1887

Journal of General Virology header logo

Volume 95, Issue 7

Differential restriction patterns of mRNA decay factor AUF1 during picornavirus infections Free

Abstract

During infection by picornaviruses, the cellular environment is modified to favour virus replication. This includes the modification of specific host proteins, including the recently discovered viral proteinase cleavage of mRNA decay factor AU-rich binding factor 1 (AUF1). This cellular RNA-binding protein was shown previously to act as a restriction factor during poliovirus, rhinovirus and coxsackievirus infection. During infection by these viruses, AUF1 relocalizes to the cytoplasm and is cleaved by the viral 3C/3CD proteinase. In this study, we demonstrated that replication of encephalomyocarditis virus (EMCV), a picornavirus belonging to the genus , is AUF1 independent. During EMCV infection, AUF1 relocalized to the cytoplasm; however, unlike what is seen during enterovirus infections, AUF1 was not cleaved to detectable levels, even at late times after infection. This suggests that AUF1 does not act broadly as an inhibitor of picornavirus infections but may instead act as a selective restriction factor targeting members of the genus .

  • Received:
  • Accepted:
  • Published Online:
© 2014 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.064501-0
2014-07-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/7/1488.html?itemId=/content/journal/jgv/10.1099/vir.0.064501-0&mimeType=html&fmt=ahah

References

  1. Agol V. I., Gmyl A. P. 2010; Viral security proteins: counteracting host defences. Nat Rev Microbiol 8:867–878 [View Article][PubMed]
     [Google Scholar]
  2. Back S. H., Kim Y. K., Kim W. J., Cho S., Oh H. R., Kim J. E., Jang S. K. 2002; Translation of polioviral mRNA is inhibited by cleavage of polypyrimidine tract-binding proteins executed by polioviral 3Cpro . J Virol 76:2529–2542 [View Article][PubMed]
     [Google Scholar]
  3. Barral P. M., Morrison J. M., Drahos J., Gupta P., Sarkar D., Fisher P. B., Racaniello V. R. 2007; MDA-5 is cleaved in poliovirus-infected cells. J Virol 81:3677–3684 [View Article][PubMed]
     [Google Scholar]
  4. Barral P. M., Sarkar D., Fisher P. B., Racaniello V. R. 2009; RIG-I is cleaved during picornavirus infection. Virology 391:171–176 [View Article][PubMed]
     [Google Scholar]
  5. Castelló A., Izquierdo J. M., Welnowska E., Carrasco L. 2009; RNA nuclear export is blocked by poliovirus 2A protease and is concomitant with nucleoporin cleavage. J Cell Sci 122:3799–3809 [View Article][PubMed]
     [Google Scholar]
  6. Castelló A., Alvarez E., Carrasco L. 2011; The multifaceted poliovirus 2A protease: regulation of gene expression by picornavirus proteases. J Biomed Biotechnol 2011:369648 [View Article][PubMed]
     [Google Scholar]
  7. Cathcart A. L., Rozovics J. M., Semler B. L. 2013; Cellular mRNA decay protein AUF1 negatively regulates enterovirus and human rhinovirus infections. J Virol 87:10423–10434 [View Article][PubMed]
     [Google Scholar]
  8. Dougherty J. D., White J. P., Lloyd R. E. 2011; Poliovirus-mediated disruption of cytoplasmic processing bodies. J Virol 85:64–75 [View Article][PubMed]
     [Google Scholar]
  9. Fitzgerald K. D., Semler B. L. 2009; Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim Biophys Acta 1789:518–528 [View Article][PubMed]
     [Google Scholar]
  10. Fitzgerald K. D., Semler B. L. 2011; Re-localization of cellular protein SRp20 during poliovirus infection: bridging a viral IRES to the host cell translation apparatus. PLoS Pathog 7:e1002127 [View Article][PubMed]
     [Google Scholar]
  11. Funk A., Truong K., Nagasaki T., Torres S., Floden N., Balmori Melian E., Edmonds J., Dong H., Shi P. Y., Khromykh A. A. 2010; RNA structures required for production of subgenomic flavivirus RNA. J Virol 84:11407–11417 [View Article][PubMed]
     [Google Scholar]
  12. Garneau N. L., Sokoloski K. J., Opyrchal M., Neff C. P., Wilusz C. J., Wilusz J. 2008; The 3′ untranslated region of Sindbis virus represses deadenylation of viral transcripts in mosquito and mammalian cells. J Virol 82:880–892 [View Article][PubMed]
     [Google Scholar]
  13. Gingras A. C., Svitkin Y., Belsham G. J., Pause A., Sonenberg N. 1996; Activation of the translational suppressor 4E-BP1 following infection with encephalomyocarditis virus and poliovirus. Proc Natl Acad Sci U S A 93:5578–5583 [View Article][PubMed]
     [Google Scholar]
  14. Gustin K. E., Sarnow P. 2001; Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J 20:240–249 [View Article][PubMed]
     [Google Scholar]
  15. Hato S. V., Ricour C., Schulte B. M., Lanke K. H., de Bruijni M., Zoll J., Melchers W. J., Michiels T., van Kuppeveld F. J. 2007; The mengovirus leader protein blocks interferon-α/β gene transcription and inhibits activation of interferon regulatory factor 3. Cell Microbiol 9:2921–2930 [View Article][PubMed]
     [Google Scholar]
  16. Lee C., Gyorgy A., Maric D., Sadri N., Schneider R. J., Barker J. L., Lawson M., Agoston D. V. 2008; Members of the NuRD chromatin remodeling complex interact with AUF1 in developing cortical neurons. Cereb Cortex 18:2909–2919 [View Article][PubMed]
     [Google Scholar]
  17. Moon S. L., Anderson J. R., Kumagai Y., Wilusz C. J., Akira S., Khromykh A. A., Wilusz J. 2012; A noncoding RNA produced by arthropod-borne flaviviruses inhibits the cellular exoribonuclease XRN1 and alters host mRNA stability. RNA 18:2029–2040 [View Article][PubMed]
     [Google Scholar]
  18. Murray K. E., Roberts A. W., Barton D. J. 2001; Poly(rC) binding proteins mediate poliovirus mRNA stability. RNA 7:1126–1141 [View Article][PubMed]
     [Google Scholar]
  19. Paek K. Y., Kim C. S., Park S. M., Kim J. H., Jang S. K. 2008; RNA-binding protein hnRNP D modulates internal ribosome entry site-dependent translation of hepatitis C virus RNA. J Virol 82:12082–12093 [View Article][PubMed]
     [Google Scholar]
  20. Palmenberg A. C. 1990; Proteolytic processing of picornaviral polyprotein. Annu Rev Microbiol 44:603–623 [View Article][PubMed]
     [Google Scholar]
  21. Papon L., Oteiza A., Imaizumi T., Kato H., Brocchi E., Lawson T. G., Akira S., Mechti N. 2009; The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology 393:311–318 [View Article][PubMed]
     [Google Scholar]
  22. Park N., Skern T., Gustin K. E. 2010; Specific cleavage of the nuclear pore complex protein Nup62 by a viral protease. J Biol Chem 285:28796–28805 [View Article][PubMed]
     [Google Scholar]
  23. Porter F. W., Palmenberg A. C. 2009; Leader-induced phosphorylation of nucleoporins correlates with nuclear trafficking inhibition by cardioviruses. J Virol 83:1941–1951 [View Article][PubMed]
     [Google Scholar]
  24. Porter F. W., Brown B., Palmenberg A. C. 2010; Nucleoporin phosphorylation triggered by the encephalomyocarditis virus leader protein is mediated by mitogen-activated protein kinases. J Virol 84:12538–12548 [View Article][PubMed]
     [Google Scholar]
  25. Racaniello V. R. 2010; Innate immune responses. In The Picornaviruses pp. 287–302 Edited by Ehrenfeld E., Domingo E., Roos R. P. Washington, DC: American Society for Microbiology; [View Article]
     [Google Scholar]
  26. Rozovics J. M., Chase A. J., Cathcart A. L., Chou W., Gershon P. D., Palusa S., Wilusz J., Semler B. L. 2012; Picornavirus modification of a host mRNA decay protein. MBio 3:e00431–e12 [View Article][PubMed]
     [Google Scholar]
  27. Shimakami T., Yamane D., Jangra R. K., Kempf B. J., Spaniel C., Barton D. J., Lemon S. M. 2012; Stabilization of hepatitis C virus RNA by an Ago2–miR-122 complex. Proc Natl Acad Sci U S A 109:941–946 [View Article][PubMed]
     [Google Scholar]
  28. Shiroki K., Isoyama T., Kuge S., Ishii T., Ohmi S., Hata S., Suzuki K., Takasaki Y., Nomoto A. 1999; Intracellular redistribution of truncated La protein produced by poliovirus 3Cpro-mediated cleavage. J Virol 73:2193–2200[PubMed]
     [Google Scholar]
  29. Silva P. A., Pereira C. F., Dalebout T. J., Spaan W. J., Bredenbeek P. J. 2010; An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. J Virol 84:11395–11406 [View Article][PubMed]
     [Google Scholar]
  30. Sokoloski K. J., Dickson A. M., Chaskey E. L., Garneau N. L., Wilusz C. J., Wilusz J. 2010; Sindbis virus usurps the cellular HuR protein to stabilize its transcripts and promote productive infections in mammalian and mosquito cells. Cell Host Microbe 8:196–207 [View Article][PubMed]
     [Google Scholar]
  31. Spurrell J. C., Wiehler S., Zaheer R. S., Sanders S. P., Proud D. 2005; Human airway epithelial cells produce IP-10 (CXCL10) in vitro and in vivo upon rhinovirus infection. Am J Physiol Lung Cell Mol Physiol 289:L85–L95 [View Article][PubMed]
     [Google Scholar]
  32. Townsend H. L., Jha B. K., Han J. Q., Maluf N. K., Silverman R. H., Barton D. J. 2008; A viral RNA competitively inhibits the antiviral endoribonuclease domain of RNase L. RNA 14:1026–1036 [View Article][PubMed]
     [Google Scholar]
  33. Watters K., Palmenberg A. C. 2011; Differential processing of nuclear pore complex proteins by rhinovirus 2A proteases from different species and serotypes. J Virol 85:10874–10883 [View Article][PubMed]
     [Google Scholar]
  34. Wong J., Si X., Angeles A., Zhang J., Shi J., Fung G., Jagdeo J., Wang T., Zhong Z.other authors 2013; Cytoplasmic redistribution and cleavage of AUF1 during coxsackievirus infection enhance the stability of its viral genome. FASEB J 27:2777–2787 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.064501-0
Loading
Differential restriction patterns of mRNA decay factor AUF1 during picornavirus infections
J. Gen. Virol. 95, 1488 (2014); https://doi.org/10.1099/vir.0.064501-0
/content/journal/jgv/10.1099/vir.0.064501-0
/content/journal/jgv/10.1099/vir.0.064501-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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