Role of herpes simplex virus ICP27 in the degradation of mRNA by virion host shutoff RNase

Journal of Virology

Volumn 84, Issue 19, 2010, Pages 10182-10190

  Taddeo, Brunella ^a   Zhang, Weiran ^a   Roizman, Bernard ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ICP27 PROTEIN; MESSENGER RNA; PROTEIN VP16; PROTEIN VP22; RIBONUCLEASE; UNCLASSIFIED DRUG; VIRION HOST SHUTOFF RIBONUCLEASE; VIRUS PROTEIN; ICP27 PROTEIN, HUMAN HERPESVIRUS 1; IMMEDIATE EARLY PROTEIN; PRIMER DNA; VIRION HOST SHUTOFF PROTEIN, SIMPLEXVIRUS; VIRUS RNA;

3' UNTRANSLATED REGION; ARTICLE; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; RNA ISOLATION; WILD TYPE; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; GENETIC COMPLEMENTATION; GENETICS; HELA CELL LINE; HERPES SIMPLEX VIRUS 1; HOST PATHOGEN INTERACTION; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RNA STABILITY; VERO CELL LINE; VIRUS ASSEMBLY; VIRUS GENE;

SIMPLEXVIRUS;

ANIMALS; BASE SEQUENCE; CELL LINE; CERCOPITHECUS AETHIOPS; DNA PRIMERS; GENES, VIRAL; GENETIC COMPLEMENTATION TEST; HELA CELLS; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; MUTATION; RIBONUCLEASES; RNA STABILITY; RNA, MESSENGER; RNA, VIRAL; VERO CELLS; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 77956864901     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00975-10     Document Type: Article

References (52)

1. Bakheet, T., B. R. Williams, and K. S. Khabar. 2003. ARED 2.0: an update of AU-rich element mRNA database. Nucleic Acids Res. 31:421-423.
2. L49 gene products. J. Biol. Chem. 269:17401-17410.
3. Brooks, S. A., J. E. Connolly, and W. F. Rigby. 2004. The role of mRNA turnover in the regulation of tristetraprolin expression: evidence for an extracellular signal-regulated kinase-specific, AU-rich element-dependent, autoregulatory pathway. J. Immunol. 172:7263-7271.
4. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
5. Chen, C. Y., R. Gherzi, S. E. Ong, E. L. Chan, R. Raijmakers, G. J. Pruijn, G. Stoecklin, C. Moroni, M. Mann, and M. Karin. 2001. AU-binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451-464.
6. Corcoran, J. A., W. L. Hsu, and J. R. Smiley. 2006. Herpes simplex virus ICP27 is required for virus-induced stabilization of the ARE-containing IEX-1 mRNA encoded by the human IER3 gene. J. Virol. 80:9720-9729.
7. DeLuca, N. A., A. McCarthy, and P. A. Schaffer. 1985. Isolation and characterization of deletion mutants of herpes simplex virus type 1 in the gene encoding immediate-early regulatory protein ICP4. J. Virol. 56:558-570.
8. Dobrikova, E., M. Shveygert, R. Walters, and M. Gromeier. 2010. Herpes simplex virus proteins ICP27 and UL47 associate with polyadenylate-binding protein and control its subcellular distribution. J. Virol. 84:270-279.
9. Doepker, R. C., W. L. Hsu, H. A. Saffran, and J. R. Smiley. 2004. Herpes simplex virus virion host shutoff protein is stimulated by translation initiation factors eIF4B and eIF4H. J. Virol. 78:4684-4699.
10. Ejercito, P. M., E. D. Kieff, and B. Roizman. 1968. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J. Gen. Virol. 2:357-364.
11. Elgadi, M. M., C. E. Hayes, and J. R. Smiley. 1999. The herpes simplex virus vhs protein induces endoribonucleolytic cleavage of target RNAs in cell extracts. J. Virol. 73:7153-7164.
12. Elgadi, M. M., and J. R. Smiley. 1999. Picornavirus internal ribosome entry site elements target RNA cleavage events induced by the herpes simplex virus virion host shutoff protein. J. Virol. 73:9222-9231.
13. Ellison, K. S., R. A. Maranchuck, K. L. Mottet, and J. R. Smiley. 2005. Control of VP16 translation by the herpes simplex virus type 1 immediate-early protein ICP27. J. Virol. 79:4120-4131.
14. L41 gene-dependent destabilization of cellular RNAs is selective and may be sequence-specific. Proc. Natl. Acad. Sci. U. S. A. 101:3603-3608.
15. Esclatine, A., B. Taddeo, and B. Roizman. 2004. Herpes simplex virus 1 induces cytoplasmic accumulation of TIA-1/TIAR and both synthesis and cytoplasmic accumulation of tristetraprolin, two cellular proteins that bind and destabilize AU-rich RNAs. J. Virol. 78:8582-8592. (Pubitemid 39025124)
16. L41 protein of herpes simplex virus mediates selective stabilization or degradation of cellular mRNAs. Proc. Natl. Acad. Sci. U. S. A. 101:18165-18170.
17. L41 is a nuclease. J. Virol. 76:8560-8571.
18. Feng, P., D. N. Everly, Jr., and G. S. Read. 2001. mRNA decay during herpesvirus infections: interaction between a putative viral nuclease and a cellular translation factor. J. Virol. 75:10272-10280.
19. Feng, P., D. N. Everly, Jr., and G. S. Read. 2005. mRNA decay during herpes simplex virus (HSV) infections: protein-protein interactions involving the HSV virion host shutoff protein and translation factors eIF4H and eIF4A. J. Virol. 79:9651-9664.
20. Fontaine-Rodriguez, E. C., T. J. Taylor, M. Olesky, and D. M. Knipe. 2004. Proteomics of herpes simplex virus infected cell protein 27: association with translation initiation factors. Virology 330:487-492.
21. Fontaine-Rodriguez, E. C., and D. M. Knipe. 2008. Herpes simplex virus ICP27 increases translation of a subset of viral late mRNAs. J. Virol. 82: 3538-3545.
22. Jones, F. E., C. A. Smibert, and J. R. Smiley. 1995. Mutational analysis of the herpes simplex virus virion host shutoff protein: evidence that vhs functions in the absence of other viral proteins. J. Virol. 69:4863-4871.
23. Krikorian, C. R., and G. S. Read. 1991. In vitro mRNA degradation system to study the virion host shutoff function of herpes simplex virus. J. Virol. 65:112-122.
24. Kwong, A. D., and N. Frenkel. 1987. Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc. Natl. Acad. Sci. U. S. A. 84:1926-1930.
25. Kwong, A. D., J. A. Kruper, and N. Frenkel. 1988. Herpes simplex virus virion host shutoff function. J. Virol. 62:912-921.
26. Kwong, A. D., and N. Frenkel. 1989. The herpes simplex virus virion host shutoff function. J. Virol. 63:4834-4839.
27. Lam, Q., C. A. Smibert, K. E. Koop, C. Lavery, J. P. Capone, S. P. Weinheimer, and J. R. Smiley. 1996. Herpes simplex virus VP16 rescues viral mRNA from destruction by the virion host shutoff function. EMBO J. 15: 2575-2581.
28. Lykke-Andersen, J., and E. Wagner. 2005. Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev. 19:351-361.
29. Oroskar, A. A., and G. S. Read. 1987. A mutant of herpes simplex virus type 1 exhibits increased stability of immediate-early (alpha) mRNAs. J. Virol. 61:604-606.
30. Oroskar, A. A., and G. S. Read. 1989. Control of mRNA stability by the virion host shutoff function of herpes simplex virus. J. Virol. 63:1897-1906.
31. L41) of herpes simplex virus interacts with the cellular capbinding complex eIF4F. J. Virol. doi:10.1128/JVI.00166-10.
32. Pak, A. S., D. N. Everly, K. Knight, and G. S. Read. 1995. The virion host shutoff protein of herpes simplex virus inhibits reporter gene expression in the absence of other viral gene products. Virology 211:491-506.
33. 134.5 genes of herpes simplex virus 1. Virology 229:98-105.
34. L41) polypeptide. J. Virol. 67:7149-7160.
35. S11 is a virion component and associates with ribosomal 60S subunits. J. Virol. 66:3624-3632.
36. Schek, N., and S. L. Bachenheimer. 1985. Degradation of cellular mRNAs induced by a virion-associated factor during herpes simplex virus infection of Vero cells. J. Virol. 55:601-610.
37. Sciortino, M. T., M. Suzuki, B. Taddeo, and B. Roizman. 2001. RNAs extracted from herpes simplex virus 1 virions: apparent selectivity of viral but not cellular RNAs packaged in virions. J. Virol. 75:8105-8116.
38. Smibert, C. A., B. Popova, P. Xiao, J. P. Capone, and J. R. Smiley. 1994. Herpes simplex virus VP16 forms a complex with the virion host shutoff protein vhs. J. Virol. 68:2339-2346.
39. Smiley, J. R. 2004. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? J. Virol. 78:1063-1068.
40. Soliman, T. M., R. M. Sandri-Goldin, and S. J. Silverstein. 1997. Shuttling of the herpes simplex virus type 1 regulatory protein ICP27 between the nucleus and the cytoplasm mediates the expression of late proteins. J. Virol. 71:9188-9197.
41. Soreson, C. M., P. A. Hart, and J. Ross. 1991. Analysis of herpes simplex virus-induced mRNA destabilizing activity using an in vitro mRNA decay system. Nucleic Acid Res. 19:4459-4465.
42. Spear, P. G., and B. Roizman. 1972. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpes virion. J. Virol. 9:143-159.
43. Strom, T., and N. Frenkel. 1987. Effects of herpes simplex virus on mRNA stability. J. Virol. 61:2198-2207. (Pubitemid 17088933)
44. Taddeo, B., A. Esclatine, W. Zhang, and B. Roizman. 2003. The stress-inducible immediate-early responsive gene IEX-1 is activated in cells infected with herpes simplex virus 1, but several viral mechanisms, including 3′ degradation of its RNA, preclude expression of the gene. J. Virol. 77:6178-6187.
45. Taddeo, B., A. Esclatine, and B. Roizman. 2004. Post-transcriptional processing of cellular RNAs in herpes simplex virus-infected cells. Biochem. Soc Trans. 32:697-701.
46. Taddeo, B., W. Zhang, and B. Roizman. 2006. The UL41 protein of herpes simplex virus 1 degrades RNA by endonucleolytic cleavage in absence of other cellular or viral proteins. Proc. Natl. Acad. Sci. U. S. A. 103:2827-2832.
47. L41) of herpes simplex virus 1 is an endoribonuclease with a substrate specificity similar to that of RNase A. J. Virol. 80:9341-9345.
48. Taddeo, B., M. T. Sciortino, W. Zhang, and B. Roizman. 2007. Interaction of herpes simplex virus RNase with VP16 and VP22 is required for the accumulation of the protein but not for accumulation of mRNA. Proc. Natl. Acad. Sci. U. S. A. 104:12163-12168.
49. Taddeo, B., W. Zhang, and B. Roizman. 2009. The virion-packaged endoribonuclease of herpes simplex virus 1 cleaves mRNA in polyribosomes. Proc. Natl. Acad. Sci. U. S. A. 106:12139-12144.
50. Ward, P. L., W. O. Ogle, and B. Roizman. 1996. Assemblons: nuclear structure defined by aggregation of immature capsids and some tegument proteins of herpes simplex virus 1. J. Virol. 70:4623-4631.
51. Wilusz, C. J., M. Wormington, and S. W. Peltz. 2001. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2:237-246.
52. Zelus, B. D., R. S. Stewart, and J. Ross. 1996. The virion host shutoff protein of herpes simplex virus type 1: messenger ribonucleolytic activity in vitro. J. Virol. 70:2411-2419.