1887

Abstract

Rubella virus (RUBV) replicates slowly and to low titre in vertebrate cultured cells, with minimal cytopathology. To determine whether a cellular stress response is induced during such an infection, the formation of Ras-GAP-SH3 domain-binding protein (G3BP)-containing stress granules (SGs) in RUBV-infected cells was examined. Late in infection, accumulation of G3BP granules was detected, albeit in fewer than half of infected cells. Active virus RNA replication was required for induction of these granules, but they were found to differ from SGs induced by arsenite treatment both in composition (they did not uniformly contain other SG proteins, such as PABP and TIA-1) and in resistance to cycloheximide treatment. Thus, bona fide SGs do not appear to be induced during RUBV infection. The distribution of G3BP, either on its own or in granules, did not overlap with that of dsRNA-containing replication complexes, indicating that it played no role in virus RNA synthesis. However, G3BP did co-localize with viral ssRNAs in perinuclear clusters, suggesting an interaction that could possibly be important in a post-replicative role in virus replication, such as encapsidation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.036780-0
2012-02-01
2020-09-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/2/267.html?itemId=/content/journal/jgv/10.1099/vir.0.036780-0&mimeType=html&fmt=ahah

References

  1. Afonina E., Stauber R., Pavlakis G. N.. 1998; The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J Biol Chem273:13015–13021 [CrossRef][PubMed]
    [Google Scholar]
  2. Anderson P., Kedersha N.. 2002; Visibly stressed: the role of eIF2, TIA-1, and stress granules in protein translation. Cell Stress Chaperones7:213–221 [CrossRef][PubMed]
    [Google Scholar]
  3. Beatch M. D., Hobman T. C.. 2000; Rubella virus capsid associates with host cell protein p32 and localizes to mitochondria. J Virol74:5569–5576 [CrossRef][PubMed]
    [Google Scholar]
  4. Beckham C. J., Parker R.. 2008; P bodies, stress granules, and viral life cycles. Cell Host Microbe3:206–212 [CrossRef][PubMed]
    [Google Scholar]
  5. Brune C., Munchel S. E., Fischer N., Podtelejnikov A. V., Weis K.. 2005; Yeast poly(A)-binding protein Pab1 shuttles between the nucleus and the cytoplasm and functions in mRNA export. RNA11:517–531 [CrossRef][PubMed]
    [Google Scholar]
  6. Cristea I. M., Rozjabek H., Molloy K. R., Karki S., White L. L., Rice C. M., Rout M. P., Chait B. T., MacDonald M. R.. 2010; Host factors associated with the Sindbis virus RNA-dependent RNA polymerase: role for G3BP1 and G3BP2 in virus replication. J Virol84:6720–6732 [CrossRef][PubMed]
    [Google Scholar]
  7. Emara M. M., Brinton M. A.. 2007; Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc Natl Acad Sci U S A104:9041–9046 [CrossRef][PubMed]
    [Google Scholar]
  8. Forng R. Y., Frey T. K.. 1995; Identification of the rubella virus nonstructural proteins. Virology206:843–853 [CrossRef][PubMed]
    [Google Scholar]
  9. Frey T. K.. 1994; Molecular biology of rubella virus. Adv Virus Res44:69–160 [CrossRef][PubMed]
    [Google Scholar]
  10. Gorchakov R., Garmashova N., Frolova E., Frolov I.. 2008; Different types of nsP3-containing protein complexes in Sindbis virus-infected cells. J Virol82:10088–10101 [CrossRef][PubMed]
    [Google Scholar]
  11. Harb M., Becker M. M., Vitour D., Baron C. H., Vende P., Brown S. C., Bolte S., Arold S. T., Poncet D.. 2008; Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. J Virol82:11283–11293 [CrossRef][PubMed]
    [Google Scholar]
  12. Hemphill M. L., Forng R. Y., Abernathy E. S., Frey T. K.. 1988; Time course of virus-specific macromolecular synthesis during rubella virus infection in Vero cells. Virology162:65–75 [CrossRef][PubMed]
    [Google Scholar]
  13. Ilkow C. S., Mancinelli V., Beatch M. D., Hobman T. C.. 2008; Rubella virus capsid protein interacts with poly(A)-binding protein and inhibits translation. J Virol82:4284–4294 [CrossRef][PubMed]
    [Google Scholar]
  14. Jiménez-García L. F., Spector D. L.. 1993; In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell73:47–59 [CrossRef][PubMed]
    [Google Scholar]
  15. Kedersha N., Anderson P.. 2002; Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem Soc Trans30:963–969 [CrossRef][PubMed]
    [Google Scholar]
  16. Kedersha N. L., Gupta M., Li W., Miller I., Anderson P.. 1999; RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2α to the assembly of mammalian stress granules. J Cell Biol147:1431–1442 [CrossRef][PubMed]
    [Google Scholar]
  17. Kedersha N., Cho M. R., Li W., Yacono P. W., Chen S., Gilks N., Golan D. E., Anderson P.. 2000; Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol151:1257–1268 [CrossRef][PubMed]
    [Google Scholar]
  18. Kedersha N., Stoecklin G., Ayodele M., Yacono P., Lykke-Andersen J., Fritzler M. J., Scheuner D., Kaufman R. J., Golan D. E., Anderson P.. 2005; Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol169:871–884 [CrossRef][PubMed]
    [Google Scholar]
  19. Kujala P., Ahola T., Ehsani N., Auvinen P., Vihinen H., Kääriäinen L.. 1999; Intracellular distribution of rubella virus nonstructural protein P150. J Virol73:7805–7811[PubMed]
    [Google Scholar]
  20. Lee J. Y., Marshall J. A., Bowden D. S.. 1992; Replication complexes associated with the morphogenesis of rubella virus. Arch Virol122:95–106 [CrossRef][PubMed]
    [Google Scholar]
  21. Lee J. Y., Marshall J. A., Bowden D. S.. 1994; Characterization of rubella virus replication complexes using antibodies to double-stranded RNA. Virology200:307–312 [CrossRef][PubMed]
    [Google Scholar]
  22. Magliano D., Marshall J. A., Bowden D. S., Vardaxis N., Meanger J., Lee J. Y.. 1998; Rubella virus replication complexes are virus-modified lysosomes. Virology240:57–63 [CrossRef][PubMed]
    [Google Scholar]
  23. Matthews J. D., Tzeng W. P., Frey T. K.. 2009; Determinants of subcellular localization of the rubella virus nonstructural replicase proteins. Virology390:315–323 [CrossRef][PubMed]
    [Google Scholar]
  24. Matthews J. D., Tzeng W. P., Frey T. K.. 2010; Analysis of the function of cytoplasmic fibers formed by the rubella virus nonstructural replicase proteins. Virology406:212–227 [CrossRef][PubMed]
    [Google Scholar]
  25. Mazroui R., Sukarieh R., Bordeleau M. E., Kaufman R. J., Northcote P., Tanaka J., Gallouzi I., Pelletier J.. 2006; Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2α phosphorylation. Mol Biol Cell17:4212–4219 [CrossRef][PubMed]
    [Google Scholar]
  26. McInerney G. M., Kedersha N. L., Kaufman R. J., Anderson P., Liljeström P.. 2005; Importance of eIF2α phosphorylation and stress granule assembly in alphavirus translation regulation. Mol Biol Cell16:3753–3763 [CrossRef][PubMed]
    [Google Scholar]
  27. Parker F., Maurier F., Delumeau I., Duchesne M., Faucher D., Debussche L., Dugue A., Schweighoffer F., Tocque B.. 1996; A Ras-GTPase-activating protein SH3-domain-binding protein. Mol Cell Biol16:2561–2569[PubMed]
    [Google Scholar]
  28. Pugachev K. V., Galinski M. S., Frey T. K.. 2000; Infectious cDNA clone of the RA27/3 vaccine strain of rubella virus. Virology273:189–197 [CrossRef][PubMed]
    [Google Scholar]
  29. Tocque B., Delumeau I., Parker F., Maurier F., Multon M. C., Schweighoffer F.. 1997; Ras-GTPase activating protein (GAP): a putative effector for Ras. Cell Signal9:153–158 [CrossRef][PubMed]
    [Google Scholar]
  30. Tourrière H., Gallouzi I. E., Chebli K., Capony J. P., Mouaikel J., van der Geer P., Tazi J.. 2001; RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol Cell Biol21:7747–7760 [CrossRef][PubMed]
    [Google Scholar]
  31. Tourrière H., Chebli K., Zekri L., Courselaud B., Blanchard J. M., Bertrand E., Tazi J.. 2003; The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol160:823–831 [CrossRef][PubMed]
    [Google Scholar]
  32. Tzeng W. P., Matthews J. D., Frey T. K.. 2006; Analysis of rubella virus capsid protein-mediated enhancement of replicon replication and mutant rescue. J Virol80:3966–3974 [CrossRef][PubMed]
    [Google Scholar]
  33. White J. P., Cardenas A. M., Marissen W. E., Lloyd R. E.. 2007; Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe2:295–305 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.036780-0
Loading
/content/journal/jgv/10.1099/vir.0.036780-0
Loading

Data & Media loading...

Most cited this month 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