The nuclear-cytoplasmic shuttling of virion host shutoff RNase is enabled by pUL47 and an embedded nuclear export signal and defines the sites of degradation of AU-rich and stable cellular mRNAs

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13569-13578

  Shu, Minfeng ^a   Taddeo, Brunella ^a   Roizman, Bernard ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; MESSENGER RNA; MUTANT PROTEIN; PROTEIN PUL47; RIBONUCLEASE; UNCLASSIFIED DRUG; URACIL; VIRUS HOST SHUTOFF RNASE; VIRUS RNA;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CODON; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENETIC TRANSFECTION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR EXPORT SIGNAL; POLYSOME; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN TRANSPORT; RNA DEGRADATION; RNA STABILITY; VIRUS CELL INTERACTION;

AT RICH SEQUENCE; CELL NUCLEUS; CYTOPLASM; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; NUCLEAR EXPORT SIGNALS; PROTEIN TRANSPORT; RIBONUCLEASES; RNA STABILITY; RNA, MESSENGER; VIRAL FUSION PROTEINS; VIRAL PROTEINS;

EID: 84888065820     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02603-13     Document Type: Article

References (41)

1. Strom T, Frenkel N. 1987. Effects of herpes simplex virus on mRNA stability. J. Virol. 61:2198-2207.
2. Read GS, Frenkel N. 1983. Herpes simplex virus mutants defective in the virion-associated shutoff of host polypeptide synthesis and exhibiting abnormal synthesis of alpha (immediate early) viral polypeptides. J. Virol. 46:498-512.
3. Kwong AD, Frenkel N. 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.
4. Barzilai A, Zivony-Elbom I, Sarid R, Noah E, Frenkel N. 2006. The herpes simplex virus type 1 vhs-UL41 gene secures viral replication by temporarily evading apoptotic cellular response to infection:vhs-UL41 activity might require interactions with elements of cellular mRNA degradation machinery. J. Virol. 80:505-513.
5. Taddeo B, Roizman B. 2006. The virion host shutoff protein (UL41) of herpes simplex virus 1 is an endoribonuclease with a substrate specificity similar to that of RNase A. J. Virol. 80:9341-9345.
6. Feng P, Everly DN, Jr, Read GS. 2001. mRNA decay during herpesvirus infections:interaction between a putative viral nuclease and a cellular translation factor. J. Virol. 75:10272-10280.
7. Esclatine A, Taddeo B, Evans L, Roizman B. 2004. The herpes simplex virus 1 UL41 gene-dependent destabilization of cellular RNAs is selective and may be sequence-specific. Proc. Natl. Acad. Sci. U.S.A. 101:3603-3608.
8. Taddeo B, Zhang W, Roizman B. 2006. The U(L)41 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.
9. Taddeo B, Sciortino MT, Zhang W, Roizman B. 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.
10. Lam Q, Smibert CA, Koop KE, Lavery C, Capone JP, Weinheimer SP, Smiley JR. 1996. Herpes simplex virus VP16 rescues viral mRNA from destruction by the virion host shutoff function. EMBO J. 15:2575-2581.
11. Shu M, Taddeo B, Zhang W, Roizman B. 2013. Selective degradation of mRNAs by the HSV host shutoff RNase is regulated by the UL47 tegument protein. Proc. Natl. Acad. Sci. U.S.A. 110:E1669-E1675.
12. Taddeo B, Zhang W, Roizman B. 2013. The herpes simplex virus host shutoff RNase degrades cellular and viral mRNAs made before infection but not viral mRNA made after infection. J. Virol. 87:4516-4522.
13. Donnelly M, Verhagen J, Elliott G. 2007. RNA binding by the herpes simplex virus type 1 nucleocytoplasmic shuttling protein UL47 is mediated by an N-terminal arginine-rich domain that also functions as its nuclear localization signal. J. Virol. 81:2283-2296.
14. Dobrikova E, Shveygert M, Walters R, Gromeier M. 2010. Herpes simplex virus proteins ICP27 and UL47 associate with polyadenylatebinding protein and control its subcellular distribution. J. Virol. 84:270-279.
15. Everly DN, Jr, Feng P, Mian IS, Read GS. 2002. mRNA degradation by the virion host shutoff (Vhs) protein of herpes simplex virus:genetic and biochemical evidence that Vhs is a nuclease. J. Virol. 76:8560-8571.
16. Ceska TA, Sayers JR. 1998. Structure-specific DNA cleavage by 5' nucleases. Trends Biochem. Sci. 23:331-336.
17. Ceska TA, Sayers JR, Stier G, Suck D. 1996. A helical arch allowing single-stranded DNA to thread through T5 5'-exonuclease. Nature 382:90-93.
18. Hosfield DJ, Mol CD, Shen B, Tainer JA. 1998. Structure of the DNA repair and replication endonuclease and exonuclease FEN-1:coupling DNA and PCNA binding to FEN-1 activity. Cell 95:135-146.
19. Hwang KY, Baek K, Kim HY, Cho Y. 1998. The crystal structure of flap endonuclease-1 from Methanococcus jannaschii. Nat. Struct. Biol. 5:707-713.
20. Kim Y, Eom SH, Wang J, Lee DS, Suh SW, Steitz TA. 1995. Crystal structure of Thermus aquaticus DNA polymerase. Nature 376:612-616.
21. Mueser TC, Nossal NG, Hyde CC. 1996. Structure of bacteriophage T4 RNase H, a 5' to 3' RNA-DNA and DNA-DNA exonuclease with sequence similarity to the RAD2 family of eukaryotic proteins. Cell 85:1101-1112.
22. Ejercito PM, Kieff ED, Roizman B. 1968. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J. Gen. Virol. 2:357-364.
23. Wang X, Patenode C, Roizman B. 2011. US3 protein kinase of HSV-1 cycles between the cytoplasm and nucleus and interacts with programmed cell death protein 4 (PDCD4) to block apoptosis. Proc. Natl. Acad. Sci. U.S.A. 108:14632-14636.
24. Roller RJ, Roizman B. 1992. The herpes simplex virus 1 RNA binding protein US11 is a virion component and associates with ribosomal 60S subunits. J. Virol. 66:3624-3632.
25. Kalamvoki M, Roizman B. 2010. Circadian CLOCK histone acetyl transferase localizes at ND10 nuclear bodies and enables herpes simplex virus gene expression. Proc. Natl. Acad. Sci. U.S.A. 107:17721-17726.
26. Sugiura T, Yamaguchi A, Miyamoto K. 2008. A cancer-associated RING finger protein, RNF43, is a ubiquitin ligase that interacts with a nuclear protein, HAP95. Exp. Cell Res. 314:1519-1528.
27. He B, Gross M, Roizman B. 1997. The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by doublestranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 94:843-848.
28. Esclatine A, Taddeo B, Roizman B. 2004. The UL41 protein of herpes simplex virus mediates selective stabilization or degradation of cellular mRNAs. Proc. Natl. Acad. Sci. U.S.A. 101:18165-18170.
29. van Lint AL, Murawski MR, Goodbody RE, Severa M, Fitzgerald KA, Finberg RW, Knipe DM, Kurt-Jones EA. 2010. Herpes simplex virus immediate-early ICP0 protein inhibits Toll-like receptor 2-dependent inflammatory responses and NF-kappaB signaling. J. Virol. 84:10802-10811.
30. Sciortino MT, Suzuki M, Taddeo B, Roizman B. 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.
31. Sciortino MT, Taddeo B, Poon AP, Mastino A, Roizman B. 2002. Of the three tegument proteins that package mRNA in herpes simplex virions, one (VP22) transports the mRNA to uninfected cells for expression prior to viral infection. Proc. Natl. Acad. Sci. U.S.A. 99:8318-8323.
32. Kwong AD, Kruper JA, Frenkel N. 1988. Herpes simplex virus virion host shutoff function. J. Virol. 62:912-921.
33. Kwong AD, Frenkel N. 1989. The herpes simplex virus virion host shutoff function. J. Virol. 63:4834-4839.
34. Hudson BP, Martinez-Yamout MA, Dyson HJ, Wright PE. 2004. Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat. Struct. Mol. Biol. 11:257-264.
35. Lai WS, Kennington EA, Blackshear PJ. 2003. Tristetraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNAs by poly(A) ribonuclease. Mol. Cell. Biol. 23:3798-3812.
36. Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ. 2000. Interactions of CCCH zinc finger proteins with mRNA:binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA. J. Biol. Chem. 275:17827-17837.
37. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ. 1999. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol. Cell. Biol. 19:4311-4323.
38. Taddeo B, Zhang W, Roizman B. 2010. Role of herpes simplex virus ICP27 in the degradation of mRNA by virion host shutoff RNase. J. Virol. 84:10182-10190.
39. Taddeo B, Zhang W, Roizman B. 2009. The virion-packaged endoribonuclease of herpes simplex virus 1 cleaves mRNA in polyribosomes. Proc. Natl. Acad. Sci. U.S.A. 106:12139-12144.
40. Esclatine A, Taddeo B, Roizman B. 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.
41. Corcoran JA, Hsu WL, Smiley JR. 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.