Induction of cellular stress overcomes the requirement of herpes simplex virus type 1 for immediate-early protein ICP0 and reactivates expression from quiescent viral genomes

Journal of Virology

Volumn 82, Issue 23, 2008, Pages 11775-11783

  Preston, Chris M ^a   Nicholl, Mary Jane ^a  

^a INSTITUTE OF VIROLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; ARSENITE SODIUM; GENOMIC RNA; GRAMICIDIN D; IMMEDIATE EARLY PROTEIN ICP0; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; VIRUS REACTIVATION; VIRUS REPLICATION;

APOPTOSIS; ARSENITES; CELLS, CULTURED; CYTOMEGALOVIRUS; GENES, IMMEDIATE-EARLY; GENOME, VIRAL; GRAMICIDIN; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; PROMOTER REGIONS, GENETIC; STRESS, PHYSIOLOGICAL; UBIQUITIN-PROTEIN LIGASES; VIRUS ACTIVATION;

HUMAN HERPESVIRUS 1;

EID: 56449126933     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01273-08     Document Type: Article

References (81)

1. Addison, C. L., M. Hitt, D. Kunsken, and F. L. Graham. 1997. Comparison of the human versus murine cytomegalovirus immediate early gene promoters for transgene expression by adenoviral vectors. J. Gen. Virol. 78:1653-1661.
2. Arthur, J. L., C. G. Scarpini, V. Connor, R. H. Lachmann, A. M. Tolkovsky, and S. Efstathiou. 2001. Herpes simplex virus type 1 promoter activity during latency establishment, maintenance, and reactivation in primary dorsal root neurons in vitro. J. Virol. 75:3885-3895.
3. Block, G. J., C. H. Eskiw, G. Dellaire, and D. P. Bazett-Jones. 2006. Transcription regulation is affected by subnuclear targeting of reporter plasmids to PML nuclear bodies. Mol. Cell. Biol. 26:8814-8825.
4. Blyth, W. A., D. A. Harbour, and T. J. Hill. 1980. Effect of immunosuppression on recurrent herpes simplex in mice. Infect. Immun. 29:902-907.
5. Bourinbaiar, A. S., and C. F. Coleman. 1997. The effect of gramicidin, a topical contraceptive and antimicrobial agent with anti-HIV activity, against herpes simplex viruses type 1 and 2 in vitro. Arch. Virol. 142:2225-2235.
6. Boutell, C., S. Sadis, and R. D. Everett. 2002. Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 76:841-850.
7. - viruses. J. Virol. 80:4528-4537.
8. Cai, W., and P. A. Schaffer. 1991. A cellular function can enhance gene expression and plating efficiency of a mutant defective in the gene for ICP0, a transactivating protein of herpes simplex virus type 1. J. Virol. 65:4078-4090.
9. Cantrell, S. R., and W. A. Bresnahan. 2006. Human cytomegalovirus (HCMV) UL82 gene product (pp71) relieves hDaxx-mediated repression of HCMV replication. J. Virol. 80:6188-6191.
10. Carrozza, M. J., and N. A. DeLuca. 1996. Interaction of the viral activator protein ICP4 with TFIID through TAF250. Mol. Cell. Biol. 16:3085-3093.
11. Danaher, R. J., R. J. Jacob, and C. S. Miller. 2006. Reactivation from quiescence does not coincide with a global induction of herpes simplex virus type 1 transactivators. Virus Genes 33:163-167.
12. Danaher, R. J., R. J. Jacob, M. R. Steiner, W. R. Allen, J. M. Hill, and C. S. Miller. 2005. Histone deacetylase inhibitors induce reactivation of herpes simplex virus type 1 in a latency-associated transcript-independent manner in neuronal cells. J. Neurovirol. 11:306-317.
13. Davison, M. J., V. G. Preston, and D. J. McGeoch. 1984. Determination of the sequence alteration in the DNA of the herpes simplex virus type 1 temperature-sensitive mutant ts K. J. Gen. Virol. 65:859-863.
14. Efstathiou, S., and C. M. Preston. 2005. Towards an understanding of the molecular basis of herpes simplex virus latency. Virus Res. 111:108-119.
15. Erl, W., C. Weber, and G. K. Hansson. 2000. Pyrollidone dithiocarbamate-induced apoptosis depends on cell type, density, and the presence of Cu(2+) and Zn(2+). Am. J. Physiol. Cell Physiol. 278:C1116-C1125.
16. Everett, R. D. 1989. Construction and characterisation of herpes simplex virus type 1 mutants with defined lesions in immediate early gene 1. J. Gen. Virol. 70:1185-1202.
17. Everett, R. D. 2000. ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761-770.
18. Everett, R. D. 1984. Transactivation of transcription by herpes virus products: requirement for two HSV-1 immediate-early polypeptides for maximum activity. EMBO J. 3:3135-3141.
19. Everett, R. D., C. Boutell, and A. Orr. 2004. Phenotype of a herpes simplex virus type 1 mutant that fails to express immediate-early regulatory protein ICP0. J. Virol. 78:1763-1774.
20. Everett, R. D., W. C. Earnshaw, J. Findlay, and P. Lomonte. 1999. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J. 18:1526-1538.
21. Everett, R. D., P. Freemont, H. Saitoh, M. Dasso, A. Orr, M. Kathoria, and J. Parkinson. 1998. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms. J. Virol. 72:6581-6591.
22. Everett, R. D., and G. G. Maul. 1994. HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO J. 13:5062-5069.
23. Everett, R. D., and J. Murray. 2005. ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J. Virol. 79:5078-5089.
24. Everett, R. D., J. Murray, A. Orr, and C. M. Preston. 2007. Herpes simplex virus type 1 genomes are associated with ND10 nuclear substructures in quiescently infected human fibroblasts. J. Virol. 81:10991-11004.
25. Everett, R. D., A. Orr, and C. M. Preston. 1998. A viral activator of gene expression functions via the ubiquitin-proteasome pathway. EMBO J. 17:7161-7169.
26. Everett, R. D., C. Parada, P. Gripon, H. Sirma, and A. Orr. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672.
27. Everett, R. D., S. Rechter, P. Papior, N. Tavalai, T. Stamminger, and A. Orr. 2006. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80:7995-8005.
28. Friedberg, I., G. A. Weisman, and B. K. De. 1985. Permeability change in transformed mouse fibroblasts caused by ionophores, and its relationship to membrane permeabilization by exogenous ATP. J. Membr. Biol. 83:251-259.
29. Furuta, S., F. Ortiz, X. Z. Sun, H.-H. Wu, A. Mason, and J. Momand. 2002. Copper uptake is required for pyrrolidine dithiocarbamate- mediated oxidation and protein level increase of p53 in cells. Biochem. J. 365:639-648.
30. Goeffroy, M. C., G. Chadeuf, A. Orr, A. Salvetti, and R. D. Everett. 2006. Impact of the interaction between herpes simplex virus type 1 regulatory protein ICP0 and ubiquitin-specific protease USP7 on activation of adeno-associated virus type 2 rep gene expression. J. Virol. 80:3650-3654.
31. Hagglund, R., and B. Roizman. 2004. Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J. Virol. 78:2169-2178.
32. Halford, W. P., B. M. Gebhardt, and D. J. Carr. 1996. Mechanisms of herpes simplex virus type 1 reactivation. J. Virol. 70:5051-5060.
33. Hancock, M. H., J. A. Corcoran, and J. R. Smiley. 2006. Herpes simplex virus regulatory proteins VP16 and ICP0 counteract an innate intranuclear barrier to viral gene expression. Virology 352:237-252.
34. Hill, J. M., J. B. Dudley, Y. Shimomura, and H. E. Kaufman. 1986. Quantitation and kinetics of induced HSV-1 ocular shedding. Curr. Eye Res. 5:241-246.
35. Hobbs, W. E., D. E. Brough, I. Kovesdi, and N. A. DeLuca. 2001. Efficient activation of viral genomes by levels of herpes simplex virus ICP0 insufficient to affect cellular gene expression or cell survival. J. Virol. 75:3391-3403.
36. Homer, E. G., A. Rinaldi, M. J. Nicholl, and C. M. Preston. 1999. Activation of herpesvirus gene expression by the human cytomegalovirus protein pp71. J. Virol. 73:8512-8518.
37. Jamieson, D. R. S., L. H. Robinson, J. I. Daksis, M. J. Nicholl, and C. M. Preston. 1995. Quiescent viral genomes in human fibroblasts after infection with herpes simplex virus Vmw65 mutants. J. Gen. Virol. 76:1417-1431.
38. Jones, C. 2003. Herpes simplex virus type 1 and bovine herpesvirus 1 latency. Clin. Microbiol. Rev. 16:79-95.
39. Kelkar, D. A., and A. Chattopadhyay. 2007. The gramicidin ion channel: a model membrane protein. Biochim. Biophys. Acta 1768:2011-2025.
40. Khalil, S., J. Luciano, W. Chen, and A. Y.-C. Liu. 2006. Dynamic regulation and involvement of heat shock transcriptional response in arsenic carcinogenesis. J. Cell. Physiol. 207:562-569.
41. Kitchin, K. T. 2001. Recent advances in arsenic carcinogenesis: modes of action, animal model systems, and methylated arsenic metabolites. Toxicol. Appl. Pharmacol. 172:249-261.
42. Lau, A. T. Y., Q.-Y. He, and J.-F. Chiu. 2004. A proteome analysis of the arsenite response in cultured lung cells: evidence for in vitro oxidative stress-induced apoptosis. Biochem. J. 382:641-650.
43. Marshall, K. R., K. V. Rowley, A. Rinaldi, I. P. Nicholson, A. M. Ishov, G. G. Maul, and C. M. Preston. 2002. Activity and intracellular localization of the human cytomegalovirus protein pp71. J. Gen. Virol. 83:1601-1612.
44. Mastrocola, T., A. Flamigni, and M. Rugulo. 1991. Hypotonic shock activated Cl- and K+ pathways in human fibroblasts. Biochim. Biophys. Acta 1069:201-208.
45. McFarlane, M., J. I. Daksis, and C. M. Preston. 1992. Hexamethylene bisacetamide stimulates herpes simplex virus immediate early gene expression in the absence of trans-induction by Vmw65. J. Gen. Virol. 73:285-292.
46. Miller, C. S., R. J. Danaher, and R. J. Jacob. 2006. ICP0 is not required for efficient stress-induced reactivation of herpes simplex virus type 1 from cultured quiescently infected neuronal cells. J. Virol. 80:3360-3368.
47. Minaker, R. L., K. L. Mossman, and J. R. Smiley. 2005. Functional inaccessibility of quiescent herpes simplex virus genomes. Virol. J. 2:85-99.
48. Mosca, J. D., D. P. Bednarik, N. B. Raj, C. A. Rosen, J. G. Sodroski, W. A. Haseltine, G. S. Hayward, and P. M. Pitha. 1987. Activation of human immunodeficiency virus by herpesvirus infection: identification of a region within the long terminal repeats that responds to a trans-acting factor encoded by herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 84:7408-7412.
49. Mossman, K. L., P. F. MacGregor, J. J. Rozmus, A. B. Goryachev, A. M. Edwards, and J. R. Smiley. 2001. Herpes simplex virus triggers and then disarms a host antiviral response. J. Virol. 75:750-758.
50. Neumann, D. M., P. S. Bhattacharjee, and J. M. Hill. 2007. Sodium butyrate: a chemical inducer of in vivo reactivation of herpes simplex virus type 1 in the ocular mouse model. J. Virol. 81:6106-6110.
51. O'Hare, P. 1993. The virion transactivator of herpes simplex virus. Semin. Virol. 4:145-155.
52. O'Hare, P., and G. S. Hayward. 1985. Evidence for a direct role for both the 175,000- and 110,000-molecular-weight immediate-early proteins of herpes simplex virus in the transactivation of delayed-early promoters. J. Virol. 53:751-760.
53. Preston, C. M. 1979. Control of herpes simplex virus type 1 mRNA synthesis in cells infected with wild-type virus or the temperature sensitive mutant tsK. J. Virol. 29:275-284.
54. Preston, C. M. 2007. Reactivation of expression from quiescent herpes simplex virus type 1 genomes in the absence of immediate-early protein ICP0. J. Virol. 81:11781-11789.
55. Preston, C. M., and M. J. Nicholl. 2005. Human cytomegalovirus tegument protein pp71 directs long-term gene expression from quiescent herpes simplex virus genomes. J. Virol. 79:525-535.
56. Preston, C. M., and M. J. Nicholl. 1997. Repression of gene expression upon infection of cells with herpes simplex virus type 1 mutants impaired for immediate-early protein synthesis. J. Virol. 71:7807-7813.
57. Preston, C. M., and M. J. Nicholl. 2006. Role of the cellular protein hDaxx in human cytomegalovirus immediate-early gene expression. J. Gen. Virol. 87:1113-1121.
58. Preston, C. M., A. Rinaldi, and M. J. Nicholl. 1998. Herpes simplex virus type 1 immediate early gene expression is stimulated by inhibition of protein synthesis. J. Gen. Virol. 79:117-124.
59. Proskuryakov, S. Y., A. G. Knonplyannikov, and V. L. Gabai. 2003. Necrosis: a specific form of programmed cell death? Exp. Cell Res. 283:1-16.
60. Rea, M. A., J. P. Gregg, Q. Qin, M. A. Phillips, and R. H. Rice. 2003. Global alteration of gene expression in human keratinocytes by inorganic arsenite. Carcinogenesis 24:747-756.
61. Sacks, W. R., and P. A. Schaffer. 1987. Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in culture. J. Virol. 61:829-839.
62. Saffert, R. T., and R. F. Kalejta. 2006. Inactivating a cellular intrinsic defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J. Virol. 80:3863-3871.
63. Samaniego, L. A., L. Neiderhiser, and N. A. DeLuca. 1998. Persistence and expression of the herpes simplex virus genome in the absence of immediateearly proteins. J. Virol. 72:3307-3320.
64. Sampath, P., and N. A. DeLuca. 2008. Binding of ICP4, TATA-binding protein, and RNA polymerase II to herpes simplex virus type 1 immediateearly, early and late promoters in virus-infected cells. J. Virol. 82:2339-2349.
65. Sawtell, N. M., and R. L. Thompson. 1992. Rapid in vivo reactivation of herpes simplex virus in latently infected murine ganglionic neurons after transient hyperthermia. J. Virol. 66:2150-2156.
66. Smith, R. L., J. M. Escudero, and C. L. Wilcox. 1992. Activation of second messenger pathways activates latent herpes simplex virus in neuronal cultures. Virology 188:311-318.
67. Stow, E. C., and N. D. Stow. 1989. Complementation of a herpes simplex virus type 1 Vmw110 deletion mutant by human cytomegalovirus. J. Gen. Virol. 70:695-704.
68. Stow, N. D., and E. C. Stow. 1986. Isolation and characterisation of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. J. Gen. Virol. 67:2571-2585.
69. Su, Y.-H., R. L. Meegalla, R. Chowhan, C. Cubitt, J. E. Oakes, R. N. Lausch, N. W. Fraser, and T. M. Block. 1999. Human corneal cells and other fibroblasts can stimulate the appearance of herpes simplex virus from quiescently infected PC12 cells. J. Virol. 73:4171-4180.
70. Tavalai, N., P. Papior, S. Rechter, and T. Stamminger. 2008. Nuclear domain 10 components promyelocytic leukemia protein and hDaxx independently contribute to an intrinsic antiviral defense against human cytomegalovirus infection. J. Virol. 82:126-137.
71. Terry-Allison, T., C. A. Smith, and N. A. DeLuca. 2007. Relaxed repression of herpes simplex virus type 1 genomes in murine trigeminal neurons. J. Virol. 81:12394-12405.
72. Thompson, R. L., and N. M. Sawtell. 2006. Evidence that the herpes simplex virus type 1 ICP0 protein does not initiate reactivation from latency in vivo. J. Virol. 80:10919-10930.
73. Wagner, E. K., and D. C. Bloom. 1997. Experimental investigation of herpes simplex virus latency. Clin. Microbiol. Rev. 10:419-443.
74. Wallace, B. A. 2000. Common structural features in gramicidin and other ion channels. Bioessays 22:227-234.
75. Wigdahl, B. L., R. J. Ziegler, M. Sneve, and F. Rapp. 1983. Herpes simplex virus latency in isolated rat sensory neurons. Virology 127:159-167.
76. Wilcox, C. L., R. L. Smith, C. R. Freed, and E. M. Johnson. 1990. Nerve growth factor-dependence of herpes simplex virus latency in peripheral sympathetic and sensory neurons in vitro. J. Neurosci. 104:1268-1275.
77. Wysocka, J., and W. Herr. 2003. The herpes simplex virus VP16-induced complex: the makings of a regulatory switch. Trends Biochem. Sci. 28:294-304.
78. Yao, F., and P. A. Schaffer. 1995. An activity specified by the osteosarcoma line U2OS can substitute functionally for ICP0, a major regulatory protein of herpes simplex virus type 1. J. Virol. 69:6249-6258.
79. Yih, L.-H., K. Peck, and T.-C. Lee. 2002. Changes in gene expression profiles of human fibroblasts in response to sodium arsenite treatment. Carcinogenesis 23:867-876.
80. Zabierowski, S., and N. A. DeLuca. 2004. Differential cellular requirements for activation of herpes simplex virus type 1 early (tk) and late (gC) promoters by ICP4. J. Virol. 78:6162-6170.
81. Zong, W. X., and C. B. Thompson. 2006. Necrotic death as a cell fate. Genes Dev. 20:1-15.