of ornithine decarboxylase during early Xenopus development. Eur J Biochem. 1991 Dec 5;202(2):575–581. doi: 10.1111/j.1432-1033.1991.tb16410.x. [DOI] [PubMed] [Google Scholar]
  25. Richards W. G., Carroll P. M., Kinloch R. A., Wassarman P. M., Strickland S. Creating maternal effect mutations in transgenic mice: antisense inhibition of an oocyte gene product. Dev Biol. 1993 Dec;160(2):543–553. doi: 10.1006/dbio.1993.1328. [DOI] [PubMed] [Google Scholar]
  26. Sallés F. J., Darrow A. L., O'Connell M. L., Strickland S. Isolation of novel murine maternal mRNAs regulated by cytoplasmic polyadenylation. Genes Dev. 1992 Jul;6(7):1202–1212. doi: 10.1101/gad.6.7.1202. [DOI] [PubMed] [Google Scholar]
  27. Sallés F. J., Lieberfarb M. E., Wreden C., Gergen J. P., Strickland S. Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. Science. 1994 Dec 23;266(5193):1996–1999. doi: 10.1126/science.7801127. [DOI] [PubMed] [Google Scholar]
  28. Sallés F. J., Richards W. G., Huarte J., Vassalli J. D., Strickland S. Microinjecting antisense sequences into oocytes. Methods Enzymol. 1993;225:351–361. doi: 10.1016/0076-6879(93)25024-v. [DOI] [PubMed] [Google Scholar]
  29. Sanger F., Coulson A. R. The use of thin acrylamide gels for DNA sequencing. FEBS Lett. 1978 Mar 1;87(1):107–110. doi: 10.1016/0014-5793(78)80145-8. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Simon R., Richter J. D. Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryonic cytoplasmic polyadenylation element-binding proteins. Mol Cell Biol. 1994 Dec;14(12):7867–7875. doi: 10.1128/mcb.14.12.7867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Strickland S., Huarte J., Belin D., Vassalli A., Rickles R. J., Vassalli J. D. Antisense RNA directed against the 3' noncoding region prevents dormant mRNA activation in mouse oocytes. Science. 1988 Aug 5;241(4866):680–684. doi: 10.1126/science.2456615. [DOI] [PubMed] [Google Scholar]
  35. Varnum S. M., Wormington W. M. Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. Genes Dev. 1990 Dec;4(12B):2278–2286. doi: 10.1101/gad.4.12b.2278. [DOI] [PubMed] [Google Scholar]
  36. Vassalli J. D., Huarte J., Belin D., Gubler P., Vassalli A., O'Connell M. L., Parton L. A., Rickles R. J., Strickland S. Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev. 1989 Dec;3(12B):2163–2171. doi: 10.1101/gad.3.12b.2163. [DOI] [PubMed] [Google Scholar]
  37. Vize P. D., Melton D. A., Hemmati-Brivanlou A., Harland R. M. Assays for gene function in developing Xenopus embryos. Methods Cell Biol. 1991;36:367–387. doi: 10.1016/s0091-679x(08)60288-5. [DOI] [PubMed] [Google Scholar]
  38. Wharton R. P., Struhl G. Structure of the Drosophila BicaudalD protein and its role in localizing the the posterior determinant nanos. Cell. 1989 Dec 1;59(5):881–892. doi: 10.1016/0092-8674(89)90611-9. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES