1887

Abstract

Passage of foot-and-mouth disease virus (FMDV) in BHK-21 cells resulted in the segmentation of the viral genome into two defective RNAs lacking part of either the L- or the capsid-coding region. The two RNAs are infectious by complementation. Electroporation of L-defective RNA in BHK-21 cells resulted in the accumulation of the precursor P3 located away from the deleted sequence. Expression of L led to the processing of P3, indicating that there is a connection between L protease activity and the secondary cleavages carried out by 3C protease within P3. These results suggest that the complementation mechanism between defective RNAs is not restricted to supplying the L and capsid proteins but that distance effects on polyprotein processing events are also implicated.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000480
2016-07-01
2020-01-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/7/1575.html?itemId=/content/journal/jgv/10.1099/jgv.0.000480&mimeType=html&fmt=ahah

References

  1. Arias A., Agudo R., Ferrer-Orta C., Pérez-Luque R., Airaksinen A., Brocchi E., Domingo E., Verdaguer N., Escarmís C.. 2005; Mutant viral polymerase in the transition of virus to error catastrophe identifies a critical site for RNA binding. J Mol Biol353:1021–1032 [CrossRef][PubMed]
    [Google Scholar]
  2. Armer H., Moffat K., Wileman T., Belsham G. J., Jackson T., Duprex W. P., Ryan M., Monaghan P.. 2008; Foot-and-mouth disease virus, but not bovine enterovirus, targets the host cell cytoskeleton via the nonstructural protein 3Cpro. J Virol82:10556–10566 [CrossRef][PubMed]
    [Google Scholar]
  3. Belsham G. J.. 1992; Dual initiation sites of protein synthesis on foot-and-mouth disease virus RNA are selected following internal entry and scanning of ribosomes in vivo. EMBO J11:1105–1110[PubMed]
    [Google Scholar]
  4. Belsham G. J.. 1993; Distinctive features of foot-and-mouth disease virus, a member of the picornavirus family; aspects of virus protein synthesis, protein processing and structure. Prog Biophys Mol Biol60:241–260[PubMed][CrossRef]
    [Google Scholar]
  5. Belsham G. J., McInerney G. M., Ross-Smith N.. 2000; Foot-and-mouth disease virus 3C protease induces cleavage of translation initiation factors eIF4A and eIF4G within infected cells. J Virol74:272–280[PubMed][CrossRef]
    [Google Scholar]
  6. Belsham G. J.. 2013; Influence of the leader protein coding region of foot-and-mouth disease virus on virus replication. J Gen Virol94:1486–1495 [CrossRef][PubMed]
    [Google Scholar]
  7. Cao X., Bergmann I. E., Füllkrug R., Beck E.. 1995; Functional analysis of the two alternative translation initiation sites of foot-and-mouth disease virus. J Virol69:560–563[PubMed]
    [Google Scholar]
  8. Carrillo C., Tulman E. R., Delhon G., Lu Z., Carreno A., Vagnozzi A., Kutish G. F., Rock D. L.. 2005; Comparative genomics of foot-and-mouth disease virus. J Virol79:6487–6504 [CrossRef][PubMed]
    [Google Scholar]
  9. Chase A. J., Daijogo S., Semler B. L.. 2014; Inhibition of poliovirus-induced cleavage of cellular protein PCBP2 reduces the levels of viral RNA replication. J Virol88:3192–3201 [CrossRef][PubMed]
    [Google Scholar]
  10. Clarke B. E., Sangar D. V., Burroughs J. N., Newton S. E., Carroll A. R., Rowlands D. J.. 1985; Two initiation sites for foot-and-mouth disease virus polyprotein in vivo. J Gen Virol66:2615–2626 [CrossRef][PubMed]
    [Google Scholar]
  11. Domingo E., Dávila M., Ortín J.. 1980; Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth-disease virus. Gene11:333–346 [CrossRef][PubMed]
    [Google Scholar]
  12. Escarmís C., Perales C., Domingo E.. 2009; Biological effect of Muller's Ratchet: distant capsid site can affect picornavirus protein processing. J Virol83:6748–6756 [CrossRef][PubMed]
    [Google Scholar]
  13. Falk M. M., Grigera P. R., Bergmann I. E., Zibert A., Multhaup G., Beck E.. 1990; Foot-and-mouth disease virus protease 3C induces specific proteolytic cleavage of host cell histone H3. J Virol64:748–756[PubMed]
    [Google Scholar]
  14. Ferrer-Orta C., Arias A., Perez-Luque R., Escarmís C., Domingo E., Verdaguer N.. 2004; Structure of foot-and-mouth disease virus RNA-dependent RNA polymerase and its complex with a template-primer RNA. J Biol Chem279:47212–47221 [CrossRef][PubMed]
    [Google Scholar]
  15. García-Arriaza J., Manrubia S. C., Toja M., Domingo E., Escarmís C.. 2004; Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol78:11678–11685 [CrossRef][PubMed]
    [Google Scholar]
  16. García-Arriaza J., Domingo E., Escarmís C.. 2005; A segmented form of foot-and-mouth disease virus interferes with standard virus: a link between interference and competitive fitness. Virology335:155–164 [CrossRef][PubMed]
    [Google Scholar]
  17. García-Arriaza J., Ojosnegros S., Dávila M., Domingo E., Escarmís C.. 2006; Dynamics of mutation and recombination in a replicating population of complementing, defective viral genomes. J Mol Biol360:558–572 [CrossRef][PubMed]
    [Google Scholar]
  18. Gullberg M., Polacek C., Belsham G. J.. 2014; Sequence adaptations affecting cleavage of the VP1/2A junction by the 3C protease in foot-and-mouth disease virus-infected cells. J Gen Virol95:2402–2410 [CrossRef][PubMed]
    [Google Scholar]
  19. Herrera M., Grande-Pérez A., Perales C., Domingo E.. 2008; Persistence of foot-and-mouth disease virus in cell culture revisited: implications for contingency in evolution. J Gen Virol89:232–244 [CrossRef][PubMed]
    [Google Scholar]
  20. Li W., Ross-Smith N., Proud C. G., Belsham G. J.. 2001; Cleavage of translation initiation factor 4AI (eIF4AI) but not eIF4AII by foot-and-mouth disease virus 3C protease: identification of the eIF4AI cleavage site. FEBS Lett507:1–5 [CrossRef][PubMed]
    [Google Scholar]
  21. Liljeström P., Garoff H.. 1991; Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor. J Virol65:147–154[PubMed]
    [Google Scholar]
  22. Manrubia S. C., García-Arriaza J., Domingo E., Escarmís C.. 2006; Long-range transport and universality classes in in vitro viral infection spread. Euro Phy Lett74:547–553 [CrossRef]
    [Google Scholar]
  23. Mateu M. G., Rocha E., Vicente O., Vayreda F., Navalpotro C., Andreu D., Pedroso E., Giralt E., Enjuanes L., Domingo E.. 1987; Reactivity with monoclonal antibodies of viruses from an episode of foot-and-mouth disease. Virus Res8:261–274[PubMed][CrossRef]
    [Google Scholar]
  24. Medina M., Domingo E., Brangwyn J. K., Belsham G. J.. 1993; The two species of the foot-and-mouth disease virus leader protein, expressed individually, exhibit the same activities. Virology194:355–359 [CrossRef][PubMed]
    [Google Scholar]
  25. Moreno E., Ojosnegros S., García-Arriaza J., Escarmís C., Domingo E., Perales C.. 2014; Exploration of sequence space as the basis of viral RNA genome segmentation. Proc Natl Acad Sci U S A111:6678–6683 [CrossRef][PubMed]
    [Google Scholar]
  26. Ojosnegros S., García-Arriaza J., Escarmís C., Manrubia S. C., Perales C., Arias A., Mateu M. G., Domingo E.. 2011; Viral genome segmentation can result from a trade-off between genetic content and particle stability. PLoS Genet7:e1001344 [CrossRef][PubMed]
    [Google Scholar]
  27. Perales C., Mateo R., Mateu M. G., Domingo E.. 2007; Insights into RNA virus mutant spectrum and lethal mutagenesis events: replicative interference and complementation by multiple point mutants. J Mol Biol369:985–1000 [CrossRef][PubMed]
    [Google Scholar]
  28. Piccone M. E., Rieder E., Mason P. W., Grubman M. J.. 1995a; The foot-and-mouth disease virus leader proteinase gene is not required for viral replication. J Virol69:5376–5382
    [Google Scholar]
  29. Piccone M. E., Sira S., Zellner M., Grubman M. J.. 1995b; Expression in Escherichia coli and purification of biologically active L proteinase of foot-and-mouth disease virus. Virus Res35:263–275[CrossRef]
    [Google Scholar]
  30. Polacek C., Gullberg M., Li J., Belsham G. J.. 2013; Low levels of foot-and-mouth disease virus 3C protease expression are required to achieve optimal capsid protein expression and processing in mammalian cells. J Gen Virol94:1249–1258 [CrossRef][PubMed]
    [Google Scholar]
  31. Sangar D. V., Newton S. E., Rowlands D. J., Clarke B. E.. 1987; All foot and mouth disease virus serotypes initiate protein synthesis at two separate AUGs. Nucleic Acids Res15:3305–3315 [CrossRef][PubMed]
    [Google Scholar]
  32. Sobrino F., Dávila M., Ortín J., Domingo E.. 1983; Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology128:310–318 [CrossRef][PubMed]
    [Google Scholar]
  33. Strong R., Belsham G. J.. 2004; Sequential modification of translation initiation factor eIF4GI by two different foot-and-mouth disease virus proteases within infected baby hamster kidney cells: identification of the 3Cpro cleavage site. J Gen Virol85:2953–2962 [CrossRef][PubMed]
    [Google Scholar]
  34. Toja M., Escarmís C., Domingo E.. 1999; Genomic nucleotide sequence of a foot-and-mouth disease virus clone and its persistent derivatives. Implications for the evolution of viral quasispecies during a persistent infection. Virus Res64:161–171[PubMed][CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000480
Loading
/content/journal/jgv/10.1099/jgv.0.000480
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error