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 Narayanan, K.
Right arrow Articles by Makino, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Narayanan, K.
Right arrow Articles by Makino, S.

 Previous Article  |  Next Article 

Journal of Virology, October 2001, p. 9059-9067, Vol. 75, No. 19
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.19.9059-9067.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Cooperation of an RNA Packaging Signal and a Viral Envelope Protein in Coronavirus RNA Packaging

Krishna Narayanan and Shinji Makino*

Department of Microbiology and Immunology, The University of Texas Medical Branch at Galveston, Galveston, Texas 77555-1019, and Department of Microbiology and Institute for Cellular and Molecular Biology, The University of Texas at Austin, Austin, Texas 78712-1095

Received 7 March 2001/Accepted 5 July 2001

Murine coronavirus mouse hepatitis virus (MHV) produces a genome-length mRNA, mRNA 1, and six or seven species of subgenomic mRNAs in infected cells. Among these mRNAs, only mRNA 1 is efficiently packaged into MHV particles. MHV N protein binds to all MHV mRNAs, whereas envelope M protein interacts only with mRNA 1. This M protein-mRNA 1 interaction most probably determines the selective packaging of mRNA 1 into MHV particles. A short cis-acting MHV RNA packaging signal is necessary and sufficient for packaging RNA into MHV particles. The present study tested the possibility that the selective M protein-mRNA 1 interaction is due to the packaging signal in mRNA 1. Regardless of the presence or absence of the packaging signal, N protein bound to MHV defective interfering RNAs and intracellularly expressed non-MHV RNA transcripts to form ribonucleoprotein complexes; M protein, however, interacted selectively with RNAs containing the packaging signal. Moreover, only the RNA that interacted selectively with M protein was efficiently packaged into MHV particles. Thus, it was the packaging signal that mediated the selective interaction between M protein and viral RNA to drive the specific packaging of RNA into virus particles. This is the first example for any RNA virus in which a viral envelope protein and a known viral RNA packaging signal have been shown to determine the specificity and selectivity of RNA packaging into virions.


* Corresponding author. Mailing address: Department of Microbiology and Immunology, The University of Texas Medical Branch at Galveston, Galveston, TX 77555-1019. Phone: (409) 772-2323. Fax: (409) 772-5065. E-mail: shmakino{at}utmb.edu.


Journal of Virology, October 2001, p. 9059-9067, Vol. 75, No. 19
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.19.9059-9067.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Hurst, K. R., Koetzner, C. A., Masters, P. S. (2009). Identification of In Vivo-Interacting Domains of the Murine Coronavirus Nucleocapsid Protein. J. Virol. 83: 7221-7234 [Abstract] [Full Text]  
  • Chen, S.-C., van den Born, E., van den Worm, S. H. E., Pleij, C. W. A., Snijder, E. J., Olsthoorn, R. C. L. (2007). New Structure Model for the Packaging Signal in the Genome of Group IIa Coronaviruses. J. Virol. 81: 6771-6774 [Abstract] [Full Text]  
  • Verma, S., Lopez, L. A., Bednar, V., Hogue, B. G. (2007). Importance of the Penultimate Positive Charge in Mouse Hepatitis Coronavirus A59 Membrane Protein. J. Virol. 81: 5339-5348 [Abstract] [Full Text]  
  • Ye, Y., Hauns, K., Langland, J. O., Jacobs, B. L., Hogue, B. G. (2007). Mouse Hepatitis Coronavirus A59 Nucleocapsid Protein Is a Type I Interferon Antagonist. J. Virol. 81: 2554-2563 [Abstract] [Full Text]  
  • Kamitani, W., Narayanan, K., Huang, C., Lokugamage, K., Ikegami, T., Ito, N., Kubo, H., Makino, S. (2006). Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc. Natl. Acad. Sci. USA 103: 12885-12890 [Abstract] [Full Text]  
  • Hsieh, P.-K., Chang, S. C., Huang, C.-C., Lee, T.-T., Hsiao, C.-W., Kou, Y.-H., Chen, I-Y., Chang, C.-K., Huang, T.-H., Chang, M.-F. (2005). Assembly of Severe Acute Respiratory Syndrome Coronavirus RNA Packaging Signal into Virus-Like Particles Is Nucleocapsid Dependent. J. Virol. 79: 13848-13855 [Abstract] [Full Text]  
  • Hurst, K. R., Kuo, L., Koetzner, C. A., Ye, R., Hsue, B., Masters, P. S. (2005). A Major Determinant for Membrane Protein Interaction Localizes to the Carboxy-Terminal Domain of the Mouse Coronavirus Nucleocapsid Protein. J. Virol. 79: 13285-13297 [Abstract] [Full Text]  
  • Ikegami, T., Won, S., Peters, C. J., Makino, S. (2005). Rift Valley Fever Virus NSs mRNA Is Transcribed from an Incoming Anti-Viral-Sense S RNA Segment. J. Virol. 79: 12106-12111 [Abstract] [Full Text]  
  • Schelle, B., Karl, N., Ludewig, B., Siddell, S. G., Thiel, V. (2005). Selective Replication of Coronavirus Genomes That Express Nucleocapsid Protein. J. Virol. 79: 6620-6630 [Abstract] [Full Text]  
  • Coley, S. E., Lavi, E., Sawicki, S. G., Fu, L., Schelle, B., Karl, N., Siddell, S. G., Thiel, V. (2005). Recombinant Mouse Hepatitis Virus Strain A59 from Cloned, Full-Length cDNA Replicates to High Titers In Vitro and Is Fully Pathogenic In Vivo. J. Virol. 79: 3097-3106 [Abstract] [Full Text]  
  • Ito, N., Mossel, E. C., Narayanan, K., Popov, V. L., Huang, C., Inoue, T., Peters, C. J., Makino, S. (2005). Severe Acute Respiratory Syndrome Coronavirus 3a Protein Is a Viral Structural Protein. J. Virol. 79: 3182-3186 [Abstract] [Full Text]  
  • Ye, R., Montalto-Morrison, C., Masters, P. S. (2004). Genetic Analysis of Determinants for Spike Glycoprotein Assembly into Murine Coronavirus Virions: Distinct Roles for Charge-Rich and Cysteine-Rich Regions of the Endodomain. J. Virol. 78: 9904-9917 [Abstract] [Full Text]  
  • Bosch, B. J., de Haan, C. A. M., Rottier, P. J. M. (2004). Coronavirus Spike Glycoprotein, Extended at the Carboxy Terminus with Green Fluorescent Protein, Is Assembly Competent. J. Virol. 78: 7369-7378 [Abstract] [Full Text]  
  • Goebel, S. J., Hsue, B., Dombrowski, T. F., Masters, P. S. (2004). Characterization of the RNA Components of a Putative Molecular Switch in the 3' Untranslated Region of the Murine Coronavirus Genome. J. Virol. 78: 669-682 [Abstract] [Full Text]  
  • Escors, D., Izeta, A., Capiscol, C., Enjuanes, L. (2003). Transmissible Gastroenteritis Coronavirus Packaging Signal Is Located at the 5' End of the Virus Genome. J. Virol. 77: 7890-7902 [Abstract] [Full Text]  
  • Haijema, B. J., Volders, H., Rottier, P. J. M. (2003). Switching Species Tropism: an Effective Way To Manipulate the Feline Coronavirus Genome. J. Virol. 77: 4528-4538 [Abstract] [Full Text]  
  • Kuo, L., Masters, P. S. (2003). The Small Envelope Protein E Is Not Essential for Murine Coronavirus Replication. J. Virol. 77: 4597-4608 [Abstract] [Full Text]  
  • Narayanan, K., Chen, C.-J., Maeda, J., Makino, S. (2003). Nucleocapsid-Independent Specific Viral RNA Packaging via Viral Envelope Protein and Viral RNA Signal. J. Virol. 77: 2922-2927 [Abstract] [Full Text]  
  • Kuo, L., Masters, P. S. (2002). Genetic Evidence for a Structural Interaction between the Carboxy Termini of the Membrane and Nucleocapsid Proteins of Mouse Hepatitis Virus. J. Virol. 76: 4987-4999 [Abstract] [Full Text]