Increased eIF2α phosphorylation attenuates replication of herpes simplex virus 2 vhs mutants in mouse embryonic fibroblasts and correlates with reduced accumulation of the PKR antagonist ICP34.5

Journal of Virology

Volumn 83, Issue 18, 2009, Pages 9151-9162

  Wylie, Kristine M ^a   Schrimpf, Jane E ^a   Morrison, Lynda A ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ICP34 5 PROTEIN; INITIATION FACTOR 2ALPHA; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN KINASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; ICP34.5 PROTEIN, HUMAN HERPESVIRUS 2; ICP34.5 PROTEIN, HUMAN HERPESVIRUS-2; INITIATION FACTOR 2; MUTANT PROTEIN; PROTEIN KINASE R; VIRION HOST SHUTOFF PROTEIN, SIMPLEXVIRUS;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; EMBRYO; FIBROBLAST; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; VIRUS MUTANT; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; VIROLOGY;

EUKARYOTA; HUMAN HERPESVIRUS 2; SIMPLEXVIRUS;

ANIMALS; CELLS, CULTURED; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; FIBROBLASTS; HERPESVIRUS 2, HUMAN; MICE; MUTANT PROTEINS; PHOSPHORYLATION; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 69449088685     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00886-09     Document Type: Article

References (61)

1. Alexander, D. E., S. L. Ward, N. Mizushima, B. Levine, and D. A. Leib. 2007. Analysis of the role of autophagy in replication of herpes simplex virus in cell culture. J. Virol. 81:12128-12134. (Pubitemid 350085828)
2. Beckham, C. J., and R. Parker. 2008. P bodies, stress granules, and viral life cycles. Cell Host Microbe 3:206-212.
3. Berlanga, J. J., I. Ventoso, H. P. Harding, J. Deng, D. Ron, N. Soneberg, L. Carrasco, and C. deHaro. 2006. Antiviral effect of the mammalian translation initiation factor 2 alpha kinase GCN2 against RNA viruses. EMBO J. 25:1730-1740.
4. Bolovan, C. A., N. M. Sawtell, and R. L. Thompson. 1994. ICP34.5 mutants of herpes simplex virus type 1 strain 17syn+ are attenuated for neurovirulence in mice and for replication in confluent primary mouse embryo cell cultures. J. Virol. 68:48-55. (Pubitemid 24974606)
5. Brown, S. M., J. Harland, A. R. MacLean, J. Podlech, and J. B. Clements. 1994. Cell type and cell state determine differential in vitro growth of non-neurovirulent ICP34.5-negative herpes simplex virus types 1 and 2. J. Gen. Virol. 75:2367-2377.
6. Brown, S. M., D. A. Ritchie, and J. H. Subak-Sharpe. 1973. Genetic studies with herpes simplex virus type 1. The isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. J. Gen. Virol. 18:329-346.
7. Cassady, K. A., and M. Gross. 2002. The herpes simplex virus type 1 US11 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.
8. 134.5 gene if present before activation of protein kinase R by precluding its phosphorylation and that of the α subunit of eukaryotic translation initiation factor 2. J. Virol. 72:8620-8626.
9. 134.5 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.
10. 134.5 protein. J. Virol. 79:1379-1388.
11. Chou, J., and B. Roizman. 1992. The gamma 1(34.5) gene of herpes simplex virus 1 precludes neuroblastoma cells from triggering total shutoff of protein synthesis characteristic of programed cell death in neuronal cells. Proc. Natl. Acad. Sci. USA 89:3266-3270.
12. Chou, J., J. J. Chen, M. Gross, and B. Roizman. 1995. Association of a M(r) 90,000 phosphoprotein with protein kinase PKR in cells exhibiting enhanced phosphorylation of translation initiation factor eIF-2 alpha and premature shutoff of protein synthesis after infection with gamma 134.5- mutants of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 92:10516-10520.
13. Duerst, R. J., and L. A. Morrison. 2004. Herpes simplex virus 2 virion host shutoff protein interferes with type I interferon production and responsiveness. Virology 322:158-167. (Pubitemid 38519877)
14. Duff, R., and F. Rapp. 1971. Oncogenic transformation of hamster cells after exposure to herpes simplex virus type 2. Nat. New Biol. 233:48-50.
15. 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.
16. 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)
17. Everly, D. N., Jr., and G. S. Read. 1997. Mutational analysis of the virion host shutoff gene (UL41) of herpes simplex virus (HSV): characterization of HSV type 1 (HSV-1)/HSV-2 chimeras. J. Virol. 71:7157-7166.
18. Fenwick, M. L., and J. Clark. 1982. Early and delayed shut-off of host protein synthesis in cells infected with herpes simplex virus. J. Gen. Virol. 61:121-125.
19. Fenwick, M. L., and S. A. Owen. 1988. On the control of immediate early (alpha) mRNA survival in cells infected with herpes simplex virus. J. Gen. Virol. 69:2869-2877.
20. Gale, M., Jr., S. L. Tan, and M. G. Katze. 2000. Translational control of viral gene expression in eukaryotes. Microbiol. Mol. Biol. Rev. 64:239-280.
21. He, B. 2006. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ. 13:393-403.
22. He, B., M. Gross, and B. Roizman. 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 double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 94:843-848.
23. He, B., M. Gross, and B. Roizman. 1998. The gamma134.5 protein of herpes simplex virus 1 has the structural and functional attributes of a protein phosphatase 1 regulatory subunit and is present in a high molecular weight complex with the enzyme in infected cells. J. Biol. Chem. 273:20737-20743.
24. Hill, T. M., R. R. Sinden, and J. R. Sadler. 1983. Herpes simplex virus types 1 and 2 induce shutoff of host protein synthesis by different mechanisms in Friend erythroleukemia cells. J. Virol. 45:241-250.
25. Kedersha, N. L., M. Gupta, W. Li, I. Miller, and P. Anderson. 1999. RNA-binding 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. Knipe, D. M., and A. E. Spang. 1982. Definition of a series of stages in the association of two herpesviral proteins with the cell nucleus. J. Virol. 43:314-324.
27. Korom, M., K. M. Wylie, and L. A. Morrison. 2008. Selective ablation of virion host shutoff protein RNase activity attenuates herpes simplex virus 2 in mice. J. Virol. 82:3642-3653.
28. 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. USA 84:1926-1930.
29. Kwong, A. D., J. A. Kruper, and N. Frenkel. 1988. Herpes simplex virus virion host shutoff function. J. Virol. 62:912-921.
30. Li, W., Y. Li, N. Kedersha, P. Anderson, M. Emara, K. M. Swiderek, G. T. Moreno, and M. A. Brinton. 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. (Pubitemid 35304299)
31. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25:402-408. (Pubitemid 34164012)
32. McDermott, M. R., J. R. Smiley, P. Leslie, J. Brais, H. E. Rudzroga, and J. Bienenstock. 1984. Immunity in the female genital tract after intravaginal vaccination of mice with an attenuated strain of herpes simplex virus type 2. J. Virol. 51:747-753. (Pubitemid 14063152)
33. Merrick, W. C. 1992. Mechanism and regulation of eukaryotic protein synthesis. Microbiol. Rev. 56:291-315.
34. Mossman, K. L., H. A. Saffran, and J. R. Smiley. 2000. Herpes simplex virus ICP0 mutants are hypersensitive to interferon. J. Virol. 74:2052-2056.
35. Mulvey, M., J. Poppers, D. Sternberg, and I. Mohr. 2003. Regulation of eIF2α phosphorylation by different functions that act during discrete phases in the herpes simplex virus type 1 life cycle. J. Virol. 77:10917-10928. (Pubitemid 37204285)
36. Mulvey, M., C. Arias, and I. Mohr. 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. (Pubitemid 44092558)
37. Mulvey, M., C. Arias, and I. Mohr. 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. (Pubitemid 46456647)
38. Murphy, J. A., R. J. Duerst, T. J. Smith, and L. A. Morrison. 2003. Herpes simplex virus type 2 virion host shutoff protein regulates alpha/beta interferon but not adaptive immune responses during primary infection in vivo. J. Virol. 77:9337-9345.
39. 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.
40. 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.
41. Orvedahl, A., D. Alexander, Z. Talloczy, Q. Sun, Y. Wei, W. Zhang, D. Burns, D. A. Leib, and B. Levine. 2007. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1:23-35. (Pubitemid 46506007)
42. Pasieka, T. J., T. Baas, V. S. Carter, S. C. Proll, M. G. Katze, and D. A. Leib. 2006. Functional genomic analysis of herpes simplex virus type 1 counteraction of the host innate response. J. Virol. 80:7600-7612. (Pubitemid 44092581)
43. Pasieka, T. J., B. Lu, S. D. Crosby, K. M. Wylie, L. A. Morrison, D. E. Alexander, V. D. Menachery, and D. A. Leib. 2008. Herpes simplex virus virion host shutoff attenuates establishment of the antiviral state. J. Virol. 82:5527-5535.
44. Pestova, T. V., V. G. Kolupaeva, I. B. Lomakin, E. V. Pilipenko, I. N. Shatsky, V. I. Agol, and C. U. Hellen. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA 98:7029-7036.
45. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
46. Poppers, J., M. Mulvey, D. Khoo, and I. Mohr. 2000. Inhibition of PKR activation by the proline-rich RNA binding domain of the herpes simplex virus type 1 Us11 protein. J. Virol. 74:11215-11221. (Pubitemid 32223989)
47. Read, G. S., and N. Frenkel. 1983. Herpes simplex virus mutants defective in the virion-associated shutoff of host polypeptide synthesis and exhibiting abnormal synthesis of α (immediate early) viral polypeptides. J. Virol. 46: 498-512.
48. Scheuner, D., B. Song, E. McEwen, C. Liu, R. Laybutt, P. Gillespie, T. Saunders, S. Bonner-Weir, and R. J. Kaufman. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165-1176. (Pubitemid 32607351)
49. Shibaki, T., T. Suzutani, I. Yoshida, M. Ogasawara, and M. Azuma. 2001. Participation of type I interferon in the decreased virulence of the UL13 gene-deleted mutant of herpes simplex virus type 1. J. Interferon Cytokine Res. 21:279-285. (Pubitemid 32727426)
50. Smiley, J. R. 2004. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase. J. Virol. 78:1063-1068. (Pubitemid 38095816)
51. Smiley, J. R., M. M. Elgadi, and H. A. Saffran. 2001. Herpes simplex virus vhs protein. Methods Enzymol. 342:440-451. (Pubitemid 32911963)
52. Smith, T. J., L. A. Morrison, and D. A. Leib. 2002. Pathogenesis of herpes simplex virus type 2 virion host shutoff (vhs) mutants. J. Virol. 76:2054-2061.
53. Taddeo, B., W. Zhang, and B. Roizman. 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. USA 103:2827-2832.
54. Talloczy, Z., W. Jiang, H. W. Virgin IV, D. A. Leib, D. Scheuner, R. J. Kaufman, E. L. Eskelinen, and B. Levine. 2002. Regulation of starvationand virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. USA 99:190-195.
55. Tang, S., A. S. Bertke, A. Patel, K. Wang, J. I. Cohen, and P. R. Krause. 2008. An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc. Natl. Acad. Sci. USA 105:10931-10936.
56. Verpooten, D., Y. Ma, S. Hou, Z. Yan, and B. He. 2009. Control of TANK-binding kinase 1-mediated signaling by the gamma134.5 protein of herpes simplex virus 1. J. Biol. Chem. 284:1097-1105.
57. Ward, S. L., D. Scheuner, J. Poppers, R. J. Kaufman, I. Mohr, and D. A. Leib. 2003. In vivo replication of an ICP34.5 second-site suppressor mutant following corneal infection correlates with in vitro regulation of eIF2α phosphorylation. J. Virol. 77:4626-4634.
58. Yang, Y. L., L. F. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B. R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14:6095-6106.
59. 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. (Pubitemid 26087605)
60. Zhang, P., B. McGrath, S. Li, A. Frank, F. Zambito, J. Reinert, M. Gannon, K. Ma, K. McNaughton, and D. R. Cavener. 2002. The PERK eukaryotic initiation factor 2α kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 22:3864-3874.
61. Zhang, P., B. C. McGrath, J. Reinert, D. S. Olsen, L. Lei, S. Gill, S. A. Wek, K. M. Vattem, R. C. Wek, S. R. Kimball, L. S. Jefferson, and D. R. Cavener. 2002. The GCN2 eIF2α kinase is required for adaptation to amino acid deprivation in mice. Mol. Cell. Biol. 22:6681-6688.