Herpes simplex virus 2 infection impacts stress granule accumulation

Journal of Virology

Volumn 86, Issue 15, 2012, Pages 8119-8130

  Finnen, Renée L ^a   Pangka, Kyle R ^a   Banfield, Bruce W ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2ALPHA; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN SAM68; PROTEIN SH3; RAS PROTEIN; RNA BINDING PROTEIN; T CELL INTERNAL ANTIGEN 1 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA;

ANIMAL CELL; ARTICLE; CELL DISRUPTION; CELL GRANULE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA REPLICATION; DOWN REGULATION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; MITOSIS; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TRANSLATION INITIATION; VIRUS REPLICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; CYTOPLASMIC GRANULES; DNA REPLICATION; DNA, VIRAL; DNA-BINDING PROTEINS; EPOXY COMPOUNDS; EUKARYOTIC INITIATION FACTOR-2; HELA CELLS; HERPES GENITALIS; HERPESVIRUS 2, HUMAN; HUMANS; MACROLIDES; PHOSPHORYLATION; POLY(A)-BINDING PROTEINS; RNA-BINDING PROTEINS; THIAZOLES; VERO CELLS; VIRUS REPLICATION;

EUKARYOTA; HUMAN HERPESVIRUS 2;

EID: 84864387040     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00313-12     Document Type: Article

References (67)

1. Abrahamyan LG, et al. 2010. Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA. J. Cell Sci. 123:369-383.
2. Alvarez E, Castello A, Menendez-Arias L, Carrasco L. 2006. HIV protease cleaves poly(A)-binding protein. Biochem. J. 396:219-226.
3. Anderson P, Kedersha N. 2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33:141-150.
4. Ariumi Y, et al. 2011. Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. J. Virol. 85:6882-6892.
5. Beckham CJ, Parker R. 2008. P bodies, stress granules, and viral life cycles. Cell Host Microbe 3:206-212.
6. Bordeleau ME, et al. 2006. RNA-mediated sequestration of the RNA helicase eIF4A by pateamine A inhibits translation initiation. Chem. Biol. 13:1287-1295.
7. Bordeleau ME, et al. 2005. Stimulation of mammalian translation initiation factor eIF4A activity by a small molecule inhibitor of eukaryotic translation. Proc. Natl. Acad. Sci. U. S. A. 102:10460-10465.
8. Bresnahan WA, Hultman GE, Shenk T. 2000. Replication of wild-type and mutant human cytomegalovirus in life-extended human diploid fibroblasts. J. Virol. 74:10816-10818.
9. Busa R, Geremia R, Sette C. 2010. Genotoxic stress causes the accumulation of the splicing regulator Sam68 in nuclear foci of transcriptionally active chromatin. Nucleic Acids Res. 38:3005-3018.
10. Busa R, et al. 2007. The RNA-binding protein Sam68 contributes to proliferation and survival of human prostate cancer cells. Oncogene 26: 4372-4382.
11. Cassady KA, Gross M. 2002. The herpes simplex virus type 1 U(S)11 protein interacts with protein kinase R in infected cells and requires a 30-amino-acid sequence adjacent to a kinase substrate domain. J. Virol. 76:2029-2035.
12. Cassady KA, Gross M, Roizman B. 1998. The herpes simplex virus US11 protein effectively compensates for the γ1(34.5) gene if present before activation of protein kinase R by precluding its phosphorylation and that of the alpha subunit of eukaryotic translation initiation factor 2. J. Virol. 72:8620-8626.
13. Chen T, Boisvert FM, Bazett-Jones DP, Richard S. 1999. A role for the GSG domain in localizing Sam68 to novel nuclear structures in cancer cell lines. Mol. Biol. Cell 10:3015-3033.
14. Cheng G, Feng Z, He B. 2005. Herpes simplex virus 1 infection activates the endoplasmic reticulum resident kinase PERK and mediates eIF-2α dephosphorylation by the γ(1)34.5 protein. J. Virol. 79:1379-1388.
15. Cheng G, Yang K, He B. 2003. Dephosphorylation of eIF-2α mediated by the γ(1)34.5 protein of herpes simplex virus type 1 is required for viral response to interferon but is not sufficient for efficient viral replication. J. Virol. 77:10154-10161.
16. -mutants of herpes simplex virus 1. Proc. Natl. Acad. Sci. U. S. A. 92:10516-10520.
17. Dauber B, Pelletier J, Smiley JR. 2011. The herpes simplex virus 1 vhs protein enhances translation of viral true late mRNAs and virus production in a cell type-dependent manner. J. Virol. 85:5363-5373.
18. Del Gatto-Konczak F, et al. 2000. The RNA-binding protein TIA-1 is a novel mammalian splicing regulator acting through intron sequences adjacent to a 5' splice site. Mol. Cell. Biol. 20:6287-6299.
19. Duncan RF, Hershey JW. 1987. Translational repression by chemical inducers of the stress response occurs by different pathways. Arch. Biochem. Biophys. 256:651-661.
20. Emara MM, Brinton MA. 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.
21. 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.
22. Everett RD, Fenwick ML. 1990. Comparative DNA sequence analysis of the host shutoff genes of different strains of herpes simplex virus: type 2 strain HG52 encodes a truncated UL41 product. J. Gen. Virol. 71(Pt 6): 1387-1390.
23. Everly DN, Jr, Read GS. 1999. Site-directed mutagenesis of the virion host shutoff gene (UL41) of herpes simplex virus (HSV): analysis of functional differences betweenHSVtype 1 (HSV-1) and HSV-2 alleles. J. Virol. 73:9117-9129.
24. Finnen RL, Roy BB, Zhang H, Banfield BW. 2010. Analysis of filamentous process induction and nuclear localization properties of the HSV-2 serine/threonine kinase Us3. Virology 397:23-33.
25. Forch P, et al. 2000. The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol. Cell 6:1089-1098.
26. Gilks N, et al. 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15:5383-5398.
27. He B, Gross M, Roizman B. 1997. The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1α to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNAactivated protein kinase. Proc. Natl. Acad. Sci. U. S. A. 94:843-848.
28. Henao-Mejia J, He JJ. 2009. Sam68 relocalization into stress granules in response to oxidative stress through complexing with TIA-1. Exp. Cell Res. 315:3381-3395.
29. Henao-Mejia J, et al. 2009. Suppression of HIV-1 Nef translation by Sam68 mutant-induced stress granules and nef mRNA sequestration. Mol. Cell 33:87-96.
30. Honess RW, Roizman B. 1974. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J. Virol. 14:8-19.
31. Huang S. 2000. Review: perinucleolar structures. J. Struct. Biol. 129:233-240.
32. Johnson DC, Baines JD. 2011. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 9:382-394.
33. Jones FE, Smibert CA, Smiley JR. 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.
34. Kedersha N, et al. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151: 1257-1268.
35. Kedersha NL, Gupta M, Li W, Miller I, Anderson P. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2α to the assembly of mammalian stress granules. J. Cell Biol. 147:1431-1442.
36. Koster M, Frahm T, Hauser H. 2005. Nucleocytoplasmic shuttling revealed by FRAP and FLIP technologies. Curr. Opin. Biotechnol. 16:28-34.
37. Langland JO, Cameron JM, Heck MC, Jancovich JK, Jacobs BL. 2006. Inhibition of PKR by RNA and DNA viruses. Virus Res. 119:100-110.
38. Legros S, et al. 2011. The HTLV-1 Tax protein inhibits formation of stress granules by interacting with histone deacetylase 6. Oncogene 30:4050-4062.
39. Li W, et al. 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.
40. Lieu PT, Wagner EK. 2000. Two leaky-late HSV-1 promoters differ significantly in structural architecture. Virology 272:191-203.
41. Lindqvist L, et al. 2008. Selective pharmacological targeting of a DEAD box RNA helicase. PLoS One 3:e1583. doi:10.1371/journal.pone.0001583.
42. Low WK, et al. 2005. Inhibition of eukaryotic translation initiation by the marine natural product pateamine A. Mol. Cell 20:709-722.
43. Lu L, Han AP, Chen JJ. 2001. Translation initiation control by heme-regulated eukaryotic initiation factor 2α kinase in erythroid cells under cytoplasmic stresses. Mol. Cell. Biol. 21:7971-7980.
44. Lukong KE, Richard S. 2003. Sam68, the KH domain-containing super-STAR. Biochim. Biophys. Acta 1653:73-86.
45. Mao JC, Robishaw EE. 1975. Mode of inhibition of herpes simplex virus DNA polymerase by phosphonoacetate. Biochemistry 14:5475-5479.
46. Martin TE, Barghusen SC, Leser GP, Spear PG. 1987. Redistribution of nuclear ribonucleoprotein antigens during herpes simplex virus infection. J. Cell Biol. 105:2069-2082.
47. Matter N, Herrlich P, Konig H. 2002. Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature 420:691-695.
48. Mazroui R, et al. 2006. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2α phosphorylation. Mol. Biol. Cell 17:4212-4219.
49. 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.
50. McInerney GM, Kedersha NL, Kaufman RJ, Anderson P, Liljestrom P. 2005. Importance of eIF2α phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16:3753-3763.
51. Monier K, Armas JC, Etteldorf S, Ghazal P, Sullivan KF. 2000. Annexation of the interchromosomal space during viral infection. Nat. Cell Biol. 2:661-665.
52. Montero H, Trujillo-Alonso V. 2011. Stress granules in the viral replication cycle. Viruses 3:2328-2338.
53. Mulvey M, Arias C, Mohr I. 2007. Maintenance of endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor. J. Virol. 81:3377-3390.
54. Mulvey M, Arias C, Mohr I. 2006. Resistance of mRNA translation to acute endoplasmic reticulum stress-inducing agents in herpes simplex virus type 1-infected cells requires multiple virus-encoded functions. J. Virol. 80:7354-7363.
55. Parsyan A, et al. 2011. mRNA helicases: the tacticians of translational control. Nat. Rev. Mol. Cell. Biol. 12:235-245.
56. Piotrowska J, et al. 2010. Stable formation of compositionally unique stress granules in virus-infected cells. J. Virol. 84:3654-3665.
57. Qin Q, Hastings C, Miller CL. 2009. Mammalian orthoreovirus particles induce and are recruited into stress granules at early times postinfection. J. Virol. 83:11090-11101.
58. Rothe F, Gueydan C, Bellefroid E, Huez G, Kruys V. 2006. Identification of FUSE-binding proteins as interacting partners of TIA proteins. Biochem. Biophys. Res. Commun. 343:57-68.
59. Schneider RJ, Mohr I. 2003. Translation initiation and viral tricks. Trends Biochem. Sci. 28:130-136.
60. Smiley JR. 2004. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? J. Virol. 78:1063-1068.
61. Smith RW, Graham SV, Gray NK. 2008. Regulation of translation initiation by herpesviruses. Biochem. Soc. Trans. 36:701-707.
62. Tourriere H, et al. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160:823-831.
63. Walsh D, Mohr I. 2011. Viral subversion of the host protein synthesis machinery. Nat. Rev. Microbiol. 9:860-875.
64. Wek RC, Jiang HY, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34:7-11.
65. White JP, Cardenas AM, Marissen WE, Lloyd RE. 2007. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2:295-305.
66. Zhang F, Moon A, Childs K, Goodbourn S, Dixon LK. 2010. The African swine fever virus DP71L protein recruits the protein phosphatase 1 catalytic subunit to dephosphorylate eIF2α and inhibits CHOP induction but is dispensable for these activities during virus infection. J. Virol. 84:10681-10689.
67. Zhang T, Delestienne N, Huez G, Kruys V, Gueydan C. 2005. Identification of the sequence determinants mediating the nucleo-cytoplasmic shuttling of TIAR and TIA-1 RNA-binding proteins. J. Cell Sci. 118:5453-5463.