Herpes simplex virus 1 has multiple mechanisms for blocking virus-induced interferon production

Journal of Virology

Volumn 78, Issue 16, 2004, Pages 8411-8420

  Melroe, Gregory T ^a   DeLuca, Neal A ^b   Knipe, David M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; IMMEDIATE EARLY PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; PROTEIN ICP0; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SENDAI VIRUS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS MUTANT; VIRUS VIRULENCE;

CELL LINE, TUMOR; CELL NUCLEUS; DNA-BINDING PROTEINS; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; RNA, MESSENGER; SENDAI VIRUS; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 3543054546     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.16.8411-8420.2004     Document Type: Article

References (75)

1. Bandyopadhyay, S. K., G. T. Leonard, Jr., T. Bandyopadhyay, G. R. Stark, and G. C. Sen. 1995. Transcriptional induction by double-stranded RNA is mediated by interferon-stimulated response elements without activation of interferon-stimulated gene factor 3. J. Biol. Chem. 270:19624-19629.
2. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhlberger, M. Bray, H. D. Klenk, P. Palese, and A. Garcia-Sastre. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
3. Batterson, W., and B. Roizman. 1983. Characterization of the herpes simplex virion-associated factor responsible for the induction of alpha genes. J. Virol. 46:371-377.
4. Biron, C. A., and G. C. Sen. 2001. Interferons and other cytokines, p. 321-351. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 1. Lippincott/The Williams & Wilkins Co., Philadelphia, Pa.
5. Bossert, B., S. Marozin, and K. K. Conzelmann. 2003. Nonstructural proteins NS1 and NS2 of bovine respiratory syncytial virus block activation of interferon regulatory factor 3. J. Virol. 77:8661-8668.
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 as a ubiquitin E3 ligases in vitro. J. Virol. 76:841-850.
7. Burysek, L., W. S. Yeow, B. Lubyova, M. Kellum, S. L. Schafer, Y. Q. Huang, and P. M. Pitha. 1999. Functional analysis of human herpesvirus 8-encoded viral interferon regulatory factor 1 and its association with cellular interferon regulatory factors and p300. J. Virol. 73:7334-7342.
8. Cai, W. Z., and P. A. Schaffer. 1989. Herpes simplex virus type 1 ICP0 plays a critical role in the de novo synthesis of infectious virus following transfection of viral DNA. J. Virol. 63:4579-4589.
9. Campbell, M. E. M., J. W. Palfreyman, and C. M. Preston. 1984. Identification of herpes simplex virus DNA sequences which encode a trans-acting polypeptide responsible for stimulation of immediate-early transcription. J. Mol. Biol. 180:1-19.
10. Chakravarti, D., V. Ogryzko, H. Y. Kao, A. Nash, H. Chen, Y. Nakatani, and R. M. Evans. 1999. A viral mechanism for inhibition of p300 and PCAF acetyltransferase activity. Cell 96:393-403.
11. Chee, A. V., P. Lopez, P. P. Pandolfi, and B. Roizman. 2003. Promyelocytic leukemia protein mediates interferon-based anti-herpes simplex virus 1 effects. J. Virol. 77:7101-7105.
12. Chelbi-Alix, M. K., and H. de The. 1999. Herpesvirus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 18:935-941.
13. Chelbi-Alix, M. K., L. Pelicano, F. Quignon, M. H. Koken, L. Venturini, M. Stadler, J. Pavlovic, L. Degos, and H. de The. 1995. Induction of the PML protein by interferons in normal and APL cells. Leukemia 9:2027-2033.
14. Chelbi-Alix, M. K., F. Quignon, L. Pelicano, M. H. Koken, and H. de The. 1998. Resistance to virus infection conferred by the interferon-induced promyelocytic leukemia protein. J. Virol. 72:1043-1051.
15. Chu, W.-M., X. Gong, Z.-W. Li, K. Takabayashi, H.-H. Ouyang, Y. Chen, A. Lois, D. J. Chen, G. C. Li, M. Karin, and E. Raz. 2000. DNA-PKcs is required for activation of innate immunity by immunostimulatory DNA. Cell 103:909-918.
16. DeLuca, N. A., and P. A. Schaffer. 1988. Physical and functional domains of the herpes simplex virus transcriptional regulatory protein ICP4. J. Virol. 62:732-743.
17. Eidson, K. M., W. E. Hobbs, B. J. Manning, P. Carlson, and N. A. DeLuca. 2002. Expression of herpes simplex virus ICP0 inhibits the induction of interferon-stimulated genes by viral Infection. J. Virol. 76:2180-2191.
18. 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.
19. Fitzgerald, K. A., S. M. McWhirter, K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S. M. Liao, and T. Maniatis. 2003. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491-496.
20. Foy, E., K. Li, C. Wang, R. J. Sumpter, M. Ikeda, S. M. Lemon, and M. J. Gale. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300:1145-1148.
21. Graff, J. W., D. N. Mitzel, C. M. Weisend, M. L. Flenniken, and M. E. Hardy. 2002. Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J. Virol. 76:9545-9550.
22. Hagglund, R., C. Van Sant, P. Lopez, and B. Roizman. 2002. Herpes simplex virus 1-infected cell protein 0 contains two E3 ubiquitin ligase sites specific for different E2 ubiquitin-conjugating enzymes. Proc. Natl. Acad. Sci. USA 99:631-636.
23. Harle, P., B. Sainz, Jr., D. J. Carr, and W. P. Halford. 2002. The immediate-early protein, ICP0, is essential for the resistance of herpes simplex virus to interferon-alpha/beta. Virology 293:295-304.
24. He, B., M. Gross, and B. Roizman. 1997. The gamma (1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1 alpha 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.
25. Hobbs, W. E., II, and N. A. DeLuca. 1999. Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J. Virol. 73:8245-8255.
26. Honess, R. W., and B. Roizman. 1974. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J. Virol. 14:8-19.
27. Honess, R. W., and B. Roizman. 1975. Regulation of herpesvirus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proc. Natl. Acad. Sci. USA 72:1276-1280.
28. Juang, Y. T., W. Lowther, M. Kellum, W. C. Au, R. Lin, J. Hiscott, and P. M. Pitha. 1998. Primary activation of interferon A and interferon B gene transcription by interferon regulatory factor 3. Proc. Natl. Acad. Sci. USA 95:9837-9842.
29. Karpova, A. Y., M. Trost, J. M. Murray, L. C. Cantley, and P. M. Howley. 2002. Interferon regulatory factor-3 is an in vivo target of DNA-PK. Proc. Natl. Acad. Sci. USA 99:2818-2823.
30. Knipe, D. M., D. Senechek, S. A. Rice, and J. L. Smith. 1987. Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4. J. Virol. 61:276-284.
31. 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.
32. Kohl, A., R. F. Clayton, F. Weber, A. Bridgen, R. E. Randall, and R. M. Elliott. 2003. Bunyamwera virus nonstructural protein NSs counteracts interferon regulatory factor 3-mediated induction of early cell death. J. Virol. 77:7999-8008.
33. Krug, A., G. D. Luker, W. Barchet, D. A. Leib, S. Akira, and M. Colonna. 2004. Herpes simplex virus type 1 activates murine natural interferon-producing cells through Toll-like receptor 9. Blood 103:1433-1437.
34. 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.
35. Kwong, A. D., J. A. Kruper, and N. Frenkel. 1988. Herpes simplex virus virion host shutoff function. J. Virol. 62:912-921.
36. Lavau, C., A. Marchio, M. Fagioli, J. Jansen, B. Falini, P. Lebon, F. Grosveld, P. P. Pandolfi, P. G. Pelicci, and A. Dejean. 1995. The acute promyelocytic leukaemia-associated PML gene is induced by interferon. Oncogene 11:871-876.
37. Lee, C. K., and D. M. Knipe. 1983. Thermolabile in vivo DNA-binding activity associated with a protein encoded by mutants of herpes simplex virus type 1. J. Virol. 46:909-919.
38. Lees-Miller, S. P., M. C. Long, M. A. Kilvert, V. Lam, S. A. Rice, and C. A. Spencer. 1996. Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J. Virol. 70:7471-7477.
39. Leib, D. A., T. E. Harrison, K. M. Laslo, M. A. Machalek, N. J. Moorman, and H. W. Virgin. 1999. Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo. J. Exp. Med. 189:663-672.
40. Leib, D. A., M. A. Machalek, B. R. G. Williams, R. H. Silverman, and H. W. Virgin. 2000. Specific phentoypic restoration of an attenuated virus by knockout of a host resistance gene. Proc. Natl. Acad. Sci. USA 97:6097-6101.
41. Lin, R., P. Genln, Y. Mamane, M. Sgarbanti, A. Battistini, W. J. Harrington, G. N. Barber, and J. Hiscott. 2001. HHV-8 encoded vIRF-1 represses the interferon antiviral response by blocking IRF-3 recruitment of the CBP/p300 coactivators. Oncogene 20:800-811.
42. Lin, R., C. Heylbroeck, P. M. Pitha, and J. Hiscott. 1998. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18:2986-2996.
43. Lin, R., Y. Mamane, and J. Hiscott. 1999. Structural and functional analysis of interferon regulatory factor 3: localization of the transactivation and autoinhibitory domains. Mol. Cell. Biol. 19:2465-2474.
44. Lin, R., R. S. Noyce, S. E. Collins, R. D. Everett, and K. L. Mossman. 2004. The herpes simplex virus ICP0 RING finger domain inhibits IRF3- and IRF7-mediated activation of interferon-stimulated genes. J. Virol. 78:1675-1684.
45. Lopez, P., R. J. Jacob, and B. Roizman. 2002. Overexpression of promyelocytic leukemia protein precludes the dispersal of ND10 structures and has no effect on accumulation of infectious herpes simplex virus 1 or its proteins. J. Virol. 76:9355-9367.
46. McCarthy, A. M., L. McMahan, and P. A. Schaffer. 1989. Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA deficient. J. Virol. 63:18-27.
47. Mittnacht, S., P. Straub, H. Kirchner, and H. Jacobsen. 1988. Interferon treatment inhibits onset of herpes simplex virus immediate-early transcription. Virology 164:201-210.
48. 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.
49. 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.
50. Muller, S., and A. Dejean. 1999. Viral immediate-early proteins abrogate the modification by SUMO-1 of PML and Sp100 proteins, correlating with nuclear body disruption. J. Virol. 73:5137-5143.
51. Nakaya, T., M. Sato, N. Hata, M. Asagiri, H. Suemori, S. Noguchi, N. Tanaka, and T. Taniguchi. 2001. Gene induction pathways mediated by distinct IRFs during viral infection. Biochem. Biophys. Res. Commun. 283:1150-1156.
52. Nicholl, M. J., L. H. Robinson, and C. M. Preston. 2000. Activation of cellular interferon-responsive genes after infection of human cells with herpes simplex virus type 1. J. Gen. Virol. 81:2215-2218.
53. Oberman, F., and A. Panet. 1989. Characterization of the early steps of herpes simplex virus replication in interferon-treated human cells. J. Interferon Res. 9:563-571.
54. Oberman, F., and A. Panet. 1988. Inhibition of transcription of herpes simplex virus immediate-early genes in interferon-treated human cells. J. Gen. Virol. 69:1167-1177.
55. Parkinson, J., S. P. Lees-Miller, and R. D. Everett. 1999. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J. Virol. 73:650-657.
56. Poole, E., B. He, R. A. Lamb, R. E. Randall, and S. Goodbourn. 2002. The V proteins of simian virus 5 and other paramyxoviruses inhibit induction of interferon-beta. Virology 303:33-46.
57. Preston, C. M., A. N. Harman, and N. M. J. 2001. Activation of interferon response factor-3 in human cells infected with herpes simplex virus type 1 or human cytomegalovirus. J. Virol. 75:8909-8916.
58. Rice, S. A., M. C. Long, V. Lam, P. A. Schaffer, and C. A. Spencer. 1995. Herpes simplex virus immediate-early protein ICP22 is required for viral modification of host RNA polymerase II and establishment of the normal viral transcription program. J. Virol. 69:5550-5559.
59. Ronco, L. V., A. Y. Karpova, M. Vidal, and P. M. Howley. 1998. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 12:2061-2072.
60. Ronnblom, L., B. Cederblad, K. Sandberg, and G. V. Alm. 1988. Determination of herpes simplex virus-induced alpha interferon-secreting human blood leucocytes by a filter immuno-plaque assay. Scand. J. Immunol. 27:165-170.
61. Samaniego, L. A., L. Neiderhiser, and N. A. DeLuca. 1998. Persistence and expression of the herpes simplex virus genome in the absence of immediate-early proteins. J. Virol. 72:3307-3320.
62. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. T. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13:539-548.
63. Sato, M., N. Tanaka, N. Hata, E. Oda, and T. Taniguchi. 1998. Involvement of the IRF family transcription factor IRF-3 in virus-induced activation of the IFN-β gene. FEBS Lett. 425:112-116.
64. 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.
65. Servant, M. J., N. Grandvaux, B. R. tenOever, D. Duguay, R. Lin, and J. Hiscott. 2003. Identification of the minimal phosphoacceptor site required for in vivo activation of interferon regulatory factor 3 in response to virus and double-stranded RNA. J. Biol. Chem. 278:9441-9447.
66. Sharma, S., B. R. tenOever, N. Grandvaux, G. P. Zhou, R. Lin, and J. Hiscott. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148-1151.
67. ten Oever, B. R., M. J. Servant, N. Grandvaux, R. Lin, and J. Hiscott. 2002. Recognition of the measles virus nucleocapsid as a mechanism of IRF-3 activation. J. Virol. 76:3659-3669.
68. Thanos, D., and T. Maniatis. 1995. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 83:1091-1100.
69. Van Sant, C., R. Hagglund, P. Lopez, and B. Roizman. 2001. The infected cell protein 0 of herpes simplex virus 1 dynamically interacts with proteasomes, binds and activates the cdc34 E2 ubiquitin-conjugating enzyme, and possesses in vitro E3 ubiquitin ligase activity. Proc. Natl. Acad. Sci. USA 98:8815-8820.
70. Wathelet, M. G., I. M. Clauss, J. Content, and G. A. Huez. 1988. Regulation of two interferon-inducible human genes by interferon, poly(rI)-poly(rC) and viruses. Eur. J. Biochem. 174:323-329.
71. Wathelet, M. G., C. H. Lin, B. S. Parekh, L. V. Ronco, P. M. Howley, and T. Maniatis. 1998. Virus infection induces the assembly of coordinately activated transcription factors on the IFN-β enhancer in vivo. Mol. Cell 1:507-518.
72. Weaver, B. K., K. P. Kumar, and N. C. Reich. 1998. Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol. Cell. Biol. 18:1359-1368.
73. Yeow, W. S., W. C. Au, W. J. Lowther, and P. M. Pitha. 2001. Downregulation of IRF-3 levels by ribozyme modulates the profile of IFNA subtypes expressed in infected human cells. J. Virol. 75:3021-3027.
74. Yokota, S., N. Yokosawa, T. Kubota, T. Suzutani, I. Yoshida, S. Miura, K. Jimbow, and N. Fujii. 2001. Herpes simplex virus type 1 suppresses the interferon signaling pathway by inhibiting phosphorylation of STATs and Janus kinases during an early infection stage. Virology 286:119-124.
75. Yoneyama, M., W. Suhara, Y. Fukuhara, M. Fukuda, E. Nishida, and T. Fujita. 1998. Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/ p300. EMBO J. 17:1087-1095.