Conserved Herpesviral Kinase Promotes Viral Persistence by Inhibiting the IRF-3-Mediated Type I Interferon Response

Cell Host and Microbe

Volumn 5, Issue 2, 2009, Pages 166-178

  Hwang, Seungmin ^a   Kim, Kyeong Seon ^a   Flano, Emilio ^c   Wu, Ting Ting ^a   Tong, Leming M ^a   Park, Ann N ^b   Song, Moon Jung ^d   Sanchez, David Jesse ^b   O'Connell, Ryan M ^b   Cheng, Genhong ^c   Sun, Ren ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONWIDE CHILDREN S HOSPITAL   (United States)

^d Korea University   (South Korea)

Author keywords

MICROBIO; MOLIMMUNO

Indexed keywords

BETA INTERFERON; HISTONE ACETYLTRANSFERASE PCAF; INTERFERON; INTERFERON REGULATORY FACTOR 3; RNA POLYMERASE II; VIRUS ENZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONSERVATION GENETICS; CONTROLLED STUDY; ENZYME ACTIVITY; HERPES VIRUS; IMMUNE RESPONSE; LUNG INFECTION; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; VIRUS INFECTION; VIRUS VIRULENCE;

ANIMALS; HERPESVIRIDAE INFECTIONS; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; LUNG; MEMBRANE PROTEINS; MICE; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN KINASES; RHADINOVIRUS; SPLEEN; VIRAL PROTEINS; VIRULENCE; VIRULENCE FACTORS;

HERPESVIRIDAE; MURINAE; MURINE HEPATITIS VIRUS;

EID: 60649109368     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2008.12.013     Document Type: Article

References (52)

1. Agnello D., Lankford C.S., Bream J., Morinobu A., Gadina M., O'Shea J.J., and Frucht D.M. Cytokines and transcription factors that regulate T helper cell differentiation: New players and new insights. J. Clin. Immunol. 23 (2003) 147-161
2. Asai R., Kato A., Kato K., Kanamori-Koyama M., Sugimoto K., Sairenji T., Nishiyama Y., and Kawaguchi Y. Epstein-Barr virus protein kinase BGLF4 is a virion tegument protein that dissociates from virions in a phosphorylation-dependent process and phosphorylates the viral immediate-early protein BZLF1. J. Virol. 80 (2006) 5125-5134
3. Asai R., Ohno T., Kato A., and Kawaguchi Y. Identification of proteins directly phosphorylated by UL13 protein kinase from herpes simplex virus 1. Microbes Infect. 9 (2007) 1434-1438
4. Barchet W., Cella M., Odermatt B., Asselin-Paturel C., Colonna M., and Kalinke U. Virus-induced interferon alpha production by a dendritic cell subset in the absence of feedback signaling in vivo. J. Exp. Med. 195 (2002) 507-516
5. Barton E.S., Lutzke M.L., Rochford R., and Virgin IV H.W. Alpha/beta interferons regulate murine gammaherpesvirus latent gene expression and reactivation from latency. J. Virol. 79 (2005) 14149-14160
6. Bechtel J.T., Winant R.C., and Ganem D. Host and viral proteins in the virion of Kaposi's sarcoma-associated herpesvirus. J. Virol. 79 (2005) 4952-4964
7. Bortz E., Whitelegge J.P., Jia Q., Zhou Z.H., Stewart J.P., Wu T.-T., and Sun R. Identification of proteins associated with murine gammaherpesvirus 68 virions. J. Virol. 77 (2003) 13425-13432
8. Braaten D.C., Sparks-Thissen R.L., Kreher S., Speck S.H., and Virgin IV H.W. An optimized CD8+ T-cell response controls productive and latent gammaherpesvirus infection. J. Virol. 79 (2005) 2573-2583
9. Compton T., Kurt-Jones E.A., Boehme K.W., Belko J., Latz E., Golenbock D.T., and Finberg R.W. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 77 (2003) 4588-4596
10. Dalod M., Salazar-Mather T.P., Malmgaard L., Lewis C., Asselin-Paturel C., Briere F., Trinchieri G., and Biron C.A. Interferon alpha/beta and interleukin 12 responses to viral infections: Pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 195 (2002) 517-528
11. Davis D.A., Singer K.E., Reynolds I.P., Haque M., and Yarchoan R. Hypoxia enhances the phosphorylation and cytotoxicity of ganciclovir and zidovudine in Kaposi's sarcoma-associated herpesvirus infected cells. Cancer Res. 67 (2007) 7003-7010
12. Doyle S., Vaidya S., O'Connell R., Dadgostar H., Dempsey P., Wu T., Rao G., Sun R., Haberland M., Modlin R., et al. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17 (2002) 251-263
13. Durand V., Wong S.Y., Tough D.F., and Le Bon A. Shaping of adaptive immune responses to soluble proteins by TLR agonists: A role for IFN-alpha/beta. Immunol. Cell Biol. 82 (2004) 596-602
14. Ebrahimi B., Dutia B.M., Roberts K.L., Garcia-Ramirez J.J., Dickinson P., Stewart J.P., Ghazal P., Roy D.J., and Nash A.A. Transcriptome profile of murine gammaherpesvirus-68 lytic infection. J. Gen. Virol. 84 (2003) 99-109
15. Garcia M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., and Esteban M. Impact of protein kinase PKR in cell biology: From antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 70 (2006) 1032-1060
16. Gershburg E., and Pagano J.S. Conserved herpesvirus protein kinases. Biochim. Biophys. Acta. 1784 (2008) 203-212
17. Hamza M.S., Reyes R.A., Izumiya Y., Wisdom R., Kung H.-J., and Luciw P.A. ORF36 protein kinase of Kaposi's sarcoma herpesvirus activates the c-Jun N-terminal kinase signaling pathway. J. Biol. Chem. 279 (2004) 38325-38330
18. Haque M., Wang V., Davis D.A., Zheng Z.-M., and Yarchoan R. Genetic organization and hypoxic activation of the Kaposi's sarcoma-associated herpesvirus ORF34-37 gene cluster. J. Virol. 80 (2006) 7037-7051
19. Hiscott J. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 282 (2007) 15325-15329
20. Hwang S., Wu T.T., Tong L.M., Kim K.S., Martinez-Guzman D., Colantonio A.D., Uittenbogaart C.H., and Sun R. Persistent gammaherpesvirus replication and dynamic interaction with the host in vivo. J. Virol. 82 (2008) 12498-12509
21. Izumiya Y., Izumiya C., Van Geelen A., Wang D.-H., Lam K.S., Luciw P.A., and Kung H.-J. Kaposi's sarcoma-associated herpesvirus-encoded protein kinase and its interaction with K-bZIP. J. Virol. 81 (2007) 1072-1082
22. Katze M.G., He Y., and Gale M. Viruses and interferon: A fight for supremacy. Nat. Rev. Immunol. 2 (2002) 675-687
23. Kawaguchi Y., and Kato K. Protein kinases conserved in herpesviruses potentially share a function mimicking the cellular protein kinase cdc2. Rev. Med. Virol. 13 (2003) 331-340
24. Kolumam G.A., Thomas S., Thompson L.J., Sprent J., and Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202 (2005) 637-650
25. Le Bon A., Etchart N., Rossmann C., Ashton M., Hou S., Gewert D., Borrow P., and Tough D.F. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat. Immunol. 4 (2003) 1009-1015
26. Lee C.-P., Chen J.-Y., Wang J.-T., Kimura K., Takemoto A., Lu C.-C., and Chen M.-R. Epstein-Barr virus BGLF4 kinase induces premature chromosome condensation through activation of condensin and topoisomerase II. J. Virol. 81 (2007) 5166-5180
27. Li X.L., Blackford J.A., and Hassel B.A. RNase L mediates the antiviral effect of interferon through a selective reduction in viral RNA during encephalomyocarditis virus infection. J. Virol. 72 (1998) 2752-2759
28. Lin R., Heylbroeck C., Pitha P.M., and Hiscott J. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18 (1998) 2986-2996
29. Lin R., Mamane Y., and Hiscott J. Structural and functional analysis of interferon regulatory factor 3: Localization of the transactivation and autoinhibitory domains. Mol. Cell. Biol. 19 (1999) 2465-2474
30. Lund J., Sato A., Akira S., Medzhitov R., and Iwasaki A. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 198 (2003) 513-520
31. Marrack P., Kappler J., and Mitchell T. Type I interferons keep activated T cells alive. J. Exp. Med. 189 (1999) 521-530
32. Martinez-Guzman D., Rickabaugh T., Wu T.T., Brown H., Cole S., Song M.J., Tong L., and Sun R. Transcription program of murine gammaherpesvirus 68. J. Virol. 77 (2003) 10488-10503
33. Michel D., and Mertens T. The UL97 protein kinase of human cytomegalovirus and homologues in other herpesviruses: Impact on virus and host. Biochim. Biophys. Acta. 1697 (2004) 169-180
34. Morrison L.A. The Toll of herpes simplex virus infection. Trends Microbiol. 12 (2004) 353-356
35. Mossman K.L., and Ashkar A.A. Herpesviruses and the innate immune response. Viral Immunol. 18 (2005) 267-281
36. Overton H.A., McMillan D.J., Klavinskis L.S., Hope L., Ritchie A.J., and Wong-kai-in P. Herpes simplex virus type 1 gene UL13 encodes a phosphoprotein that is a component of the virion. Virology 190 (1992) 184-192
37. Player M.R., and Torrence P.F. The 2-5 A system: Modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacol. Ther. 78 (1998) 55-113
38. Qin B.Y., Liu C., Srinath H., Lam S.S., Correia J.J., Derynck R., and Lin K. Crystal structure of IRF-3 in complex with CBP. Structure 13 (2005) 1269-1277
39. Sharma S., tenOever B.R., Grandvaux N., Zhou G.P., Lin R., and Hiscott J. Triggering the interferon antiviral response through an IKK-related pathway. Science 300 (2003) 1148-1151
40. Simmen K.A., Singh J., Luukkonen B.G., Lopper M., Bittner A., Miller N.E., Jackson M.R., Compton T., and Früh K. Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc. Natl. Acad. Sci. USA 98 (2001) 7140-7145
41. Smith G.A., and Enquist L.W. Construction and transposon mutagenesis in Escherichia coli of a full-length infectious clone of pseudorabies virus, an alphaherpesvirus. J. Virol. 73 (1999) 6405-6414
42. Song M.J., Hwang S., Wong W.H., Wu T.T., Lee S., Liao H.I., and Sun R. Identification of viral genes essential for replication of murine gamma-herpesvirus 68 using signature-tagged mutagenesis. Proc. Natl. Acad. Sci. USA 102 (2005) 3805-3810
43. Sparks-Thissen R.L., Braaten D.C., Kreher S., Speck S.H., and Virgin IV H.W. An optimized CD4 T-cell response can control productive and latent gammaherpesvirus infection. J. Virol. 78 (2004) 6827-6835
44. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., and Schreiber R.D. How cells respond to interferons. Annu. Rev. Biochem. 67 (1998) 227-264
45. Stevenson P.G., and Efstathiou S. Immune mechanisms in murine gammaherpesvirus-68 infection. Viral Immunol. 18 (2005) 445-456
46. Sunil-Chandra N.P., Arno J., Fazakerley J., and Nash A.A. Lymphoproliferative disease in mice infected with murine gammaherpesvirus 68. Am. J. Pathol. 145 (1994) 818-826
47. Taniguchi T., and Takaoka A. The interferon-alpha/beta system in antiviral responses: A multimodal machinery of gene regulation by the IRF family of transcription factors. Curr. Opin. Immunol. 14 (2002) 111-116
48. Tarakanova V.L., Leung-Pineda V., Hwang S., Yang C.-W., Matatall K., Basson M., Sun R., Piwnica-Worms H., Sleckman B.P., and Virgin IV H.W. Gamma-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe 1 (2007) 275-286
49. Varnum S.M., Streblow D.N., Monroe M.E., Smith P., Auberry K.J., Pasa-Tolic L., Wang D., Camp II D.G., Rodland K., Wiley S., et al. Identification of proteins in human cytomegalovirus (HCMV) particles: The HCMV proteome. J. Virol. 78 (2004) 10960-10966
50. Weslow-Schmidt J.L., Jewell N.A., Mertz S.E., Simas J.P., Durbin J.E., and Flano E. Type I interferon inhibition and dendritic cell activation during gammaherpesvirus respiratory infection. J. Virol. 81 (2007) 9778-9789
51. Wherry E.J., Puorro K.A., Porgador A., and Eisenlohr L.C. The induction of virus-specific CTL as a function of increasing epitope expression: Responses rise steadily until excessively high levels of epitope are attained. J. Immunol. 163 (1999) 3735-3745
52. Zhu F.X., Chong J.M., Wu L., and Yuan Y. Virion proteins of Kaposi's sarcoma-associated herpesvirus. J. Virol. 79 (2005) 800-811