Antiviral signaling through pattern recognition receptors

Journal of Biochemistry

Volumn 141, Issue 2, 2007, Pages 137-145

  Kawai, Taro ^a   Akira, Shizuo ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Innate immunity; RIG I like RNA helicase; Signal transduction; Toll like receptor; Virus infection

Indexed keywords

INTERFERON; NUCLEIC ACID; PATTERN RECOGNITION RECEPTOR; RNA HELICASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; VIRUS RNA;

CARBOXY TERMINAL SEQUENCE; CYTOPLASM; DENDRITIC CELL; ENDOSOME; IMMUNE RESPONSE; INFECTION SENSITIVITY; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; VIRUS INFECTION;

ANIMALS; HUMANS; IMMUNITY, NATURAL; RECEPTORS, PATTERN RECOGNITION; RNA HELICASES; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 8; VIRUS DISEASES;

EID: 34248672889     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvm032     Document Type: Review

References (69)

1. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801
2. Kawai, T. and Akira, S. (2006) Innate immune recognition of viral infection. Nat. Immunol. 7, 131-137
3. Honda, K., Takaoka, A., and Taniguchi, T. (2006) Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25, 349-360
4. Kaisho, T. and Akira, S. (2006) Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 117, 979-987
5. Alexopoulou, L., Holt, A.C., Medzhitov, R., and Flavell, R.A. (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413, 732-738
6. Schulz, O., Diebold, S.S., Chen, M., Naslund, T.I., Nolte, M.A., Alexopoulou, L., Azuma, Y.T., Flavell, R.A., Liljestrom, P., and Reis e Sousa, C. (2005) Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 433, 887-892
7. Wang, T., Town, T., Alexopoulou, L., Anderson, J.F., Fikrig, E., and Flavell, R.A. (2004) Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 10, 1366-1373
8. Hemmi, H., Kaisho, T., Takeuchi, O., Sato, S., Sanjo, H., Hoshino, K., Horiuchi, T., Tomizawa, H., Takeda, K., and Akira, S. (2002) Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3, 196-200
9. Heil, F., Ahmad-Nejad, P., Hemmi, H., Hochrein, H., Ampenberger, F., Gellert, T., Dietrich, H., Lipford, G., Takeda, K., Akira, S., Wagner, H., and Bauer, S. (2003) The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily. Eur. J. Immunol. 33, 2987-2997
10. Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., Lipford, G., Wagner, H., and Bauer, S. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303, 1526-1529
11. Diebold, S.S., Kaisho, T., Hemmi, H., Akira, S., Reis, E., and Sousa, C. (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303, 1529-1531
12. Lund, J.M., Alexopoulou, L., Sato, A., Karow, M., Adams, N.C., Gale, N.W., Iwasaki, A., and Flavell, R.A. (2004) Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101, 5598-5603
13. Hornung, V., Guenthner-Biller, M., Bourquin, C., Ablasser, A., Schlee, M., Uematsu, S., Noronha, A., Manoharan, M., Akira, S., de Fougerolles, A., Endres, S., and Hartmann, G. (2005) Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med. 11, 263-270
14. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., and Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745
15. Krug, A., French, A.R., Barchet, W., Fischer, J.A., Dzionek, A., Pingel, J.T., Orihuela, M.M., Akira, S., Yokoyama, W.M., and Colonna, M. (2004) TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21, 107-119
16. Lund, J., Sato, A., Akira, S., Medzhitov, R., and Iwasaki, A. (2003) Toll-like receptor 9-mediated recognition of HSV-2 by plasmacytoid dendritic cells. J. Exp. Med. 198, 513-520
17. Barton, G.M., Kagan, J.C., and Medzhitov, R. (2006) Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat. Immunol. 7, 49-56
18. Colonna, M., Trinchieri, G., and Liu, Y.J. (2004) Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5, 1219-1226
19. Liu, Y.J. (2005) IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23, 275-306
20. Krug, A., Luker, G.D., Barchet, W., Leib, D.A., Akira, S., and Colonna, M. (2004) Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 103, 1433-1437
21. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K., Akira, S., and Fujita, T. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737
22. Hemmi, H., Takeuchi, O., Sato, S., Yamamoto, M., Kaisho, T., Sanjo, H., Kawai, T., Hoshino, K., Takeda, K., and Akira, S. (2004) The roles of two IkappaB Kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199, 1641-1650
23. Lopez, C.B., Moltedo, B., Alexopoulou, L., Bonifaz, L., Flavell, R.A., and Moran, T. M. (2004) TLR-independent induction of dendritic cell maturation and adaptive immunity by negative-strand RNA viruses. J. Immunol. 173, 6882-6889
24. Edelmann, K. H., Richardson-Burns, S., Alexopoulou, L., Tyler, K.L., Flavell, R.A., and Oldstone, M.B. (2004) Does toll-like receptor 3 play a biological role in virus infections? Virology 322, 231-238
25. Yoneyama, M., Kikuchi, M., Matsumoto, K., Imaizumi, T., Miyagishi, M., Taira, K., Foy, E., Loo, Y.M., Gale, M.J., Akira, S., Yonehara, S., Kato, A., and Fujita, T. (2005) Shared and unique functions of the DExD/H-Box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175, 2851-2858
26. Rothenfusser, S., Goutagny, N., DiPerna, G., Gong, M., Monks, B.G., Schoenemeyer, A., Yamamoto, M., Akira, S., and Fitzgerald, K.A. (2005) The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 175, 5260-5268
27. Kato, H., Sato, S., Yoneyama, M., Yamamoto, M., Uematsu, S., Matsui, K., Tsujimura, T., Takeda, K., Fujita, T., Takeuchi, O., and Akira, S. (2005) Cell type specific involvment of RIG-I in antiviral response. Immunity 23, 19-28
28. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., Uematsu, S., Jung, A., Kawai, T., Ishii, K. J., Yamaguchi, O., Otsu, K., Tsujimura, T., Koh, C.S., Reis e Sousa, C., Matsuura, Y., Fujita, T., and Akira, S. (2006) Differential role of MDA5 and RIG-I in the recognition of RNA viruses. Nature 441, 101-105
29. Gitlin, L., Barchet, W., Gilfillan, S., Cella, M., Beutler, B., Flavell, R.A., Diamond, M.S., and Colonna, M. (2006) Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103, 8459-8464
30. Hornung, V., Ellegast, J., Kim, S., Brzozka, K., Jung, A., Kato, H., Poeck, H., Akira, S., Conzelmann, K.K., Schlee, M., Endres, S., and Hartmann, G. (2006) 5′-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997
31. Pichlmair, A., Schulz, O., Tan, C.P., Naslund, T.I., Liljestrom, P., Weber, F., and Reis e Sousa, C. (2006) RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314, 997-1001
32. 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
33. Hoebe, K., Du, X., Georgel, P., Janssen, E., Tabeta, K., Kim, S.O., Goode, J., Lin, P., Mann, N., Mudd, S., Crozat, K., Sovath, S., Han, J., and Beutler, B. (2003) Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424, 743-748
34. 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
35. 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) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496
36. 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
37. Sato, S., Sugiyama, M., Yamamoto, M., Watanabe, Y., Kawai, T., Takeda, K., and Akira, S. (2003) Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-kappa B and IFN-regulatory factor-3, in the Toll-like receptor signaling. J. Immunol. 171, 4304-4310
38. Chen, Z.J. (2005) Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 7, 758-765
39. Meylan, E., Burns, K., Hofmann, K., Blancheteau, V., Martinon, F., Kelliher, M., and Tschopp, J. (2004) RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappaB activation. Nat. Immunol. 5, 503-507
40. Cusson-Hermance, N., Lee, T.H., Fitzgerald, K.A., and Kelliher, M.A. (2005) Rip1 mediates the Trif-dependent toll-like receptor 3 and 4-induced NF-kappa B activation but does not contribute to IRF-3 activation. J. Biol. Chem. 280, 36560-36566
41. 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
42. 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
43. Kawai, T., Sato, S., Ishii, K.J., Coban, C., Hemmi, H., Yamamoto, M., Terai, K., Matsuda, M., Inoue, J., Uematsu, S., Takeuchi, O., and Akira, S. (2004) Interferon-alpha induction through toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5, 1061-1068
44. Honda, K., Yanai, H., Mizutani, T., Negishi, H., Shimada, N., Suzuki, N., Ohba, Y., Takaoka, A., Yeh, W.C., and Taniguchi, T. (2004) Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 101, 15416-15421
45. Uematsu, S., Sato, S., Yamamoto, M., Hirotani, T., Kato, H., Takeshita, F., Matsuda, M., Coban, C., Ishii, K.J., Kawai, T., Takeuchi, O., and Akira, S. (2005) Interleukin-1 Receptor-Associated Kinase-1 (IRAK-1) plays an essential role for TLR7- and TLR9-mediated interferon-α induction. J. Exp. Med. 201, 915-923
46. Hoshino, K., Sugiyama, T., Matsumoto, M., Tanaka, T., Saito, M., Hemmi, H., Ohara, O., Akira, S., and Kaisho, T. (2006) IkappaB kinase-alpha is critical for interferon-alpha production induced by Toll-like receptors 7 and 9. Nature 440, 949-953
47. Tsujimura, H., Tamura, T., Kong, H.J., Nishiyama, A., Ishii, K.J., Klinman, D.M., and Ozato, K. (2004) Toll-like receptor 9 signaling activates NF-kappaB through IFN regulatory factor-8/IFN consensus sequence binding protein in dendritic cells. J. Immunol. 172, 6820-6827
48. Hacker, H., Redecke, V., Blagoev, B., Kratchmarova, I., Hsu, L.C., Wang, G.G., Kamps, M.P., Raz, E., Wagner, H., Hacker, G., Mann, M., and Karin, M. (2006) Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439, 204-207
49. 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
50. Shinohara, M.L., Lu, L., Bu, J., Werneck, M.B., Kobayashi, K.S., Glimcher, L.H., and Cantor, H. (2006) Osteopontin expression is essential for interferon-alpha production by plasmacytoid dendritic cells. Nat. Immunol. 7, 498-506
51. Negishi, H., Fujita, Y., Yanai, H., Sakaguchi, S., Ouyang, X., Shinohara, M., Takayanagi, H., Ohba, Y., Taniguchi, T., and Honda, K. (2006) Evidence for licensing of IFN-gamma-induced IFN regulatory factor 1 transcription factor by MyD88 in Toll-like receptor-dependent gene induction program. Proc. Natl. Acad. Sci. USA 103, 15136-15141
52. Takaoka, A., Yanai, H., Kondo, S., Duncan, G., Negishi, H., Mizutani, T., Kano, S.I., Honda, K., Ohba, Y., Mak, T.W., and Taniguchi, T. (2005) Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434, 243-249
53. Negishi, H., Ohba, Y., Yanai, H., Takaoka, A., Honma, K., Yui, K., Matsuyama, T., Taniguchi, T., and Honda, K. (2005) Negative regulation of Toll-like-receptor signaling by IRF-4. Proc. Natl. Acad. Sci. USA 102, 15989-15994
54. Kawai, T., Takahashi, K., Sato, S., Coban, C., Kumar, H., Kato, H., Ishii, K.J., Takeuchi, O., and Akira, S. (2005) IPS-1; an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6, 981-988
55. Seth, R.B., Sun, L., Ea, C.K., and Chen, Z.J. (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF3. Cell 122, 669-682
56. Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R., and Tschopp, J. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437, 1167-1172
57. Xu, L.G., Wang, Y.Y., Han, K.J., Li, L.Y., Zhai, Z., and Shu, H.B. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19, 727-740
58. Kumar, H., Kawai, T., Kato, H., Sato, S., Takahashi, K., Coban, C., Yamamoto, M., Uematsu, S., Ishii, K.J., Takeuchi, O., and Akira, S. (2006) Essential role of IPS-1 in innate immune responses against RNA viruses. J. Exp. Med. 203, 1795-1803
59. Sun, Q., Sun, L., Liu, H.H., Chen, X., Seth, R.B., Forman, J., and Chen, Z.J. (2006) The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24, 633-642
60. Saha, S.K., Pietras, E.M., He, J.Q., Kang, J.R., Liu, S.Y., Oganesyan, G., Shahangian, A., Zarnegar, B., Shiba, T.L., Wang, Y., and Cheng, G. (2006) Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. Embo J. 25, 3257-3263
61. Balachandran, S., Thomas, E., and Barber, G.N. (2004) A FADD-dependent innate immune mechanism in mammalian cells. Nature 432, 401-405
62. Takahashi, K., Kawai, T., Kumar, H., Sato, S., Yonehara, S., and Akira, S. (2006) Roles of Caspase-8 and Caspase-10 in antiviral innate immune responses. J. Immunol. 176, 4520-4524
63. Li, X.D., Sun, L., Seth, R.B., Pineda, G., and Chen, Z.J. (2005) Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc. Natl. Acad. Sci. USA 102, 17717-17722
64. Lin, R., Lacoste, J., Nakhaei, P., Sun, Q., Yang, L., Paz, S., Wilkinson, P., Julkunen, I., Vitour, D., Meurs, E., and Hiscott, J. (2006) Dissociation of a MAVS/IPS-1/VISA/ Cardif-IKKepsilon molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J. Virol. 80, 6072-6083
65. Loo, Y.M., Owen, D.M., Li, K., Erickson, A.K., Johnson, C.L., Fish, P.M., Carney, D. S., Wang, T., Ishida, H., Yoneyama, M., Fujita, T., Saito, T., Lee, W.M., Hagedorn, C. H., Lau, D.T., Weinman, S.A., Lemon, S.M., and Gale, M.J. (2006) Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. USA 103, 6001-6006
66. Li, K., Foy, E., Ferreon, J.C., Nakamura, M., Ferreon, A.C., Ikeda, M., Ray, S.C., Gale, M.J., and Lemon, S.M. (2005) Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. USA 102, 2992-2997
67. Ferreon, J.C., Ferreon, A.C., Li, K., and Lemon, S.M. (2005) Molecular determinants of TRIF proteolysis mediated by the hepatitis C virus NS3/4A protease. J. Biol. Chem. 280, 20483-20492
68. Ishii, K.J., Coban, C., Kato, H., Takahashi, K., Torii, Y., Takeshita, F., Ludwig, H., Sutter, G., Suzuki, K., Hemmi, H., Sato, S., Yamamoto, M., Uematsu, S., Kawai, T., Takeuchi, O., and Akira, S. (2006) A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 7, 40-48
69. Stetson, D.B. and Medzhitov, R. (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24, 93-103