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 Latorre, P.
Right arrow Articles by Curran, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Latorre, P.
Right arrow Articles by Curran, J.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, September 1998, p. 5021-5031, Vol. 18, No. 9
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Sendai Virus Y Proteins Are Initiated by a Ribosomal Shunt

Patrizia Latorre, Daniel Kolakofsky, and Joseph Curran*

Department of Genetics and Microbiology, University of Geneva Medical School (CMU), CH1211 Geneva, Switzerland

Received 9 February 1998/Returned for modification 24 March 1998/Accepted 25 May 1998

The Sendai virus P/C mRNA expresses eight primary translation products by using a combination of ribosomal choice and cotranscriptional mRNA editing. The longest open reading frame (ORF) of the mRNA starts at AUG104 (the second initiation site) and encodes the 568-amino-acid P protein, an essential subunit of the viral polymerase. The first (ACG81), third (ATG114), fourth (ATG183), and fifth (ATG201) initiation sites are used to express a C-terminal nested set of polypeptides (collectively named the C proteins) in the +1 ORF relative to P, namely, C', C, Y1, and Y2, respectively. Leaky scanning accounts for translational initiation at the first three start sites (a non-ATG followed by ATGs in progressively stronger contexts). Consistent with this, changing ACG81/C' to ATG (GCCATG81G) abrogates expression from the downstream ATG104/P and ATG114/C initiation codons. However, expression of the Y1 and Y2 proteins remains normal in this background. We now have evidence that initiation from ATG183/Y1 and ATG201/Y2 takes place via a ribosomal shunt or discontinuous scanning. Scanning complexes appear to assemble at the 5' cap and then scan ca. 50 nucleotides (nt) of the 5' untranslated region before being translocated to an acceptor site at or close to the Y initiation codons. No specific donor site sequences are required, and translation of the Y proteins continues even when their start codons are changed to ACG. Curiously, ATG codons (in good contexts) in the P ORF, placed either 16 nt upstream of Y1, 29 nt downstream of Y2, or between the Y1 and Y2 codons, are not expressed even in the ACGY1/ACGY2 background. This indicates that ATG183/Y1 and ATG201/Y2 are privileged start sites within the acceptor site. Our observations suggest that the shunt delivers the scanning complex directly to the Y start codons.


* Corresponding author. Mailing address: Department of Genetics and Microbiology, University of Geneva Medical School (CMU), 9 Ave. Champel, CH1211 Geneva, Switzerland. Phone: 41-22-702-57.27. Fax: 41-22-346-72.37. E-mail: curran{at}cmu.unige.ch.


Molecular and Cellular Biology, September 1998, p. 5021-5031, Vol. 18, No. 9
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Luttermann, C., Meyers, G. (2009). The importance of inter- and intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA. Genes Dev. 23: 331-344 [Abstract] [Full Text]  
  • Racine, T., Barry, C., Roy, K., Dawe, S. J., Shmulevitz, M., Duncan, R. (2007). Leaky Scanning and Scanning-independent Ribosome Migration on the Tricistronic S1 mRNA of Avian Reovirus. J. Biol. Chem. 282: 25613-25622 [Abstract] [Full Text]  
  • Gould, P. S., Easton, A. J. (2007). Coupled Translation of the Second Open Reading Frame of M2 mRNA Is Sequence Dependent and Differs Significantly within the Subfamily Pneumovirinae. J. Virol. 81: 8488-8496 [Abstract] [Full Text]  
  • Marq, J.-B., Brini, A., Kolakofsky, D., Garcin, D. (2007). Targeting of the Sendai Virus C Protein to the Plasma Membrane via a Peptide-Only Membrane Anchor. J. Virol. 81: 3187-3197 [Abstract] [Full Text]  
  • Luttermann, C., Meyers, G. (2007). A Bipartite Sequence Motif Induces Translation Reinitiation in Feline Calicivirus RNA. J. Biol. Chem. 282: 7056-7065 [Abstract] [Full Text]  
  • Pooggin, M. M., Ryabova, L. A., He, X., Futterer, J., Hohn, T. (2006). Mechanism of ribosome shunting in Rice tungro bacilliform pararetrovirus. RNA 12: 841-850 [Abstract] [Full Text]  
  • Edgil, D., Polacek, C., Harris, E. (2006). Dengue Virus Utilizes a Novel Strategy for Translation Initiation When Cap-Dependent Translation Is Inhibited. J. Virol. 80: 2976-2986 [Abstract] [Full Text]  
  • Gould, P. S., Easton, A. J. (2005). Coupled Translation of the Respiratory Syncytial Virus M2 Open Reading Frames Requires Upstream Sequences. J. Biol. Chem. 280: 21972-21980 [Abstract] [Full Text]  
  • Sen, N., Cao, F., Tavis, J. E. (2004). Translation of Duck Hepatitis B Virus Reverse Transcriptase by Ribosomal Shunting. J. Virol. 78: 11751-11757 [Abstract] [Full Text]  
  • Garcin, D., Marq, J.-B., Iseni, F., Martin, S., Kolakofsky, D. (2004). A Short Peptide at the Amino Terminus of the Sendai Virus C Protein Acts as an Independent Element That Induces STAT1 Instability. J. Virol. 78: 8799-8811 [Abstract] [Full Text]  
  • Xi, Q., Cuesta, R., Schneider, R. J. (2004). Tethering of eIF4G to adenoviral mRNAs by viral 100k protein drives ribosome shunting. Genes Dev. 18: 1997-2009 [Abstract] [Full Text]  
  • de Breyne, S., Monney, R. S., Curran, J. (2004). Proteolytic Processing and Translation Initiation: TWO INDEPENDENT MECHANISMS FOR THE EXPRESSION OF THE SENDAI VIRUS Y PROTEINS. J. Biol. Chem. 279: 16571-16580 [Abstract] [Full Text]  
  • Vassilaki, N., Mavromara, P. (2003). Two Alternative Translation Mechanisms Are Responsible for the Expression of the HCV ARFP/F/Core+1 Coding Open Reading Frame. J. Biol. Chem. 278: 40503-40513 [Abstract] [Full Text]  
  • Meyers, G. (2003). Translation of the Minor Capsid Protein of a Calicivirus Is Initiated by a Novel Termination-dependent Reinitiation Mechanism. J. Biol. Chem. 278: 34051-34060 [Abstract] [Full Text]  
  • Garcin, D., Marq, J.-B., Goodbourn, S., Kolakofsky, D. (2003). The Amino-Terminal Extensions of the Longer Sendai Virus C Proteins Modulate pY701-Stat1 and Bulk Stat1 Levels Independently of Interferon Signaling. J. Virol. 77: 2321-2329 [Abstract] [Full Text]  
  • de Breyne, S., Simonet, V., Pelet, T., Curran, J. (2003). Identification of a cis-acting element required for shunt-mediated translational initiation of the Sendai virus Y proteins. Nucleic Acids Res 31: 608-618 [Abstract] [Full Text]  
  • Neumann, G., Whitt, M. A., Kawaoka, Y. (2002). A decade after the generation of a negative-sense RNA virus from cloned cDNA - what have we learned?. J. Gen. Virol. 83: 2635-2662 [Abstract] [Full Text]  
  • Shmulevitz, M., Yameen, Z., Dawe, S., Shou, J., O'Hara, D., Holmes, I., Duncan, R. (2002). Sequential Partially Overlapping Gene Arrangement in the Tricistronic S1 Genome Segments of Avian Reovirus and Nelson Bay Reovirus: Implications for Translation Initiation. J. Virol. 76: 609-618 [Abstract] [Full Text]  
  • Garcin, D., Curran, J., Itoh, M., Kolakofsky, D. (2001). Longer and Shorter Forms of Sendai Virus C Proteins Play Different Roles in Modulating the Cellular Antiviral Response. J. Virol. 75: 6800-6807 [Abstract] [Full Text]  
  • Pooggin, M. M., Futterer, J., Skryabin, K. G., Hohn, T. (2001). Ribosome shunt is essential for infectivity of cauliflower mosaic virus. Proc. Natl. Acad. Sci. USA 98: 886-891 [Abstract] [Full Text]  
  • CUESTA, R., XI, Q., SCHNEIDER, R.J. (2001). Preferential Translation of Adenovirus mRNAs in Infected Cells. Cold Spring Harb Symp Quant Biol 66: 259-268 [Abstract]  
  • HOHN, T., PARK, H.-S., GUERRA-PERAZA, O., STAVOLONE, L., POOGGIN, M.M., KOBAYASHI, K., RYABOVA, L.A. (2001). Shunting and Controlled Reinitiation: The Encounter of Cauliflower Mosaic Virus with the Translational Machinery. Cold Spring Harb Symp Quant Biol 66: 269-276 [Abstract]  
  • Garcin, D., Curran, J., Kolakofsky, D. (2000). Sendai Virus C Proteins Must Interact Directly with Cellular Components To Interfere with Interferon Action. J. Virol. 74: 8823-8830 [Abstract] [Full Text]  
  • Hemmings-Mieszczak, M., Hohn, T., Preiss, T. (2000). Termination and Peptide Release at the Upstream Open Reading Frame Are Required for Downstream Translation on Synthetic Shunt-Competent mRNA Leaders. Mol. Cell. Biol. 20: 6212-6223 [Abstract] [Full Text]  
  • Stacey, S. N., Jordan, D., Williamson, A. J. K., Brown, M., Coote, J. H., Arrand, J. R. (2000). Leaky Scanning Is the Predominant Mechanism for Translation of Human Papillomavirus Type 16 E7 Oncoprotein from E6/E7 Bicistronic mRNA. J. Virol. 74: 7284-7297 [Abstract] [Full Text]  
  • Ryabova, L. A., Hohn, T. (2000). Ribosome shunting in the cauliflower mosaic virus 35S RNA leader is a special case of reinitiation of translation functioning in plant and animal systems. Genes Dev. 14: 817-829 [Abstract] [Full Text]  
  • Yueh, A., Schneider, R. J. (2000). Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes Dev. 14: 414-421 [Abstract] [Full Text]  
  • Bermingham, A., Collins, P. L. (1999). The M2-2 protein of human respiratory syncytial virus is a regulatory factor involved in the balance between RNA replication and transcription. Proc. Natl. Acad. Sci. USA 96: 11259-11264 [Abstract] [Full Text]  
  • Garcin, D., Latorre, P., Kolakofsky, D. (1999). Sendai Virus C Proteins Counteract the Interferon-Mediated Induction of an Antiviral State. J. Virol. 73: 6559-6565 [Abstract] [Full Text]  
  • Pooggin, M. M., Hohn, T., Futterer, J. (2000). Role of a Short Open Reading Frame in Ribosome Shunt on the Cauliflower Mosaic Virus RNA Leader. J. Biol. Chem. 275: 17288-17296 [Abstract] [Full Text]  
  • Ryabova, L. A., Pooggin, M. M., Dominguez, D. I., Hohn, T. (2000). Continuous and Discontinuous Ribosome Scanning on the Cauliflower Mosaic Virus 35 S RNA Leader Is Controlled by Short Open Reading Frames. J. Biol. Chem. 275: 37278-37284 [Abstract] [Full Text]