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 Tapparel, C.
Right arrow Articles by Roux, L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Tapparel, C.
Right arrow Articles by Roux, L.

 Previous Article  |  Next Article 

J Virol, April 1998, p. 3117-3128, Vol. 72, No. 4
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

The Activity of Sendai Virus Genomic and Antigenomic Promoters Requires a Second Element Past the Leader Template Regions: a Motif (GNNNNN)3 Is Essential for Replication

Caroline Tapparel, Diane Maurice, and Laurent Roux*

Department of Genetics and Microbiology, University of Geneva Medical School, Centre Medical Universitaire, 1211 Geneva 4, Switzerland

Received 10 November 1997/Accepted 23 December 1997

The paramyxovirus genome, a nonsegmented, negative-polarity, single-stranded RNA of ~15 kb, contains six transcription units flanked at the 3' and 5' ends by a short (~ 50- to 60-nucleotide) extracistronic sequence, dubbed the positive and negative leader regions. These leader template regions, present at the 3' end of the genome and the antigenome, have been shown to contain essential signals governing RNA replication activity. Whether they are sufficient to promote replication is still open to question. By using a series of Sendai virus defective interfering RNAs carrying a nested set of deletions in the promoter regions, it is shown here that for both the genomic and antigenomic promoters, a 3'-end RNA sequence of 96 nucleotides is required to allow replication. Sequence comparison of active and inactive promoters led to the identification of a set of three nucleotide hexamers (nucleotides 79 to 84, 85 to 90, and 91 to 96) containing a repeated motif RXXYXX [shown as 5'-3' positive-strand]. Sequential mutation of each hexamer into its complementary sequence confirmed their essential role. The three hexamers are required, and their relative positioning is important, since displacing them by 6 nucleotides destroyed promoter function. RNAs carrying degenerate nucleotides in the three hexamers were used as replication templates. They led to the selection of actively replicating RNA species exclusively carrying the basic motif (GNNNNN)3 from nucleotides 79 to 96. These results clearly show that, apart from the region from nucleotides 1 to 31, previously identified as governing Sendai virus replication activity, a second element, spanning at the most nucleotides 79 to 96, appears essential. Thus, the paramyxovirus replication promoters are not confined to the leader template regions, as seems to be the case for the rhabdoviruses.


* Corresponding author. Mailing address: Department of Genetics and Microbiology, University of Geneva Medical School, CMU, 9 ave. de Champel, 1211 Geneva 4, Switzerland. Phone: 41-22-702-56-83. Fax: 41-22-702-57-02. E-mail: Laurent.Roux{at}medecine.unige.ch.




This article has been cited by other articles:

  • Manuse, M. J., Parks, G. D. (2009). Role for the Paramyxovirus Genomic Promoter in Limiting Host Cell Antiviral Responses and Cell Killing. J. Virol. 83: 9057-9067 [Abstract] [Full Text]  
  • Enterlein, S., Schmidt, K. M., Schumann, M., Conrad, D., Krahling, V., Olejnik, J., Muhlberger, E. (2009). The Marburg Virus 3' Noncoding Region Structurally and Functionally Differs from That of Ebola Virus. J. Virol. 83: 4508-4519 [Abstract] [Full Text]  
  • Rennick, L. J., Duprex, W. P., Rima, B. K. (2007). Measles virus minigenomes encoding two autofluorescent proteins reveal cell-to-cell variation in reporter expression dependent on viral sequences between the transcription units. J. Gen. Virol. 88: 2710-2718 [Abstract] [Full Text]  
  • Walpita, P., Peters, C. J. (2007). Cis-acting elements in the antigenomic promoter of Nipah virus. J. Gen. Virol. 88: 2542-2551 [Abstract] [Full Text]  
  • Cordey, S., Roux, L. (2007). Further characterization of a paramyxovirus transcription initiation signal: search for required nucleotides upstream and importance of the N phase context. J. Gen. Virol. 88: 1555-1564 [Abstract] [Full Text]  
  • Cowton, V. M., McGivern, D. R., Fearns, R. (2006). Unravelling the complexities of respiratory syncytial virus RNA synthesis. J. Gen. Virol. 87: 1805-1821 [Abstract] [Full Text]  
  • Hoffman, M. A., Thorson, L. M., Vickman, J. E., Anderson, J. S., May, N. A., Schweitzer, M. N. (2006). Roles of human parainfluenza virus type 3 bases 13 to 78 in replication and transcription: identification of an additional replication promoter element and evidence for internal transcription initiation.. J. Virol. 80: 5388-5396 [Abstract] [Full Text]  
  • Cordey, S., Roux, L. (2006). Transcribing paramyxovirus RNA polymerase engages the template at its 3' extremity.. J. Gen. Virol. 87: 665-672 [Abstract] [Full Text]  
  • Cowton, V. M., Fearns, R. (2005). Evidence that the Respiratory Syncytial Virus Polymerase Is Recruited to Nucleotides 1 to 11 at the 3' End of the Nucleocapsid and Can Scan To Access Internal Signals. J. Virol. 79: 11311-11322 [Abstract] [Full Text]  
  • Weik, M., Enterlein, S., Schlenz, K., Muhlberger, E. (2005). The Ebola Virus Genomic Replication Promoter Is Bipartite and Follows the Rule of Six. J. Virol. 79: 10660-10671 [Abstract] [Full Text]  
  • Kolakofsky, D., Roux, L., Garcin, D., Ruigrok, R. W. H. (2005). Paramyxovirus mRNA editing, the 'rule of six' and error catastrophe: a hypothesis. J. Gen. Virol. 86: 1869-1877 [Abstract] [Full Text]  
  • Banyard, A. C., Baron, M. D., Barrett, T. (2005). A role for virus promoters in determining the pathogenesis of Rinderpest virus in cattle. J. Gen. Virol. 86: 1083-1092 [Abstract] [Full Text]  
  • McGivern, D. R., Collins, P. L., Fearns, R. (2005). Identification of Internal Sequences in the 3' Leader Region of Human Respiratory Syncytial Virus That Enhance Transcription and Confer Replication Processivity. J. Virol. 79: 2449-2460 [Abstract] [Full Text]  
  • Vulliemoz, D., Cordey, S., Mottet-Osman, G., Roux, L. (2005). Nature of a paramyxovirus replication promoter influences a nearby transcription signal. J. Gen. Virol. 86: 171-180 [Abstract] [Full Text]  
  • Le Mercier, P., Garcin, D., Garcia, E., Kolakofsky, D. (2003). Competition between the Sendai Virus N mRNA Start Site and the Genome 3'-End Promoter for Viral RNA Polymerase. J. Virol. 77: 9147-9155 [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]  
  • Bhella, D., Ralph, A., Murphy, L. B., Yeo, R. P. (2002). Significant differences in nucleocapsid morphology within the Paramyxoviridae. J. Gen. Virol. 83: 1831-1839 [Abstract] [Full Text]  
  • Vulliemoz, D., Roux, L. (2002). Given the Opportunity, the Sendai Virus RNA-Dependent RNA Polymerase Could as Well Enter Its Template Internally. J. Virol. 76: 7987-7995 [Abstract] [Full Text]  
  • Le Mercier, P., Garcin, D., Hausmann, S., Kolakofsky, D. (2002). Ambisense Sendai Viruses Are Inherently Unstable but Are Useful To Study Viral RNA Synthesis. J. Virol. 76: 5492-5502 [Abstract] [Full Text]  
  • Schmidt, A. C., Wenzke, D. R., McAuliffe, J. M., St. Claire, M., Elkins, W. R., Murphy, B. R., Collins, P. L. (2002). Mucosal Immunization of Rhesus Monkeys against Respiratory Syncytial Virus Subgroups A and B and Human Parainfluenza Virus Type 3 by Using a Live cDNA-Derived Vaccine Based on a Host Range-Attenuated Bovine Parainfluenza Virus Type 3 Vector Backbone. J. Virol. 76: 1089-1099 [Abstract] [Full Text]  
  • Mioulet, V., Barrett, T., Baron, M. D. (2001). Scanning mutagenesis identifies critical residues in the rinderpest virus genome promoter. J. Gen. Virol. 82: 2905-2911 [Abstract] [Full Text]  
  • Vulliémoz, D., Roux, L. (2001). "Rule of Six": How Does the Sendai Virus RNA Polymerase Keep Count?. J. Virol. 75: 4506-4518 [Abstract] [Full Text]  
  • Schmidt, A. C., McAuliffe, J. M., Murphy, B. R., Collins, P. L. (2001). Recombinant Bovine/Human Parainfluenza Virus Type 3 (B/HPIV3) Expressing the Respiratory Syncytial Virus (RSV) G and F Proteins Can Be Used To Achieve Simultaneous Mucosal Immunization against RSV and HPIV3. J. Virol. 75: 4594-4603 [Abstract] [Full Text]  
  • Coronel, E. C., Takimoto, T., Murti, K. G., Varich, N., Portner, A. (2001). Nucleocapsid Incorporation into Parainfluenza Virus Is Regulated by Specific Interaction with Matrix Protein. J. Virol. 75: 1117-1123 [Abstract] [Full Text]  
  • Parks, C. L., Lerch, R. A., Walpita, P., Wang, H.-P., Sidhu, M. S., Udem, S. A. (2001). Analysis of the Noncoding Regions of Measles Virus Strains in the Edmonston Vaccine Lineage. J. Virol. 75: 921-933 [Abstract] [Full Text]  
  • Fearns, R., Collins, P. L., Peeples, M. E. (2000). Functional Analysis of the Genomic and Antigenomic Promoters of Human Respiratory Syncytial Virus. J. Virol. 74: 6006-6014 [Abstract] [Full Text]  
  • Choudhary, S., De, B. P., Banerjee, A. K. (2000). Specific Phosphorylated Forms of Glyceraldehyde 3-Phosphate Dehydrogenase Associate with Human Parainfluenza Virus Type 3 and Inhibit Viral Transcription In Vitro. J. Virol. 74: 3634-3641 [Abstract] [Full Text]  
  • Stillman, E. A., Whitt, M. A. (1999). Transcript Initiation and 5'-End Modifications Are Separable Events during Vesicular Stomatitis Virus Transcription. J. Virol. 73: 7199-7209 [Abstract] [Full Text]  
  • Finke, S., Conzelmann, K.-K. (1999). Virus Promoters Determine Interference by Defective RNAs: Selective Amplification of Mini-RNA Vectors and Rescue from cDNA by a 3' Copy-Back Ambisense Rabies Virus. J. Virol. 73: 3818-3825 [Abstract] [Full Text]  
  • Whelan, S. P. J., Wertz, G. W. (1999). Regulation of RNA Synthesis by the Genomic Termini of Vesicular Stomatitis Virus: Identification of Distinct Sequences Essential for Transcription but Not Replication. J. Virol. 73: 297-306 [Abstract] [Full Text]  
  • Murphy, S. K., Parks, G. D. (1999). RNA Replication for the Paramyxovirus Simian Virus 5 Requires an Internal Repeated (CGNNNN) Sequence Motif. J. Virol. 73: 805-809 [Abstract] [Full Text]