Targeting IRFs by ubiquitination: Regulating antiviral responses

Biochemical Society Transactions

Volumn 36, Issue 3, 2008, Pages 453-458

  Higgs, Rowan ^a   Jefferies, Caroline A ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

Antiviral response; Cell signalling; Interferon regulatory factor (IRF); Toll like receptor; Type I interferon; Ubiquitination

Indexed keywords

INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 2; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 5; INTERFERON REGULATORY FACTOR 7; NONSTRUCTURAL PROTEIN 1; PROTEASOME; VIF PROTEIN; VPR PROTEIN;

ANTIVIRAL ACTIVITY; CONFERENCE PAPER; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; IMMUNE RESPONSE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TARGETING; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIVIRAL AGENTS; HUMANS; INTERFERON REGULATORY FACTORS; MOLECULAR SEQUENCE DATA; UBIQUITIN; UBIQUITINATION;

EID: 45249083451     PISSN: 03005127     EISSN: None     Source Type: Journal    
DOI: 10.1042/BST0360453     Document Type: Conference Paper

References (52)

1. Kawai, T. and Akira, S. (2006) Innate immune recognition of viral infection. Nat. Immunol. 7, 131-137
2. Isaacs, A. and Lindenmann, J. (1957) Virus interference. I. The interferon. Proc. R. Soc. London Ser. B 147, 258-267
3. Pichlmair, A. and Reis e Sousa, C. (2007) Innate recognition of viruses. Immunity 27, 370-383
4. Uematsu, S. and Akira, S. (2007) Toll-like receptors and type I interferons. J. Biol. Chem. 282, 15319-15323
5. Akira, S., Uematsu, S. and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801
6. Brandenburg, B. and Zhuang, X. (2007) Virus trafficking: learning from single-virus tracking. Nat. Rev. Microbiol. 5, 197-208
7. Ozato, K., Tailor, P. and Kubota, T. (2007) The interferon regulatory factor family in host defense: mechanism of action. J. Biol. Chem. 282, 20065-20069
8. Fitzgerald, K.A., McWhirter, S.M., Faia, K.L., Rowe, D.C., Latz, E., Golenbock, D.T., Coyle, A.J., Liao, S.M. and Maniatis, T. (2003) IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496
9. McWhirter, S.M., Fitzgerald, K.A., Rosains, J., Rowe, D.C., Golenbock, D.T. and Maniatis, T. (2004) IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 101, 233-238
10. Sharma, S., tenOever, B.R., Grandvaux, N., Zhou, G.P., Lin, R. and Hiscott, J. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151
11. Honda, K., Yanai, H., Negishi, H., Asagiri, M., Sato, M., Mizutani, T., Shimada, N., Ohba, Y., Takaoka, A., Yoshida, N. and Taniguchi, T. (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434, 772-777
12. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K. and Akira, S. (2003) Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301, 640-643
13. Hacker, H., Redecke, V., Blagoev, B., Kratchmarova, I., Hsu, L.C., Wang, G.G., Kamps, M.P., Raz, E., Wagner, H., Hacker, G. et al. (2006) Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439, 204-207
14. Oganesyan, G., Saha, S.K., Guo, B., He, J.Q., Shahangian, A., Zarnegar, B., Perry, A. and Cheng, G. (2006) Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 439, 208-211
15. Fitzgerald, K.A., Rowe, D.C., Barnes, B.J., Caffrey, D.R., Visintin, A., Latz, E., Monks, B., Pitha, P.M. and Golenbock, D.T. (2003) LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the Toll adapters TRAM and TRIF. J. Exp. Med. 198, 1043-1055
16. Yamamoto, M., Sato, S., Hemmi, H., Uematsu, S., Hoshino, K., Kaisho, T., Takeuchi, O., Takeda, K. and Akira, S. (2003) TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 4, 1144-1150
17. Kawai, T., Sato, S., Ishii, K.J., Coban, C., Hemmi, H., Yamamoto, M., Terai, K., Matsuda, M., Inoue, J., Uematsu, S. et al. (2004) Interferon-α induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5, 1061-1068
18. Uematsu, S., Sato, S., Yamamoto, M., Hirotani, T., Kato, H., Takeshita, F., Matsuda, M., Coban, C., Ishii, K.J., Kawai, T. et al. (2005) Interleukin-1 receptor-associated kinase-1 plays an essential role for Toll-like receptor (TLR)7- and TLR9-mediated interferon-α induction. J. Exp. Med. 201, 915-923
19. Schmitz, F., Heit, A., Guggemoos, S., Krug, A., Mages, J., Schiemann, M., Adler, H., Drexler, I., Haas, T., Lang, R. and Wagner, H. (2007) Interferon-regulatory-factor 1 controls Toll-like receptor 9-mediated IFN-β production in myeloid dendritic cells. Eur. J. Immunol. 37, 315-327
20. Gabriele, L. and Ozato, K. (2007) The role of the interferon regulatory factor (IRF) family in dendritic cell development and function. Cytokine Growth Factor Rev. 18, 503-510
21. Tamura, T., Thotakura, P., Tanaka, T.S., Ko, M.S. and Ozato, K. (2005) Identification of target genes and a unique eis element regulated by IRF-8 in developing macrophages. Blood 106, 1938-1947
22. Sciammas, R., Shaffer, A.L., Schatz, J.H., Zhao, H., Staudt, L.M. and Singh, H. (2006) Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25, 225-236
23. Harada, H., Kitagawa, M., Tanaka, N., Yamamoto, H., Harada, K., Ishihara, M. and Taniguchi, T. (1993) Anti-oncogenic and oncogenic potentials of interferon regulatory factors-1 and -2. Science 259, 971-974
24. Lin, R., Heylbroeck, C., Pitha, P.M. and Hiscott, J. (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
25. Yoneyama, M., Suhara, W., Fukuhara, Y., Fukuda, M., Nishida, E. and 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
26. Qin, B.Y., Liu, C., Lam, S.S., Srinath, H., Delston, R., Correia, J.J., Derynck, R. and Lin, K. (2003) Crystal structure of IRF-3 reveals mechanism of autoinhibition and virus-induced phosphoactivation. Nat. Struct. Biol. 10, 913-921
27. Sato, M., Suemori, H., Hata, N., Asagiri, M., Ogasawara, K., Nakao, K., Nakaya, T., Katsuki, M., Noguchi, S., Tanaka, N. and Taniguchi, T. (2000) Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity 13, 539-548
28. Sato, M., Hata, N., Asagiri, M., Nakaya, T., Taniguchi, T. and Tanaka, N. (1998) Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 441, 106-110
29. Caillaud, A., Hovanessian, A.G., Levy, D.E. and Marie, I.J. (2005) Regulatory serine residues mediate phosphorylation-dependent and phosphorylation-independent activation of interferon regulatory factor 7. J. Biol. Chem. 280, 17671-17677
30. tenOever, B.R., Sharma, S., Zou, W., Sun, Q., Grandvaux, N., Julkunen, I., Hemmi, H., Yamamoto, M., Akira, S., Yeh, W.C. et al. (2004) Activation of TBK1 and IKKε kinases by vesicular stomatitis virus infection and the role of viral ribonucleoprotein in the development of interferon antiviral immunity. J. Virol. 78, 10636-10649
31. Caillaud, A., Prakash, A., Smith, E., Masumi, A., Hovanessian, A.G., Levy, D.E. and Marie, I. (2002) Acetylation of interferon regulatory factor-7 by p300/CREB-binding protein (CBP)-associated factor (PCAF) impairs its DNA binding. J. Biol. Chem. 277, 49417-49421
32. Banchereau, J. and Pascual, V. (2006) Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 25, 383-392
33. Barrat, F.J., Meeker, T., Gregorio, J., Chan, J.H., Uematsu, S., Akira, S., Chang, B., Duramad, O. and Coffman, R.L. (2005) Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202, 1131-1139
34. Vollmer, J., Tluk, S., Schmitz, C., Hamm, S., Jurk, M., Forsbach, A., Akira, S., Kelly, K.M., Reeves, W.H., Bauer, S. and Krieg, A.M. (2005) Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J. Exp. Med. 202, 1575-1585
35. Ben-Neriah, Y. (2002) Regulatory functions of ubiquitination in the immune system. Nat. Immunol. 3, 20-26
36. Wang, J. and Maldonado, M.A. (2006) The ubiquitin-proteasome system and its role in inflammatory and autoimmune diseases. Cell. Mol. Immunol. 3, 255-261
37. Liu, Y.C. (2004) Ubiquitin ligases and the immune response. Annu. Rev. Immunol. 22, 81-127
38. Saitoh, T., Tun-Kyi, A., Ryo, A., Yamamoto, M., Finn, G., Fujita, T., Akira, S., Yamamoto, N., Lu, K.P. and Yamaoka, S. (2006) Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1. Nat. Immunol. 7, 598-605
39. Bibeau-Poirier, A., Gravel, S.P., Clement, J.F., Rolland, S., Rodier, G., Coulombe, P., Hiscott, J., Grandvaux, N., Meloche, S. and Servant, M.J. (2006) Involvement of the IκB kinase (IKK)-related kinases Tank-binding kinase 1/IKKi and cullin-based ubiquitin ligases in IFN regulatory factor-3 degradation. J. Immunol. 177, 5059-5067
40. Meroni, G. and Diez-Roux, G. (2005) TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. BioEssays 27, 1147-1157
41. Nisole, S., Stoye, J.P. and Saib, A. (2005) TRIM family proteins: retroviral restriction and antiviral defence. Nat. Rev. Microbiol. 3, 799-808
42. Kong, H.J., Anderson, D.E., Lee, C.H., Jang, M.K., Tamura, T., Tailor, P., Cho, H.K., Cheong, J., Xiong, H., Morse, III, H.C. and Ozato, K. (2007) Cutting edge: autoantigen ro52 is an interferon inducible E3 ligase that ubiquitinates IRF-8 and enhances cytokine expression in macrophages. J. Immunol. 179, 26-30
43. Barro, M. and Patton, J.T. (2005) Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc. Natl. Acad. Sci. U.S.A. 102, 4114-4119
44. Graff, J.W., Ewen, J., Ettayebi, K. and Hardy, M.E. (2007) Zinc-binding domain of rotavirus NSP1 is required for proteasome-dependent degradation of IRF3 and autoregulatory NSP1 stability. J. Gen. Virol. 88, 613-620
45. pro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J. Virol. 81, 3087-3096
46. Pro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J. Virol. 80, 11723-11732
47. Saira, K., Zhou, Y. and Jones, C. (2007) The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and, consequently, inhibits β interferon promoter activity. J. Virol. 81, 3077-3086
48. Melroe, G.T., Silva, L., Schaffer, P.A. and Knipe, D.M. (2007) Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: potential role in blocking IFN-β induction. Virology 360, 305-321
49. Okumura, A., Alce, T., Lubyova, B., Ezelle, H., Strebel, K. and Pitha, P.M. (2007) HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 373, 85-97
50. Nakagawa, K. and Yokosawa, H. (2000) Degradation of transcription factor IRF-1 by the ubiquitin-proteasome pathway: the C-terminal region governs the protein stability. Eur. J. Biochem. 267, 1680-1686
51. Xiong, H., Li, H., Kong, H.J., Chen, Y., Zhao, J., Xiong, S., Huang, B., Gu, H., Mayer, L., Ozato, K. and Unkeless, J.C. (2005) Ubiquitin-dependent degradation of interferon regulatory factor-8 mediated by Cbl down-regulates interleukin-12 expression. J. Biol. Chem. 280, 23531-23539
52. Huye, L.E., Ning, S., Kelliher, M. and Pagano, J.S. (2007) Interferon regulatory factor 7 is activated by a viral oncoprotein through RIP-dependent ubiquitination. Mol. Cell. Biol. 27, 2910-2918