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 Whelan, S. P. J.
Right arrow Articles by Wertz, G. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Whelan, S. P. J.
Right arrow Articles by Wertz, G. W.

 Previous Article  |  Next Article 

Journal of Virology, January 1999, p. 297-306, Vol. 73, No. 1
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Regulation of RNA Synthesis by the Genomic Termini of Vesicular Stomatitis Virus: Identification of Distinct Sequences Essential for Transcription but Not Replication

Sean P. J. Whelan and Gail W. Wertz*

Department of Microbiology, The Medical School, University of Alabama at Birmingham, Birmingham, Alabama

Received 6 August 1998/Accepted 5 October 1998

The RNA-dependent RNA polymerase of vesicular stomatitis virus (VSV), a nonsegmented negative-strand RNA virus, directs two discrete RNA synthetic processes, transcription and replication. Available evidence suggests that the two short extragenic regions at the genomic termini, the 3' leader (Le) and the complement of the 5' trailer (TrC), contain essential signals for these processes. We examined the roles in transcription and replication of sequences in Le and TrC by monitoring the effects of alterations to the termini of subgenomic replicons, or infectious viruses, on these RNA synthetic processes. Distinct elements in Le were found to be required for transcription that were not required for replication. The promoter for mRNA transcription was shown to include specific sequence elements within Le at positions 19 to 29 and 34 to 46, a separate element at nucleotides 47 to 50, the nontranscribed leader-N gene junction. The sequence requirements for transcription within the Le region could not be supplied by sequences found at the equivalent positions in TrC. In contrast, sequences from either Le or TrC functioned well to signal replication, indicating that within the confines of the VSV termini, the sequence requirements for replication were less stringent. Deletions engineered at the termini showed that the terminal 15 nucleotides of either Le or TrC allowed a minimal level of replication. Within these confines, levels of replication were affected by both the extent of complementarity between the genomic termini and the involvement of the template in transcription. In agreement with our previous observations, increasing the extent of complementarity between the natural termini increased levels of replication, and this effect was most operative at the extreme genome ends. In addition, abolishing the use of Le as a promoter for transcription enhanced replication. These analyses (i) identified signals at the termini required for transcription and replication and (ii) showed that Le functions as a less efficient promoter for replication than TrC at least in part because of its essential role in transcription. Consequently, these observations help explain the asymmetry of VSV replication which results in the synthesis of more negative- than positive-sense replication products in infected cells.

* Corresponding author. Mailing address: Department of Microbiology, The Medical School, University of Alabama at Birmingham, BBRB17 Room 366, 845 19th St. South, Birmingham, AL 35294. Phone: (205) 934-0453. Fax: (205) 934-1636. E-mail: gail_wertz{at}microbio.uab.edu.

Journal of Virology, January 1999, p. 297-306, Vol. 73, No. 1
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Li, J., Rahmeh, A., Brusic, V., Whelan, S. P. J. (2009). Opposing Effects of Inhibiting Cap Addition and Cap Methylation on Polyadenylation during Vesicular Stomatitis Virus mRNA Synthesis. J. Virol. 83: 1930-1940 [Abstract] [Full Text]  
  • Wang, J. T., McElvain, L. E., Whelan, S. P. J. (2007). Vesicular Stomatitis Virus mRNA Capping Machinery Requires Specific cis-Acting Signals in the RNA. J. Virol. 81: 11499-11506 [Abstract] [Full Text]  
  • Li, J., Chorba, J. S., Whelan, S. P. J. (2007). Vesicular Stomatitis Viruses Resistant to the Methylase Inhibitor Sinefungin Upregulate RNA Synthesis and Reveal Mutations That Affect mRNA Cap Methylation. J. Virol. 81: 4104-4115 [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]  
  • Lowen, A. C., Elliott, R. M. (2005). Mutational Analyses of the Nonconserved Sequences in the Bunyamwera Orthobunyavirus S Segment Untranslated Regions. J. Virol. 79: 12861-12870 [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]  
  • Rosario, D., Perez, M., de la Torre, J. C. (2005). Functional Characterization of the Genomic Promoter of Borna Disease Virus (BDV): Implications of 3'-Terminal Sequence Heterogeneity for BDV Persistence. J. Virol. 79: 6544-6550 [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]  
  • Perez, M., de la Torre, J. C. (2002). Characterization of the Genomic Promoter of the Prototypic Arenavirus Lymphocytic Choriomeningitis Virus. J. Virol. 77: 1184-1194 [Abstract] [Full Text]  
  • Gupta, A. K., Shaji, D., Banerjee, A. K. (2002). Identification of a Novel Tripartite Complex Involved in Replication of Vesicular Stomatitis Virus Genome RNA. J. Virol. 77: 732-738 [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]  
  • Rodriguez, L. L., Pauszek, S. J., Bunch, T. A., Schumann, K. R. (2002). Full-length genome analysis of natural isolates of vesicular stomatitis virus (Indiana 1 serotype) from North, Central and South America. J. Gen. Virol. 83: 2475-2483 [Abstract] [Full Text]  
  • Whelan, S. P. J., Wertz, G. W. (2002). Transcription and replication initiate at separate sites on the vesicular stomatitis virus genome. Proc. Natl. Acad. Sci. USA 99: 9178-9183 [Abstract] [Full Text]  
  • Hinzman, E. E., Barr, J. N., Wertz, G. W. (2002). Identification of an Upstream Sequence Element Required for Vesicular Stomatitis Virus mRNA Transcription. J. Virol. 76: 7632-7641 [Abstract] [Full Text]  
  • Wertz, G. W., Moudy, R., Ball, L. A. (2002). Adding Genes to the RNA Genome of Vesicular Stomatitis Virus: Positional Effects on Stability of Expression. J. Virol. 76: 7642-7650 [Abstract] [Full Text]  
  • Fearns, R., Peeples, M. E., Collins, P. L. (2002). Mapping the Transcription and Replication Promoters of Respiratory Syncytial Virus. J. Virol. 76: 1663-1672 [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]  
  • Lyons, T., Murray, K. E., Roberts, A. W., Barton, D. J. (2001). Poliovirus 5'-Terminal Cloverleaf RNA Is Required in cis for VPg Uridylylation and the Initiation of Negative-Strand RNA Synthesis. J. Virol. 75: 10696-10708 [Abstract] [Full Text]  
  • Barr, J. N., Wertz, G. W. (2001). Polymerase Slippage at Vesicular Stomatitis Virus Gene Junctions To Generate Poly(A) Is Regulated by the Upstream 3'-AUAC-5' Tetranucleotide: Implications for the Mechanism of Transcription Termination. J. Virol. 75: 6901-6913 [Abstract] [Full Text]  
  • Huang, P., Lai, M. M. C. (2001). Heterogeneous Nuclear Ribonucleoprotein A1 Binds to the 3'-Untranslated Region and Mediates Potential 5'-3'-End Cross Talks of Mouse Hepatitis Virus RNA. J. Virol. 75: 5009-5017 [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]  
  • Whelan, S. P. J., Barr, J. N., Wertz, G. W. (2000). Identification of a Minimal Size Requirement for Termination of Vesicular Stomatitis Virus mRNA: Implications for the Mechanism of Transcription. J. Virol. 74: 8268-8276 [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]  
  • Dupuy, L. C., Dobson, S., Bitko, V., Barik, S. (1999). Casein Kinase 2-Mediated Phosphorylation of Respiratory Syncytial Virus Phosphoprotein P Is Essential for the Transcription Elongation Activity of the Viral Polymerase; Phosphorylation by Casein Kinase 1 Occurs Mainly at Ser215 and Is without Effect. J. Virol. 73: 8384-8392 [Abstract] [Full Text]  
  • Whelan, S. P. J., Wertz, G. W. (1999). The 5' Terminal Trailer Region of Vesicular Stomatitis Virus Contains a Position-Dependent cis-Acting Signal for Assembly of RNA into Infectious Particles. J. Virol. 73: 307-315 [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»