Role for subgenomic mRNA in host translation inhibition during Sindbis virus infection of mammalian cells

Virology

Volumn 441, Issue 2, 2013, Pages 171-181

  Patel, Rohini K ^a   Burnham, Andrew J ^a,b   Gebhart, Natasha N ^a   Sokoloski, Kevin J ^a   Hardy, Richard W ^a  

^a INDIANA UNIVERSITY   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Sindbis virus; Subgenomic mRNA; Translation

Indexed keywords

MESSENGER RNA; NUCLEOTIDE; VIRUS PROTEIN;

5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOREDUPLICATION; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENOMICS; MAMMAL CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RNA TRANSLATION; SINDBIS VIRUS; SINDBIS VIRUS INFECTION; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS INFECTION; VIRUS INHIBITION; VIRUS MUTANT;

5' UNTRANSLATED REGIONS; ANIMALS; CELL LINE; CRICETINAE; CULICIDAE; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, VIRAL; SEQUENCE DELETION; SINDBIS VIRUS; VIRAL PLAQUE ASSAY;

MAMMALIA; SINDBIS VIRUS; VERTEBRATA;

EID: 84877921380     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.03.022     Document Type: Article

References (53)

1. Balachandran S., Roberts P.C., et al. Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 2000, 13(1):129-141.
2. Burnham A.J., Gong L., et al. Heterogeneous nuclear ribonuclear protein K interacts with Sindbis virus nonstructural proteins and viral subgenomic mRNA. Virology 2007, 367:212-221.
3. Cancedda R., Villa-Komaroff L., et al. Initiation sites for translation of sindbis virus 42S and 26S messenger RNAs. Cell 1975, 6(2):215-222.
4. Castello A., Sanz M.A., et al. Translation of Sindbis virus 26S mRNA does not require intact eukariotic initiation factor 4G. J. Mol. Biol. 2006, 355(5):942-956.
5. Dar A.C., Dever T.E., et al. Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell 2005, 122(6):887-900.
6. Dever T.E. Gene-specific regulation by general translation factors. Cell 2002, 108(4):545-556.
7. Ding M.X., Schlesinger M.J. Evidence that Sindbis virus NSP2 is an autoprotease which processes the virus nonstructural polyprotein. Virology 1989, 171(1):280-284.
8. Etchison D., Milburn S.C., et al. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J. Biol. Chem. 1982, 257(24):14806-14810.
9. Feigenblum D., Schneider R.J. Modification of eukaryotic initiation factor 4F during infection by influenza virus. J. Virol. 1993, 67(6):3027-3035.
10. Frolov I., Agapov E., et al. Selection of RNA replicons capable of persistent noncytopathic replication in mammalian cells. J. Virol. 1999, 73(5):3854-3865.
11. Frolov I., Hardy R., et al. Cis-acting RNA elements at the 5' end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis. RNA 2001, 7(11):1638-1651.
12. Frolov I., Schlesinger S. Comparison of the effects of Sindbis virus and Sindbis virus replicons on host cell protein synthesis and cytopathogenicity in BHK cells. J. Virol. 1994, 68(3):1721-1727.
13. Frolov I., Schlesinger S. Translation of Sindbis virus mRNA: effects of sequences downstream of the initiating codon. J. Virol. 1994, 68(12):8111-8117.
14. Frolov I., Schlesinger S. Translation of Sindbis virus mRNA: analysis of sequences downstream of the initiating AUG codon that enhance translation. J. Virol. 1996, 70(2):1182-1190.
15. Frolova E.I., Fayzulin R.Z., et al. Roles of nonstructural protein nsP2 and Alpha/Beta interferons in determining the outcome of Sindbis virus infection. J. Virol. 2002, 76(22):11254-11264.
16. Gale M., Tan S.L., et al. Translational control of viral gene expression in eukaryotes. Microbiol. Mol. Biol. Rev. 2000, 64(2):239-280.
17. Garcia-Moreno M., Sanz M.A., et al. Requirements for eIF4A and eIF2 during translation of Sindbis virus subgenomic mRNA in vertebrate and invertebrate host cells. Cell. Microbiol. 2012, [Epub ahead of print]. 10.1111/cmi.12079.
18. Garmashova N., Gorchakov R., et al. Sindbis virus nonstructural protein nsP2 is cytotoxic and inhibits cellular transcription. J. Virol. 2006, 80(12):5686-5696.
19. Gorchakov R., Frolova E., et al. Inhibition of transcription and translation in Sindbis virus-infected cells. J. Virol. 2005, 79(15):9397-9409.
20. Gorchakov R., Frolova E., et al. A new role for ns polyprotein cleavage in Sindbis virus replication. J. Virol. 2008, 82(13):6218-6231.
21. Gorchakov R., Frolova E., et al. PKR-dependent and -independent mechanisms are involved in translational shutoff during Sindbis virus infection. J. Virol. 2004, 78(16):8455-8467.
22. Gradi A., Svitkin Y.V., et al. Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc. Natl. Acad. Sci. USA 1998, 95(19):11089-11094.
23. Green S.R., Mathews M.B. Two RNA-binding motifs in the double-stranded RNA-activated protein kinase, DAI. Genes Dev. 1992, 6(12B):2478-2490.
24. Hahn Y.S., Strauss E.G., et al. Mapping of RNA-temperature-sensitive mutants of Sindbis virus: assignment of complementation groups A, B, and G to nonstructural proteins. J. Virol. 1989, 63(7):3142-3150.
25. Hardy R.W., Rice C.M. Requirements at the 3' end of the sindbis virus genome for efficient synthesis of minus-strand RNA. J. Virol. 2005, 79(8):4630-4639.
26. Hardy W.R., Strauss J.H. Processing the nonstructural polyproteins of sindbis virus: nonstructural proteinase is in the C-terminal half of nsP2 and functions both in cis and in trans. J. Virol. 1989, 63(11):4653-4664.
27. Jang S.K. Internal initiation: IRES elements of picornaviruses and hepatitis c virus. Virus Res. 2006, 119(1):2-15.
28. Kash J.C., Goodman A.G., et al. Hijacking of the host-cell response and translational control during influenza virus infection. Virus Res. 2006, 119(1):111-120.
29. Krausslich H.G., Nicklin M.J., et al. Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4F polypeptide p220. J. Virol. 1987, 61(9):2711-2718.
30. Lemm J.A., Rumenapf T., et al. Polypeptide requirements for assembly of functional Sindbis virus replication complexes: a model for the temporal regulation of minus- and plus-strand RNA synthesis. EMBO J. 1994, 13(12):2925-2934.
31. Levis R., Schlesinger S., et al. Promoter for Sindbis virus RNA-dependent subgenomic RNA transcription. J. Virol. 1990, 64(4):1726-1733.
32. Li M.L., Stollar V. Distinct sites on the Sindbis virus RNA-dependent RNA polymerase for binding to the promoters for the synthesis of genomic and subgenomic RNA. J. Virol. 2007, 81(8):4371-4373.
33. Mayuri, Geders T.W., et al. Role for conserved residues of sindbis virus nonstructural protein 2 methyltransferase-like domain in regulation of minus-strand synthesis and development of cytopathic infection. J. Virol. 2008, 82(15):7284-7297.
34. Raju R., Huang H.V. Analysis of Sindbis virus promoter recognition in vivo, using novel vectors with two subgenomic mRNA promoters. J. Virol. 1991, 65(5):2501-2510.
35. Rice C.M., Levis R., et al. Production of infectious RNA transcripts from Sindbis virus cDNA clones: mapping of lethal mutations, rescue of a temperature-sensitive marker, and in vitro mutagenesis to generate defined mutants. J. Virol. 1987, 61(12):3809-3819.
36. Romano P.R., Garcia-Barrio M.T., et al. Autophosphorylation in the activation loop is required for full kinase activity in vivo of human and yeast eukaryotic initiation factor 2alpha kinases PKR and GCN2. Mol. Cell Biol. 1998, 18(4):2282-2297.
37. Rupp J.C., Jundt N., et al. Requirment for the amino-terminal domain of Sindbis virus nsP4 during virus infection. J. Virol. 2011, 85(7):3449-3460.
38. Russo A.T., White M.A., et al. The crystal structure of the Venezuelan equine encephalitis alphavirus nsP2 protease. Structure 2006, 14(9):1449-1458.
39. Sanz M.A., Castello A., et al. Viral translation is coupled to transcription in sindbis virus-infected cells. J. Virol. 2007, 81(13):7061-7068.
40. Sanz M.A., Castello A., et al. Dual mechanism for the translation of subgenomic mRNA from Sindbis virus in infected and uninfected cells. PLoS One 2009, 4(3):e4772.
41. Shirako Y., Strauss J.H. Regulation of Sindbis virus RNA replication: uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand RNA synthesis. J. Virol. 1994, 68(3):1874-1885.
42. Sokoloski K.J., Hayes C.A., et al. Sindbis virus infectivity improves during the course of infection in both mammalian and mosquito cells. Virus Res. 2012, 167:26-33.
43. Stojdl D.F., Abraham N., et al. The murine double-stranded RNA-dependent protein kinase PKR is required for resistance to vesicular stomatitis virus. J. Virol. 2000, 74(20):9580-9585.
44. Strauss J.H., Strauss E.G. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 1994, 58(3):491-562.
45. Suopanki J., Sawicki D.L., et al. Regulation of alphavirus 26S mRNA transcription by replicase component nsP2. J. Gen. Virol. 1998, 79(Pt 2):309-319.
46. Toribio R., Ventoso I. Inhibition of host translation by virus infection in vivo. Proc. Natl. Acad. Sci. USA 2010, 107(21):9837-9842.
47. van Steeg H., Thomas A., et al. Shutoff of neuroblastoma cell protein synthesis by Semliki Forest virus: loss of ability of crude initiation factors to recognize early Semliki Forest virus and host mRNA's. J. Virol. 1981, 38(2):728-736.
48. van Steeg H., van Grinsven M., et al. Initiation of protein synthesis in neuroblastoma cells infected by Semliki forest virus. A decreased requirement of late viral mRNA for eIF-4B and cap binding protein. FEBS Lett. 1981, 129(1):62-66.
49. Ventoso I. Adaptive changes in alphavirus mRNA translation allowed colonization of vertebrate hosts. J. Virol. 2012, 86(17):9484-9494.
50. Ventoso I., Sanz M.A., et al. Translational resistance of late alphavirus mRNA to eIF2alpha phosphorylation: a strategy to overcome the antiviral effect of protein kinase PKR. Genes Dev. 2006, 20(1):87-100.
51. Weber F., Wagner V., et al. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J. Virol. 2006, 80(10):5059-5064.
52. Wielgosz M.M., Raju R., et al. Sequence requirements for Sindbis virus subgenomic mRNA promoter function in cultured cells. J. Virol. 2001, 75(8):3509-3519.
53. Zhang Y., Feigenblum D., et al. A late adenovirus factor induces eIF-4E dephosphorylation and inhibition of cell protein synthesis. J. Virol. 1994, 68(11):7040-7050.