This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Noueiry, A. O. Articles by Ahlquist, P. Search for Related Content PubMed PubMed Citation Articles by Noueiry, A. O. Articles by Ahlquist, P.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, June 2003, p. 4094-4106, Vol. 23, No. 12
0270-7306/03/$08.00+0     DOI: 10.1128/MCB.23.12.4094-4106.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Yeast Lsm1p-7p/Pat1p Deadenylation-Dependent mRNA-Decapping Factors Are Required for Brome Mosaic Virus Genomic RNA Translation

Institute for Molecular Virology,¹ Howard Hughes Medical Institute, University of Wisconsin-Madison, Madison, Wisconsin 53706,³ Microbiology Unit, Universidad Pompeu Fabra, E-08003 Barcelona, Spain²

Received 17 September 2002/ Returned for modification 6 November 2002/ Accepted 20 March 2003

Previously, we used the ability of the higher eukaryotic positive-strand RNA virus brome mosaic virus (BMV) to replicate in yeast to show that the yeast LSM1 gene is required for recruiting BMV RNA from translation to replication. Here we extend this observation to show that Lsm1p and other components of the Lsm1p-Lsm7p/Pat1p deadenylation-dependent mRNA decapping complex were also required for translating BMV RNAs. Inhibition of BMV RNA translation was selective, with no effect on general cellular translation. We show that viral genomic RNAs suitable for RNA replication were already distinguished from nonreplication templates at translation, well before RNA recruitment to replication. Among mRNA turnover pathways, only factors specific for deadenylated mRNA decapping were required for BMV RNA translation. Dependence on these factors was not only a consequence of the nonpolyadenylated nature of BMV RNAs but also involved the combined effects of the viral 5' and 3' noncoding regions and 2a polymerase open reading frame. High-resolution sucrose density gradient analysis showed that, while mutating factors in the Lsm1p-7p/Pat1p complex completely inhibited viral RNA translation, the levels of viral RNA associated with ribosomes were only slightly reduced in mutant yeast. This polysome association was further verified by using a conditional allele of essential translation initiation factor PRT1, which markedly decreased polysome association of viral genomic RNA in the presence or absence of an LSM7 mutation. Together, these results show that a defective Lsm1p-7p/Pat1p complex inhibits BMV RNA translation primarily by stalling or slowing the elongation of ribosomes along the viral open reading frame. Thus, factors in the Lsm1p-7p/Pat1p complex function not only in mRNA decapping but also in translation, and both translation and recruitment of BMV RNAs to viral RNA replication are regulated by a cell pathway that transfers mRNAs from translation to degradation.

This article has been cited by other articles:

• Beckham, C., Hilliker, A., Cziko, A.-M., Noueiry, A., Ramaswami, M., Parker, R. (2008). The DEAD-Box RNA Helicase Ded1p Affects and Accumulates in Saccharomyces cerevisiae P-Bodies. Mol. Biol. Cell 19: 984-993 [Abstract] [Full Text]  
• Beckham, C. J., Light, H. R., Amar Nissan, T., Ahlquist, P., Parker, R., Noueiry, A. (2007). Interactions between Brome Mosaic Virus RNAs and Cytoplasmic Processing Bodies. J. Virol. 81: 9759-9768 [Abstract] [Full Text]  
• Alves-Rodrigues, I., Mas, A., Diez, J. (2007). Xenopus Xp54 and Human RCK/p54 Helicases Functionally Replace Yeast Dhh1p in Brome Mosaic Virus RNA Replication. J. Virol. 81: 4378-4380 [Abstract] [Full Text]  
• Yi, G., Gopinath, K., Kao, C. C. (2007). Selective Repression of Translation by the Brome Mosaic Virus 1a RNA Replication Protein. J. Virol. 81: 1601-1609 [Abstract] [Full Text]  
• Wierzchoslawski, R., Urbanowicz, A., Dzianott, A., Figlerowicz, M., Bujarski, J. J. (2006). Characterization of a Novel 5' Subgenomic RNA3a Derived from RNA3 of Brome Mosaic Bromovirus. J. Virol. 80: 12357-12366 [Abstract] [Full Text]  
• Mas, A., Alves-Rodrigues, I., Noueiry, A., Ahlquist, P., Diez, J. (2006). Host Deadenylation-Dependent mRNA Decapping Factors Are Required for a Key Step in Brome Mosaic Virus RNA Replication. J. Virol. 80: 246-251 [Abstract] [Full Text]  
• Wang, X., Lee, W.-M., Watanabe, T., Schwartz, M., Janda, M., Ahlquist, P. (2005). Brome Mosaic Virus 1a Nucleoside Triphosphatase/Helicase Domain Plays Crucial Roles in Recruiting RNA Replication Templates. J. Virol. 79: 13747-13758 [Abstract] [Full Text]  
• Thivierge, K., Nicaise, V., Dufresne, P. J., Cotton, S., Laliberte, J.-F., Le Gall, O., Fortin, M. G. (2005). Plant Virus RNAs. Coordinated Recruitment of Conserved Host Functions by (+) ssRNA Viruses during Early Infection Events. Plant Physiol. 138: 1822-1827 [Abstract] [Full Text]  
• Grdzelishvili, V. Z., Garcia-Ruiz, H., Watanabe, T., Ahlquist, P. (2005). Mutual Interference between Genomic RNA Replication and Subgenomic mRNA Transcription in Brome Mosaic Virus. J. Virol. 79: 1438-1451 [Abstract] [Full Text]  
• Barends, S., Rudinger-Thirion, J., Florentz, C., Giege, R., Pleij, C. W. A., Kraal, B. (2004). tRNA-Like Structure Regulates Translation of Brome Mosaic Virus RNA. J. Virol. 78: 4003-4010 [Abstract] [Full Text]  
• Chong, J.-L., Chuang, R.-Y., Tung, L., Chang, T.-H. (2004). Ded1p, a conserved DExD/H-box translation factor, can promote yeast L-A virus negative-strand RNA synthesis in vitro. Nucleic Acids Res 32: 2031-2038 [Abstract] [Full Text]  
• Kushner, D. B., Lindenbach, B. D., Grdzelishvili, V. Z., Noueiry, A. O., Paul, S. M., Ahlquist, P. (2003). Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc. Natl. Acad. Sci. USA 100: 15764-15769 [Abstract] [Full Text]