A rhesus rhadinovirus viral interferon (IFN) regulatory factor is virion associated and inhibits the early IFN antiviral response

Journal of Virology

Volumn 89, Issue 15, 2015, Pages 7707-7721

  Morin, Gabriela ^a,b   Robinson, Bridget A ^a,b,d   Rogers, Kelsey S ^a,b,e   Wong, Scott W ^a,b,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR 3; PROTEIN BINDING; VIRAL INTERFERON REGULATORY FACTORS; VIRUS PROTEIN;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN HERPESVIRUS 8; IFN BETA GENE; IMMUNOELECTRON MICROSCOPY; IMMUNOMODULATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RHADINOVIRUS; RHESUS MACAQUE RHADINOVIRUS; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; VIRION; VIRUS IMMUNITY; VIRUS INHIBITION; ANIMAL; CELL LINE; GENETICS; HERPES VIRUS INFECTION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE EVASION; IMMUNOLOGY; RHESUS MONKEY; VIROLOGY;

CERCOPITHECINE HERPESVIRUS 17; HUMAN HERPESVIRUS 8;

ANIMALS; CELL LINE; CREB-BINDING PROTEIN; HERPESVIRIDAE INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTORS; INTERFERON-BETA; MACACA MULATTA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RHADINOVIRUS; VIRAL PROTEINS; VIRION;

EID: 84937680260     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01175-15     Document Type: Article

References (56)

1. Fitzgerald-Bocarsly P, Dai J, Singh S. 2008. Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev 19:3-19. http://dx.doi.org/10.1016/j.cytogfr.2007.10.006.
2. Ivashkiv LB, Donlin LT. 2014. Regulation of type I interferon responses. Nat Rev Immunol 14:36-49. http://dx.doi.org/10.1038/nri3581.
3. Sen GC. 2001. Viruses and interferons. Annu Rev Microbiol 55:255-281. http://dx.doi.org/10.1146/annurev.micro.55.1.255.
4. Taniguchi T, Ogasawara K, Takaoka A, Tanaka N. 2001. IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 19:623-655. http://dx.doi.org/10.1146/annurev.immunol.19.1.623.
5. Mamane Y, Heylbroeck C, Genin P, Algarte M, Servant MJ, LePage C, DeLuca C, Kwon H, Lin R, Hiscott J. 1999. Interferon regulatory factors: thenextgeneration. Gene 237:1-14.http://dx.doi.org/10.1016/S0378-1119(99)00262-0.
6. Areste C, Blackbourn DJ. 2009. Modulation of the immune system by Kaposi's sarcoma-associated herpesvirus. Trends Microbiol 17:119-129. http://dx.doi.org/10.1016/j.tim.2008.12.001.
7. Bowie AG, Unterholzner L. 2008. Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 8:911-922. http://dx.doi.org/10.1038/nri2436.
8. Rezaee SA, Cunningham C, Davison AJ, Blackbourn DJ. 2006. Kaposi's sarcoma-associated herpesvirus immune modulation: an overview. J Gen Virol 87:1781-1804. http://dx.doi.org/10.1099/vir.0.81919-0.
9. Alexander L, Denekamp L, Knapp A, Auerbach MR, Damania B, Desrosiers RC. 2000. The primary sequence of rhesus monkey rhadinovirus isolate 26-95: sequence similarities to Kaposi's sarcoma-associated herpesvirus and rhesus monkey rhadinovirus isolate 17577. J Virol 74: 3388-3398. http://dx.doi.org/10.1128/JVI.74.7.3388-3398.2000.
10. Moore PS, Gao SJ, Dominguez G, Cesarman E, Lungu O, Knowles DM, Garber R, Pellett PE, McGeoch DJ, Chang Y. 1996. Primary characterization of a herpesvirus agent associated with Kaposi's sarcoma. J Virol 70:549-558.
11. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, Moore PS. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA 93:14862-14867. http://dx.doi.org/10.1073/pnas.93.25.14862.
12. Searles RP, Bergquam EP, Axthelm MK, Wong SW. 1999. Sequence and genomic analysis of a rhesus macaque rhadinovirus with similarity to Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8. J Virol 73: 3040-3053.
13. Burysek L, Pitha PM. 2001. Latently expressed human herpesvirus 8-encoded interferon regulatory factor 2 inhibits double-stranded RNAactivated protein kinase. J Virol 75:2345-2352. http://dx.doi.org/10.1128/JVI.75.5.2345-2352.2001.
14. Burysek L, Yeow WS, Lubyova B, Kellum M, Schafer SL, Huang YQ, Pitha PM. 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.
15. Burysek L, Yeow WS, Pitha PM. 1999. Unique properties of a second human herpesvirus 8-encoded interferon regulatory factor (vIRF-2). J Hum Virol 2:19-32.
16. Lubyova B, Pitha PM. 2000. Characterization of a novel human herpesvirus 8-encoded protein, vIRF-3, that shows homology to viral and cellular interferon regulatory factors. J Virol 74:8194-8201. http://dx.doi.org/10.1128/JVI.74.17.8194-8201.2000.
17. Lubyova B, Kellum MJ, Frisancho AJ, Pitha PM. 2004. Kaposi's sarcoma-associated herpesvirus-encoded vIRF-3 stimulates the transcriptional activity of cellular IRF-3 and IRF-7. J Biol Chem 279:7643-7654. http://dx.doi.org/10.1074/jbc.M309485200.
18. Lin R, Genin P, Mamane Y, Sgarbanti M, Battistini A, Harrington WJ, Jr, Barber GN, Hiscott J. 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. http://dx.doi.org/10.1038/sj.onc.1204163.
19. Fuld S, Cunningham C, Klucher K, Davison AJ, Blackbourn DJ. 2006. Inhibition of interferon signaling by the Kaposi's sarcoma-associated herpesvirus full-length viral interferon regulatory factor 2 protein. J Virol 80:3092-3097. http://dx.doi.org/10.1128/JVI.80.6.3092-3097.2006.
20. Flowers C, Flowers S, Nabel G. 1998. Kaposi's sarcoma-associated herpesvirus viral interferon regulatory factor confers resistance to the antiproliferative effect of interferon-alpha. Mol Med 4:402-412.
21. Gao SJ, Boshoff C, Jayachandra S, Weiss RA, Chang Y, Moore PS. 1997. KSHV ORF K9 (vIRF) is an oncogene which inhibits the interferon signaling pathway. Oncogene 15:1979-1985. http://dx.doi.org/10.1038/sj.onc.1201571.
22. Joo CH, Shin YC, Gack M, Wu L, Levy D, Jung JU. 2007. Inhibition of interferon regulatory factor 7 (IRF7)-mediated interferon signal transduction by the Kaposi's sarcoma-associated herpesvirus viral IRF homolog vIRF3. J Virol 81:8282-8292. http://dx.doi.org/10.1128/JVI.00235-07.
23. Wies E, Hahn AS, Schmidt K, Viebahn C, Rohland N, Lux A, Schellhorn T, Holzer A, Jung JU, Neipel F. 2009. The Kaposi's sarcomaassociated herpesvirus-encoded vIRF-3 inhibits cellular IRF-5. J Biol Chem 284:8525-8538. http://dx.doi.org/10.1074/jbc.M809252200.
24. Zimring JC, Goodbourn S, Offermann MK. 1998. Human herpesvirus 8 encodes an interferon regulatory factor (IRF) homolog that represses IRF-1-mediated transcription. J Virol 72:701-707.
25. Mutocheluh M, Hindle L, Areste C, Chanas SA, Butler LM, Lowry K, Shah K, Evans DJ, Blackbourn DJ. 2011. Kaposi's sarcoma-associated herpesvirus viral interferon regulatory factor-2 inhibits type 1 interferon signalling by targeting interferon-stimulated gene factor-3. J Gen Virol 92:2394-2398. http://dx.doi.org/10.1099/vir.0.034322-0.
26. Li M, Damania B, Alvarez X, Ogryzko V, Ozato K, Jung JU. 2000. Inhibition of p300 histone acetyltransferase by viral interferon regulatory factor. Mol Cell Biol 20:8254-8263. http://dx.doi.org/10.1128/MCB.20.21.8254-8263.2000.
27. Seo T, Lee D, Lee B, Chung JH, Choe J. 2000. Viral interferon regulatory factor 1 of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) binds to, and inhibits transactivation of, CREB-binding protein. Biochem Biophys Res Commun 270:23-27. http://dx.doi.org/10.1006/bbrc.2000.2393.
28. Shin YC, Nakamura H, Liang X, Feng P, Chang H, Kowalik TF, Jung JU. 2006. Inhibition of the ATM/p53 signal transduction pathway by Kaposi's sarcoma-associated herpesvirus interferon regulatory factor 1. J Virol 80:2257-2266. http://dx.doi.org/10.1128/JVI.80.5.2257-2266.2006.
29. Rivas C, Thlick AE, Parravicini C, Moore PS, Chang Y. 2001. Kaposi's sarcoma-associated herpesvirus LANA2 is a B-cell-specific latent viral protein that inhibits p53. J Virol 75:429-438. http://dx.doi.org/10.1128/JVI.75.1.429-438.2001.
30. Nakamura H, Li M, Zarycki J, Jung JU. 2001. Inhibition of p53 tumor suppressor by viral interferon regulatory factor. J Virol 75:7572-7582. http://dx.doi.org/10.1128/JVI.75.16.7572-7582.2001.
31. Lee HR, Toth Z, Shin YC, Lee JS, Chang H, Gu W, Oh TK, Kim MH, Jung JU. 2009. Kaposi's sarcoma-associated herpesvirus viral interferon regulatory factor 4 targetsMDM2to deregulate the p53 tumor suppressor pathway. J Virol 83:6739-6747. http://dx.doi.org/10.1128/JVI.02353-08.
32. Kirchhoff S, Sebens T, Baumann S, Krueger A, Zawatzky R, Li-Weber M, Meinl E, Neipel F, Fleckenstein B, Krammer PH. 2002. Viral IFNregulatory factors inhibit activation-induced cell death via two positive regulatory IFN-regulatory factor 1-dependent domains in the CD95 ligand promoter. J Immunol 168:1226-1234. http://dx.doi.org/10.4049/jimmunol.168.3.1226.
33. Robinson BA, Estep RD, Messaoudi I, Rogers KS, Wong SW. 2012. Viral interferon regulatory factors decrease the induction of type I and type II interferon during rhesus macaque rhadinovirus infection. J Virol 86:2197-2211. http://dx.doi.org/10.1128/JVI.05047-11.
34. Robinson BA, O'Connor MA, Li H, Engelmann F, Poland B, Grant R, DeFilippis V, Estep RD, Axthelm MK, Messaoudi I, Wong SW. 2012. Viral interferon regulatory factors are critical for delay of the host immune response against rhesus macaque rhadinovirus infection. J Virol 86:2769-2779. http://dx.doi.org/10.1128/JVI.05657-11.
35. Estep RD, Powers MF, Yen BK, Li H, Wong SW. 2007. Construction of an infectious rhesus rhadinovirus bacterial artificial chromosome for the analysis of Kaposi's sarcoma-associated herpesvirus-related disease development. J Virol 81:2957-2969. http://dx.doi.org/10.1128/JVI.01997-06.
36. DeFilippis VR, Sali T, Alvarado D, White L, Bresnahan W, Fruh KJ. 2010. Activation of the interferon response by human cytomegalovirus occurs via cytoplasmic double-stranded DNA but not glycoprotein B. J Virol 84:8913-8925. http://dx.doi.org/10.1128/JVI.00169-10.
37. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG. 2005. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33:e36. http://dx.doi.org/10.1093/nar/gni035.
38. Kawai T, Akira S. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143:1-20. http://dx.doi.org/10.1196/annals.1443.020.
39. Genin P, Vaccaro A, Civas A. 2009. The role of differential expression of human interferon-a genes in antiviral immunity. Cytokine Growth Factor Rev 20:283-295. http://dx.doi.org/10.1016/j.cytogfr.2009.07.005.
40. Wathelet MG, Lin CH, Parekh BS, Ronco LV, Howley PM, Maniatis T. 1998. Virus infection induces the assembly of coordinately activated transcription factors on the IFN-beta enhancer in vivo. Mol Cell 1:507-518. http://dx.doi.org/10.1016/S1097-2765(00)80051-9.
41. Yang H, Lin CH, Ma G, Orr M, Baffi MO, Wathelet MG. 2002. Transcriptional activity of interferon regulatory factor (IRF)-3 depends on multiple protein-protein interactions. Eur J Biochem 269:6142-6151. http://dx.doi.org/10.1046/j.1432-1033.2002.03330.x.
42. Yoneyama M, Suhara W, Fukuhara Y, Fukuda M, Nishida E, Fujita T. 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. http://dx.doi.org/10.1093/emboj/17.4.1087.
43. Melroe GT, Silva L, Schaffer PA, Knipe DM. 2007. Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: potential role in blocking IFN-beta induction. Virology 360:305-321. http://dx.doi.org/10.1016/j.virol.2006.10.028.
44. Zhu FX, King SM, Smith EJ, Levy DE, Yuan Y. 2002. A Kaposi's sarcoma-associated herpesviral protein inhibits virus-mediated induction of type I interferon by blocking IRF-7 phosphorylation and nuclear accumulation. Proc Natl Acad Sci USA 99:5573-5578. http://dx.doi.org/10.1073/pnas.082420599.
45. Zhu FX, Sathish N, Yuan Y. 2010. Antagonism of host antiviral responses by Kaposi's sarcoma-associated herpesvirus tegument protein ORF45. PLoS One 5:e10573. http://dx.doi.org/10.1371/journal.pone.0010573.
46. Zhu FX, Yuan Y. 2003. The ORF45 protein of Kaposi's sarcomaassociated herpesvirus is associated with purified virions. J Virol 77:4221-4230. http://dx.doi.org/10.1128/JVI.77.7.4221-4230.2003.
47. Zhu FX, Chong JM, Wu L, Yuan Y. 2005. Virion proteins of Kaposi's sarcoma-associated herpesvirus. J Virol 79:800-811. http://dx.doi.org/10.1128/JVI.79.2.800-811.2005.
48. O'Connor CM, Kedes DH. 2006. Mass spectrometric analyses of purified rhesus monkey rhadinovirus reveal 33 virion-associated proteins. J Virol 80:1574-1583. http://dx.doi.org/10.1128/JVI.80.3.1574-1583.2006.
49. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. 1998. How cells respond to interferons. Annu Rev Biochem 67:227-264. http://dx.doi.org/10.1146/annurev.biochem.67.1.227.
50. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. 1999. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 17:189-220. http://dx.doi.org/10.1146/annurev.immunol.17.1.189.
51. Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ, Liew FY, Caligiuri MA, Durbin JE, Biron CA. 2002. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol 169:4279-4287. http://dx.doi.org/10.4049/jimmunol.169.8.4279.
52. Huber JP, Farrar JD. 2011. Regulation of effector and memory T-cell functions by type I interferon. Immunology 132:466-474. http://dx.doi.org/10.1111/j.1365-2567.2011.03412.x.
53. Marrack P, Kappler J, Mitchell T. 1999. Type I interferons keep activated T cells alive. J Exp Med 189:521-530. http://dx.doi.org/10.1084/jem.189.3.521.
54. Ito T, Amakawa R, Inaba M, Ikehara S, Inaba K, Fukuhara S. 2001. Differential regulation of human blood dendritic cell subsets by IFNs. J Immunol 166:2961-2969. http://dx.doi.org/10.4049/jimmunol.166.5.2961.
55. Luft T, Pang KC, Thomas E, Hertzog P, Hart DN, Trapani J, Cebon J. 1998. Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 161:1947-1953.
56. Montoya M, Schiavoni G, Mattei F, Gresser I, Belardelli F, Borrow P, Tough DF. 2002. Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 99:3263-3271. http://dx.doi.org/10.1182/blood.V99.9.3263.