Poliovirus unlinks TIA1 aggregation and mRNA stress granule formation

Journal of Virology

Volumn 85, Issue 23, 2011, Pages 12442-12454

  White, James P ^a   Lloyd, Richard E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; INITIATION FACTOR 3; INITIATION FACTOR 3A; INITIATION FACTOR 4B; MESSENGER RNA; RASGAP SH3 DOMAIN BINDING PROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; T CELL RESTRICTED INTRACELLULAR ANTIGEN 1; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HEAT SHOCK; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; OXIDATIVE STRESS; POLIOMYELITIS VIRUS; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STRESS GRANULE; VIRUS CELL INTERACTION;

BLOTTING, WESTERN; CYTOPLASM; CYTOPLASMIC GRANULES; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; IN SITU HYBRIDIZATION; OXIDATIVE STRESS; PEPTIDE INITIATION FACTORS; POLIOMYELITIS; POLIOVIRUS; POLY(A)-BINDING PROTEINS; PROTEIN BIOSYNTHESIS; RNA PROBES; RNA, MESSENGER; RNA-BINDING PROTEINS;

MAMMALIA; POLIOVIRUS;

EID: 81255123305     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05888-11     Document Type: Article

References (57)

1. Baguet, A., et al. 2007. The exon-junction-complex-component metastatic lymph node 51 functions in stress-granule assembly. J. Cell Sci. 120: 2774-2784.
2. Blyn, L. B., J. S. Towner, B. L. Semler, and E. Ehrenfeld. 1997. Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. J. Virol. 71: 6243-6246.
3. Borghese, F., and T. Michiels. 2011. The leader protein of cardioviruses inhibits stress granule assembly. J. Virol. 85: 9614-9622.
4. Boussadia, O., et al. 2003. Unr is required in vivo for efficient initiation of translation from the internal ribosome entry sites of both rhinovirus and poliovirus. J. Virol. 77: 3353-3359.
5. Buchan, J. R., and R. Parker. 2009. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36: 932-941.
6. Buchan, J. R., J. H. Yoon, and R. Parker. 2011. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J. Cell Sci. 124: 228-239.
7. Byrd, M. P., M. Zamora, and R. E. Lloyd. 2005. Translation of eukaryotic translation initiation factor 4GI (eIF4GI) proceeds from multiple mRNAs containing a novel cap-dependent internal ribosome entry site (IRES) that is active during poliovirus infection. J. Biol. Chem. 280: 18610-18622.
8. Chernov, K. G., et al. 2009. Role of microtubules in stress granule assembly: microtubule dynamical instability favors the formation of micrometric stress granules in cells. J. Biol. Chem. 284: 36569-36580.
9. Choe, S. S., D. A. Dodd, and K. Kirkegaard. 2005. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 337: 18-29.
10. Clark, M. E., T. Hammerle, E. Wimmer, and A. Dasgupta. 1991. Poliovirus proteinase 3C converts an active form of transcription factor IIIC to an inactive form: a mechanism for inhibition of host cell polymerase III transcription by poliovirus. EMBO J. 10: 2941-2947.
11. Clark, M. E., P. M. Lieberman, A. J. Berk, and A. Dasgupta. 1993. Direct cleavage of human TATA-binding protein by poliovirus protease 3C in vivo and in vitro. Mol. Cell. Biol. 13: 1232-1237.
12. Dang, Y., et al. 2006. Eukaryotic initiation factor 2alpha-independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 281: 32870-32878.
13. de Breyne, S., Y. Yu, A. Unbehaun, T. V. Pestova, and C. U. Hellen. 2009. Direct functional interaction of initiation factor eIF4G with type 1 internal ribosomal entry sites. Proc. Natl. Acad. Sci. U. S. A. 106: 9197-9202.
14. Dodd, D. A., T. H. Giddings, Jr., and K. Kirkegaard. 2001. Poliovirus 3A protein limits interleukin-6 (IL-6), IL-8, and beta interferon secretion during viral infection. J. Virol. 75: 8158-8165.
15. Fitzgerald, K. D., and B. L. Semler. 2009. Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim. Biophys. Acta 1789: 518-528.
16. Fujimura, K., F. Kano, and M. Murata. 2008. Identification of PCBP2, a facilitator of IRES-mediated translation, as a novel constituent of stress granules and processing bodies. RNA 14: 425-431.
17. Gilks, N., et al. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15: 5383-5398.
18. Gustin, K. E., and P. Sarnow. 2001. Effects of poliovirus infection on nucleocytoplasmic trafficking and nuclear pore complex composition. EMBO J. 20: 240-249.
19. Hellen, C. U. T., et al. 1993. A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein. Proc. Natl. Acad. Sci. U. S. A. 90: 7642-7646.
20. Ivanov, P. A., E. M. Chudinova, and E. S. Nadezhdina. 2003. Disruption of microtubules inhibits cytoplasmic ribonucleoprotein stress granule formation. Exp. Cell Res. 290: 227-233.
21. Jones, C., and E. Ehrenfeld. 1983. The effect of poliovirus infection on the translation in vitro of VSV messenger ribonucleoprotein particles. Virology 129: 415-430.
22. Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30: 963-969.
23. Kedersha, N., et al. 2002. Evidence that ternary complex (eIF2-GTPtRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 13: 195-210.
24. Kedersha, N., et al. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169: 871-884.
25. Kedersha, N. L., M. Gupta, W. Li, I. Miller, and P. Anderson. 1999. RNAbinding 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.
26. Kim, W. J., J. H. Kim, and S. K. Jang. 2007. Anti-inflammatory lipid mediator 15d-PGJ2 inhibits translation through inactivation of eIF4A. EMBO J. 26: 5020-5032.
27. Kimball, S. R., R. L. Horetsky, D. Ron, L. S. Jefferson, and H. P. Harding. 2003. Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am. J. Physiol. Cell Physiol. 284: C273-C284.
28. Kondratova, A. A., N. Neznanov, R. V. Kondratov, and A. V. Gudkov. 2005. Poliovirus protein 3A binds and inactivates LIS1, causing block of membrane protein trafficking and deregulation of cell division. Cell Cycle 4: 1403-1410.
29. Kuyumcu-Martinez, M., et al. 2004. Calicivirus 3C-like proteinase inhibits cellular translation by cleavage of poly(A)-binding protein. J. Virol. 78: 8172-8182.
30. Kwon, S., Y. Zhang, and P. Matthias. 2007. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 21: 3381-3394.
31. Lindquist, M. E., A. W. Lifland, T. J. Utley, P. J. Santangelo, and J. E. Crowe, Jr. 2010. Respiratory syncytial virus induces host RNA stress granules to facilitate viral replication. J. Virol. 84: 12274-12284.
32. Lloyd, R. 2006. Translational control by viral proteinases. Virus Res. 119: 76-88.
33. Loschi, M., C. C. Leishman, N. Berardone, and G. L. Boccaccio. 2009. Dynein and kinesin regulate stress-granule and P-body dynamics. J. Cell Sci. 122: 3973-3982.
34. Mazroui, R., et al. 2006. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol. Biol. Cell 17: 4212-4219.
35. McEwen, E., et al. 2005. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J. Biol. Chem. 280: 16925-16933.
36. McInerney, G. M., N. L. Kedersha, R. J. Kaufman, P. Anderson, and P. Liljeström. 2005. Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16: 3753-3763.
37. Meerovitch, K., et al. 1993. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J. Virol. 67: 3798-3807.
38. 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.
39. Nonhoff, U., et al. 2007. Ataxin-2 interacts with the DEAD/H-box RNA helicase DDX6 and interferes with P-bodies and stress granules. Mol. Biol. Cell 18: 1385-1396.
40. Ochs, K., et al. 2002. Interaction of translation initiation factor eIF4B with the poliovirus internal ribosome entry site. J. Virol. 76: 2113-2122.
41. O'Neill, R. E., and V. R. Racaniello. 1989. Inhibition of translation in cells infected with a poliovirus 2Apro mutant correlates with phosphorylation of the alpha subunit of eucaryotic initiation factor 2. J. Virol. 63: 5069-5075.
42. Pacheco, A., and E. Martinez-Salas. 2010. Insights into the biology of IRES elements through riboproteomic approaches. J. Biomed. Biotechnol. 2010: 458927.
43. Park, N., P. Katikaneni, T. Skern, and K. E. Gustin. 2008. Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J. Virol. 82: 1647-1655.
44. Piotrowska, J., et al. 2010. Stable formation of compositionally unique stress granules in virus-infected cells. J. Virol. 84: 3654-3665.
45. Qin, Q., K. Carroll, C. Hastings, and C. L. Miller. 2011. Mammalian orthoreovirus escape from host translational shutoff correlates with stress granule disruption and is independent of eIF2alpha phosphorylation and PKR. J. Virol. 85: 8798-8810.
46. 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.
47. Rozovics, J. M., and B. L. Semler. 2010. Genome replication. I. The players, p. 107-125. In E. Ehrenfeld, E. Domingo, and R. P. Roos (ed), The picornaviruses. ASM Press, Washington, DC.
48. Smith, J. A., et al. 2006. Reovirus induces and benefits from an integrated cellular stress response. J. Virol. 80: 2019-2033.
49. Sola, I., et al. 2011. The polypyrimidine tract-binding protein affects coronavirus RNA accumulation levels and relocalizes viral RNAs to novel cytoplasmic domains different from replication-transcription sites. J. Virol. 85: 5136-5149.
50. Stoecklin, G., et al. 2004. MK2-induced tristetraprolin: 14-13-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J. 23: 1313-1324.
51. Tolskaya, E. A., et al. 1994. Genetic studies on the poliovirus 2C protein, an NTPase. A plausible mechanism of guanidine effect on the 2C function and evidence for the importance of 2C oligomerization. J. Mol. Biol. 236: 1310-1323.
52. Tourriere, H., et al. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160: 823-831.
53. Tsai, N. P., P. C. Ho, and L. N. Wei. 2008. Regulation of stress granule dynamics by Grb7 and FAK signalling pathway. EMBO J. 27: 715-726.
54. Tsai, N. P., Y. C. Tsui, and L. N. Wei. 2009. Dynein motor contributes to stress granule dynamics in primary neurons. Neuroscience 159: 647-656.
55. 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.
56. White, J. P., L. C. Reineke, and R. E. Lloyd. 2011. Poliovirus switches to an eIF2-independent mode of translation during infection. J. Virol. 85: 8884-8893.
57. Yalamanchili, P., U. Datta, and A. Dasgupta. 1997. Inhibition of host cell transcription by poliovirus: cleavage of transcription factor CREB by poliovirus-encoded protease 3Cpro. J. Virol. 71: 1220-1226.