Respiratory syncytial virus induces host RNA stress granules to facilitate viral replication

Journal of Virology

Volumn 84, Issue 23, 2010, Pages 12274-12284

  Lindquist, Michael E ^a   Lifland, Aaron W ^c   Utley, Thomas J ^b   Santangelo, Philip J ^c   Crowe Jr , James E ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c Emory University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GENOMIC RNA; HUR PROTEIN; RAS GAP SH3 DOMAIN BINDING PROTEIN; RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CELL GRANULE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; PNEUMOVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RNA INTERFERENCE; RNA PROBE; STRESS GRANULE; VIRUS CELL INTERACTION; VIRUS INCLUSION; VIRUS REPLICATION;

ANTIGENS, SURFACE; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE; CYTOPLASMIC GRANULES; EPITHELIAL CELLS; HUMANS; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; RNA-BINDING PROTEINS; STRESS, PHYSIOLOGICAL; VIRUS REPLICATION;

MAMMALIA; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 78049506923     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00260-10     Document Type: Article

References (39)

1. Brown, G., H. W. Rixon, J. Steel, T. P. McDonald, A. R. Pitt, S. Graham, and R. J. Sugrue. 2005. Evidence for an association between heat shock protein 70 and the respiratory syncytial virus polymerase complex within lipid-raft membranes during virus infection. Virology 338:69-80.
2. Carlos, T. S., D. F. Young, M. Schneider, J. P. Simas, and R. E. Randall. 2009. Parainfluenza virus 5 genomes are located in viral cytoplasmic bodies whilst the virus dismantles the interferon-induced antiviral state of cells. J. Gen. Virol. 90:2147-2156.
3. Carromeu, C., F. M. Simabuco, R. E. Tamura, L. E. Farinha Arcieri, and A. M. Ventura. 2007. Intracellular localization of human respiratory syncytial virus L protein. Arch. Virol. 152:2259-2263.
4. Cristea, I. M., J. W. Carroll, M. P. Rout, C. M. Rice, B. T. Chait, and M. R. MacDonald. 2006. Tracking and elucidating alphavirus-host protein interactions. J. Biol. Chem. 281:30269-30278.
5. Dang, Y., N. Kedersha, W. K. Low, D. Romo, M. Gorospe, R. Kaufman, P. Anderson, and J. O. Liu. 2006. Eukaryotic initiation factor 2alpha-independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 281:32870-32878.
6. Emara, M. M., and M. A. Brinton. 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. A. 104:9041-9046.
7. Fields, B. N., D. M. Knipe, and P. M. Howley. 2007. Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
8. Gallouzi, I. E., F. Parker, K. Chebli, F. Maurier, E. Labourier, I. Barlat, J. P. Capony, B. Tocque, and J. Tazi. 1998. A novel phosphorylation- dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol. Cell. Biol. 18:3956-3965.
9. Garcia, J., B. Garcia-Barreno, A. Vivo, and J. A. Melero. 1993. Cytoplasmic inclusions of respiratory syncytial virus-infected cells: formation of inclusion bodies in transfected cells that coexpress the nucleoprotein, the phosphoprotein, and the 22K protein. Virology 195:243-247.
10. Garcia-Barreno, B., T. Delgado, and J. A. Melero. 1996. Identification of protein regions involved in the interaction of human respiratory syncytial virus phosphoprotein and nucleoprotein: significance for nucleocapsid assembly and formation of cytoplasmic inclusions. J. Virol. 70:801-808.
11. Gilks, N., N. Kedersha, M. Ayodele, L. Shen, G. Stoecklin, L. M. Dember, and P. Anderson. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15:5383-5398.
12. Iseni, F., D. Garcin, M. Nishio, N. Kedersha, P. Anderson, and D. Kolakofsky. 2002. Sendai virus trailer RNA binds TIAR, a cellular protein involved in virus-induced apoptosis. EMBO J. 21:5141-5150.
13. Katsafanas, G. C., and B. Moss. 2007. Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2:221-228.
14. Kedersha, N., and P. Anderson. 2007. Mammalian stress granules and processing bodies. Methods Enzymol. 431:61-81.
15. Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30: 963-969.
16. Kedersha, N., S. Chen, N. Gilks, W. Li, I. J. Miller, J. Stahl, and P. Anderson. 2002. Evidence that ternary complex (eIF2-GTP-tRNA(iMet))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 13:195-210.
17. Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M. J. Fritzler, D. Scheuner, R. J. Kaufman, D. E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871-884. (Pubitemid 41002864)
18. Kedersha, N., S. Tisdale, T. Hickman, and P. Anderson. 2008. Real-time and quantitative imaging of mammalian stress granules and processing bodies. Methods Enzymol. 448:521-552.
19. Kedersha, N. L., M. Gupta, W. Li, I. Miller, and P. Anderson. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 147:1431-1442.
20. Korf, M., D. Jarczak, C. Beger, M. P. Manns, and M. Kruger. 2005. Inhibition of hepatitis C virus translation and subgenomic replication by siRNAs directed against highly conserved HCV sequence and cellular HCV cofactors. J. Hepatol. 43:225-234. (Pubitemid 40956874)
21. Li, D., D. A. Jans, P. G. Bardin, J. Meanger, J. Mills, and R. Ghildyal. 2008. Association of respiratory syncytial virus M protein with viral nucleocapsids is mediated by the M2-1 protein. J. Virol. 82:8863-8870.
22. Li, W., Y. Li, N. Kedersha, P. Anderson, M. Emara, K. M. Swiderek, G. T. Moreno, and M. A. Brinton. 2002. Cell proteins TIA-1 and TIAR interact with the 3′ stem-loop of the West Nile virus complementary minus-strand RNA and facilitate virus replication. J. Virol. 76:11989-12000.
23. Mazroui, R., S. Di Marco, R. J. Kaufman, and I. E. Gallouzi. 2007. Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol. Biol. Cell 18:2603-2618.
24. McInerney, G. M., N. L. Kedersha, R. J. Kaufman, P. Anderson, and P. Liljestrom. 2005. Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16:3753-3763.
25. Mokas, S., J. R. Mills, C. Garreau, M. J. Fournier, F. Robert, P. Arya, R. J. Kaufman, J. Pelletier, and R. Mazroui. 2009. Uncoupling stress granule assembly and translation initiation inhibition. Mol. Biol. Cell 20:2673-2683.
26. Mollet, S., N. Cougot, A. Wilczynska, F. Dautry, M. Kress, E. Bertrand, and D. Weil. 2008. Translationally repressed mRNA transiently cycles through stress granules during stress. Mol. Biol. Cell 19:4469-4479.
27. Montero, H., M. Rojas, C. F. Arias, and S. Lopez. 2008. Rotavirus infection induces the phosphorylation of eIF2alpha but prevents the formation of stress granules. J. Virol. 82:1496-1504.
28. Norrby, E., H. Marusyk, and C. Orvell. 1970. Morphogenesis of respiratory syncytial virus in a green monkey kidney cell line (Vero). J. Virol. 6:237-242.
29. Parker, F., F. Maurier, I. Delumeau, M. Duchesne, D. Faucher, L. Debussche, A. Dugue, F. Schweighoffer, and B. Tocque. 1996. A Ras-GTPase-activating protein SH3-domain-binding protein. Mol. Cell. Biol. 16:2561-2569.
30. Raaben, M., M. J. Groot Koerkamp, P. J. Rottier, and C. A. de Haan. 2007. Mouse hepatitis coronavirus replication induces host translational shutoff and mRNA decay, with concomitant formation of stress granules and processing bodies. Cell Microbiol. 9:2218-2229. (Pubitemid 47250293)
31. Rivas-Aravena, A., P. Ramdohr, M. Vallejos, F. Valiente-Echeverria, V. Dormoy-Raclet, F. Rodriguez, K. Pino, C. Holzmann, J. P. Huidobro-Toro, I. E. Gallouzi, and M. Lopez-Lastra. 2009. The Elav-like protein HuR exerts translational control of viral internal ribosome entry sites. Virology 392:178-185.
32. Santangelo, P., N. Nitin, L. LaConte, A. Woolums, and G. Bao. 2006. Live-cell characterization and analysis of a clinical isolate of bovine respiratory syncytial virus, using molecular beacons. J. Virol. 80:682-688. (Pubitemid 43062881)
33. Santangelo, P. J., A. W. Lifland, P. Curt, Y. Sasaki, G. J. Bassell, M. E. Lindquist, and J. E. Crowe, Jr. 2009. Single molecule-sensitive probes for imaging RNA in live cells. Nat. Methods 6:347-349.
34. Smith, J. A., S. C. Schmechel, A. Raghavan, M. Abelson, C. Reilly, M. G. Katze, R. J. Kaufman, P. R. Bohjanen, and L. A. Schiff. 2006. Reovirus induces and benefits from an integrated cellular stress response. J. Virol. 80:2019-2033.
35. Spangberg, K., L. Wiklund, and S. Schwartz. 2000. HuR, a protein implicated in oncogene and growth factor mRNA decay, binds to the 3′ ends of hepatitis C virus RNA of both polarities. Virology 274:378-390.
36. Spann, K. M., K. C. Tran, B. Chi, R. L. Rabin, and P. L. Collins. 2004. Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J. Virol. 78:4363-4369.
37. Tourriere, H., K. Chebli, L. Zekri, B. Courselaud, J. M. Blanchard, E. Bertrand, and J. Tazi. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160:823-831. (Pubitemid 36350838)
38. Tourriere, H., I. E. Gallouzi, K. Chebli, J. P. Capony, J. Mouaikel, P. van der Geer, and J. Tazi. 2001. RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol. Cell. Biol. 21:7747-7760.
39. White, J. P., A. M. Cardenas, W. E. Marissen, and R. E. Lloyd. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295-305.