This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Gillian-Daniel, D. L.
Right arrow Articles by Wickens, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Gillian-Daniel, D. L.
Right arrow Articles by Wickens, M.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, October 1998, p. 6152-6163, Vol. 18, No. 10
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Modifications of the 5' Cap of mRNAs during Xenopus Oocyte Maturation: Independence from Changes in Poly(A) Length and Impact on Translation

Donald L. Gillian-Daniel, Nicola K. Gray, Jonas Åström,dagger Aaron Barkoff, and Marvin Wickens*

Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706

Received 28 May 1998/Returned for modification 30 June 1998/Accepted 17 July 1998

The translation of specific maternal mRNAs is regulated during early development. For some mRNAs, an increase in translational activity is correlated with cytoplasmic extension of their poly(A) tails; for others, translational inactivation is correlated with removal of their poly(A) tails. Recent results in several systems suggest that events at the 3' end of the mRNA can affect the state of the 5' cap structure, m7G(5')ppp(5')G. We focus here on the potential role of cap modifications on translation during early development and on the question of whether any such modifications are dependent on cytoplasmic poly(A) addition or removal. To do so, we injected synthetic RNAs into Xenopus oocytes and examined their cap structures and translational activities during meiotic maturation. We draw four main conclusions. First, the activity of a cytoplasmic guanine-7-methyltransferase increases during oocyte maturation and stimulates translation of an injected mRNA bearing a nonmethylated GpppG cap. The importance of the cap for translation in oocytes is corroborated by the sensitivity of protein synthesis to cap analogs and by the inefficient translation of mRNAs bearing nonphysiologically capped 5' termini. Second, deadenylation during oocyte maturation does not cause decapping, in contrast to deadenylation-triggered decapping in Saccharomyces cerevisiae. Third, the poly(A) tail and the N-7 methyl group of the cap stimulate translation synergistically during oocyte maturation. Fourth, cap ribose methylation of certain mRNAs is very inefficient and is not required for their translational recruitment by poly(A). These results demonstrate that polyadenylation can cause translational recruitment independent of ribose methylation. We propose that polyadenylation enhances translation through at least two mechanisms that are distinguished by their dependence on ribose modification.

* Corresponding author. Mailing address: Department of Biochemistry, 433 Babcock Dr., University of Wisconsin, Madison, WI 53706. Phone: (608) 262-8007. Fax: (608) 262-9108. E-mail: wickens{at}biochem.wisc.edu.

dagger Present address: Amersham Pharmacia Biotech, SE-751 84, Uppsala, Sweden.

Molecular and Cellular Biology, October 1998, p. 6152-6163, Vol. 18, No. 10
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Minshall, N., Kress, M., Weil, D., Standart, N. (2009). Role of p54 RNA Helicase Activity and Its C-terminal Domain in Translational Repression, P-body Localization and Assembly. Mol. Biol. Cell 20: 2464-2472 [Abstract] [Full Text]  
  • Li, Y., Guarino, L. A. (2008). Roles of LEF-4 and PTP/BVP RNA Triphosphatases in Processing of Baculovirus Late mRNAs. J. Virol. 82: 5573-5583 [Abstract] [Full Text]  
  • Zamudio, J. R., Mittra, B., Foldynova-Trantirkova, S., Zeiner, G. M., Lukes, J., Bujnicki, J. M., Sturm, N. R., Campbell, D. A. (2007). The 2'-O-Ribose Methyltransferase for Cap 1 of Spliced Leader RNA and U1 Small Nuclear RNA in Trypanosoma brucei. Mol. Cell. Biol. 27: 6084-6092 [Abstract] [Full Text]  
  • Wilkie, G. S., Gautier, P., Lawson, D., Gray, N. K. (2005). Embryonic Poly(A)-Binding Protein Stimulates Translation in Germ Cells. Mol. Cell. Biol. 25: 2060-2071 [Abstract] [Full Text]  
  • Dickson, K. S., Thompson, S. R., Gray, N. K., Wickens, M. (2001). Poly(A) Polymerase and the Regulation of Cytoplasmic Polyadenylation. J. Biol. Chem. 276: 41810-41816 [Abstract] [Full Text]  
  • Palancade, B., Bellier, S., Almouzni, G., Bensaude, O. (2001). Incomplete RNA polymerase II phosphorylation in Xenopus laevis early embryos. J. Cell Sci. 114: 2483-2489 [Abstract] [Full Text]  
  • Gillian, A. L., Schmechel, S. C., Livny, J., Schiff, L. A., Nibert, M. L. (2000). Reovirus Protein sigma NS Binds in Multiple Copies to Single-Stranded RNA and Shares Properties with Single-Stranded DNA Binding Proteins. J. Virol. 74: 5939-5948 [Abstract] [Full Text]  
  • Burkard, K. T. D., Butler, J. S. (2000). A Nuclear 3'-5' Exonuclease Involved in mRNA Degradation Interacts with Poly(A) Polymerase and the hnRNA Protein Npl3p. Mol. Cell. Biol. 20: 604-616 [Abstract] [Full Text]  
  • Yamada-Okabe, T., Mio, T., Kashima, Y., Matsui, M., Arisawa, M., Yamada-Okabe, H. (1999). The Candida albicans gene for mRNA 5'-cap methyltransferase: identification of additional residues essential for catalysis. Microbiology 145: 3023-3033 [Abstract] [Full Text]  
  • Richter, J. D. (1999). Cytoplasmic Polyadenylation in Development and Beyond. Microbiol. Mol. Biol. Rev. 63: 446-456 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»