Toll-IL-1-receptor-containing adaptor molecule-1: A signaling adaptor linking innate immunity to adaptive immunity

Progress in Molecular Biology and Translational Science

Volumn 117, Issue , 2013, Pages 487-510

  Matsumoto, Misako ^a   Funami, Kenji ^a   Oshiumi, Hiroyuki ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Adaptor protein; Adjuvant; Cross presentation; Dendritic cells; Double stranded RNA; Innate immunity; Toll like receptor; Type I interferon; Virus infection

Indexed keywords

BETA INTERFERON; DOUBLE STRANDED RNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1 RECEPTOR; MEMBRANE PROTEIN; PATTERN RECOGNITION RECEPTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTION FACTOR AP 1;

ADAPTIVE IMMUNITY; ANIMAL; APOPTOSIS; ARTICLE; CELL MATURATION; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; NATURAL KILLER CELL; NECROPTOSIS; OLIGOMERIZATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; VIRUS INFECTION;

EID: 84896708687     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386931-9.00018-0     Document Type: Chapter

References (113)

1. C.A. Janeway Jr., and R. Medzhitov Innate immune recognition Annu Rev Immunol 20 2002 197 216
2. S. Akira, S. Uematsu, and O. Takeuchi Pathogen recognition and innate immunity Cell 124 2006 783 801
3. A. Marshak-Rothstein Toll-like receptors in systemic autoimmune disease Nat Rev Immunol 6 2006 823 835
4. H. Kono, and K.L. Rock How dying cells alert the immune system to danger Nat Rev Immunol 8 2008 279 289
5. R. Medzhitov, P. Preston-Hurburt, and C.A. Janeway Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity Nature 388 1997 394 397
6. J.K. Bell, G.E.D. Mullen, C.A. Leifer, A. Mazzoni, D.R. Davies, and D.M. Segal Leucine-rich repeats and pathogen recognition in Toll-like receptors Trends Immunol 24 2003 528 533
7. N.J. Gay, M. Gangloff, and A.N.R. Weber Toll-like receptors as molecular switches Nat Rev Immunol 6 2006 693 698
8. L.A.J. O'Neill, and A.G. Bowie The family of five: TIR-domain-containing adaptors in Toll-like receptor signaling Nat Rev Immunol 7 2007 353 364
9. T. Kawai, S. Sato, K.J. Ishii, C. Coban, H. Hemmi, and M. Yamamoto Interferon-α induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6 Nat Immunol 5 2004 1061 1068
10. H. Oshiumi, M. Matsumoto, K. Funami, T. Akazawa, and T. Seya TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction Nat Immunol 4 2003 161 167
11. M. Yamamoto, S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, and H. Sanjo Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway Science 301 2003 640 643
12. H. Oshiumi, M. Sasai, K. Shida, T. Fujita, M. Matsumoto, and T. Seya TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to Toll-like receptor 4 TICAM-1 that induces interferon-β J Biol Chem 278 2003 49751 49762
13. K.A. Fitzgerald, D.C. Rowe, B.J. Barnes, D.R. Caffrey, A. Visintin, and E. Latz LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the toll adapters TRAM and TRIF J Exp Med 198 2003 1043 1055
14. K.A. Fitzgerald, E.M. Palsson-McDermott, A.G. Bowie, C.A. Jefferies, A.S. Mansell, and G. Brady Mal (Myd88-adapter-like) is required for Toll-like receptor 4 signal transduction Nature 413 2001 78 83
15. T. Horng, G.M. Barton, and R. Medzhitov TIRAP: an adaptor molecule in the Toll signaling pathway Nat Immunol 2 2001 835 841
16. M. Carty, R. Goodbody, M. Schroder, J. Stack, P.N. Moynagh, and A. Bowie The human afdaptor SARM nrgatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling Nat Immunol 7 2006 1074 1081
17. L. Alexopoulou, A.C. Holt, R. Medzhitov, and R.A. Flavell Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3 Nature 413 2001 732 738
18. M. Matsumoto, S. Kikkawa, M. Kohase, K. Miyake, and T. Seya Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling Biochem Biophys Res Commun 239 2002 1364 1369
19. M. Yoneyama, M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, and M. Miyagishi The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nat Immunol 5 2004 730 737
20. V. Hornung, J. Ellegast, S. Kim, K. Brzózka, A. Jung, and H. Kato 5′-Triphosphate RNA is ligand for RIG-I Science 314 2006 994 997
21. A. Pichlmair, O. Schulz, C.P. Tan, T.I. Näslund, P. Liljeström, and F. Weber RIG-I-mediated anti-viral responses to single-stranded RNA bearing 5′-phosphates Science 314 2006 997 1001
22. H. Kato, O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, and K. Matsushita Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5 J Exp Med 205 2008 1601 1610
23. T. Kawai, K. Takahashi, S. Sato, C. Coban, H. Kumar, and H. Kato IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction Nat Immunol 6 2005 981 988
24. R.B. Seth, L. Sun, C.K. Ea, and Z.J. Chen Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3 Cell 122 2005 669 682
25. E. Meylan, J. Curran, K. Hofmann, D. Moradpour, M. Binder, and R. Bartenschlager Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus Nature 437 2005 1167 1172
26. L.G. Xu, Y.Y. Wang, K.J. Han, L.Y. Li, Z. Zhai, and H.B. Shu VISA is an adapter protein required for virus-triggered IFN-beta signaling Mol Cell 19 2005 727 740
27. Z. Zhang, T. Kim, M. Bao, V. Facchinetti, S.Y. Jung, and A.A. Ghaffari DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cells Immunity 34 2011 866 878
28. C. Farina, M. Krumbholz, T. Giese, G. Hartmann, F. Aloisi, and E. Meinl Preferential expression and function of Toll-like receptor 3 in human astrocytes J Neuroimmunol 159 2005 12 19
29. T. Town, D. Jeng, L. Alexopoulou, J. Tan, and R.A. Flavell Microglia recognize double-stranded RNA via TLR3 J Immunol 176 2006 3804 3812
30. M. Muzio, D. Bosisio, N. Polentarutti, G. D'amico, A. Stoppacciaro, and R. Mancinelli Differential expression and regulation of Toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells J Immunol 64 2000 5998 6004
31. A. Visintin, A. Mazzoni, J.H. Spitzer, D.H. Wyllie, S.K. Dower, and D.M. Segal Regulation of Toll-like receptors in human monocytes and dendritic cells J Immunol 166 2001 249 254
32. N. Kadowaki, S. Ho, S. Antonenko, R.W. Malefyt, R.A. Kastelein, and F. Bazan Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens J Exp Med 194 2001 863 870
33. V. Hornung, S. Rothenfusser, S. Britisch, A. Krug, B. Jahrsdörfer, and T. Giese Quantitative expression of Toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides J Immunol 168 2002 4531 4537
34. M. Matsumoto, K. Funami, M. Tanabe, H. Oshiumi, M. Shingai, and Y. Seto Subcellular localization of Toll-like receptor 3 in human dendritic cells J Immunol 171 2003 3154 3162
35. S.L. Jongbloed, A.J. Kassianos, K.J. McDonald, G.J. Clark, X. Ju, and C.E. Angel Human CD141 + (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens J Exp Med 207 2010 1247 1260
36. L.F. Poulin, M. Salio, E. Griessinger, F. Anjos-Afonso, L. Craciun, and J.L. Chen Characterization of human DNGR-1 + BDCA3 + leukocytes as putative equivalents of mouse CD8α + dendritic cells J Exp Med 207 2010 1261 1271
37. M. Matsumoto, and T. Seya TLR3: interferon induction by double-stranded RNA including poly(I:C) Adv Drug Deliv Rev 60 2008 805 812
38. M. Miettinen, T. Sareneva, I. Julkunen, and S. Matikainen IFNs activate toll-like receptor gene expression in viral infections Genes Immun 2 2001 349 355
39. M.M. Brinkmann, E. Spooner, K. Hoebe, B. Beutler, and H.L. Ploegh The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling J Cell Biol 177 2007 265 275
40. K. Funami, M. Matsumoto, H. Oshiumi, T. Akazawa, A. Yamamoto, and T. Seya The cytoplasmic 'linker region' in Toll-like receptor 3 controls receptor localization and signaling Int Immunol 16 2004 1143 1154
41. T. Nishiya, E. Kajita, S. Miwa, and A. DeFranco TLR3 and TLR7 are targeted to the same intracellular compartments by distinct regulatory elements J Biol Chem 280 2005 37107 37117
42. T. Seya, M. Matsumoto, T. Ebihara, and H. Oshiumi Functional evolution of the TICAM-1 pathway for extrinsic RNA sensing Immunol Rev 227 2009 44 53
43. J. Choe, M.S. Kelker, and I.A. Wilson Crystal structure of human Toll-like receptor 3 (TLR3) ectodomain Science 309 2005 581 585
44. J.K. Bell, I. Botos, P.R. Hall, J. Askins, J. Shiloach, and D.M. Segal The molecular structure of the Toll-like receptor 3 ligand-binding domain Proc Natl Acad Sci USA 102 2005 10976 10980
45. L. Liu, I. Botos, Y. Wang, J.N. Leonard, J. Shiloach, and D.M. Segal Structural basis of Toll-like receptor 3 signaling with double-stranded RNA Science 320 2008 379 381
46. J.K. Bell, J. Askins, P.R. Hall, D.R. Davies, and D.M. Segal The dsRNA binding site of human Toll-like receptor 3 Proc Natl Acad Sci USA 103 2006 8792 8797
47. K. Fukuda, T. Watanabe, T. Tokisue, T. Tsujita, S. Nishikawa, and T. Hasegawa Modulation of double-stranded RNA recognition by the N-terminal histidine-rich region of the human Toll-like receptor 3 J Biol Chem 283 2008 22787 22794
48. N. Pirher, K. Ivicak, J. Pohar, M. Bencina, and R. Jerala A second binding site for double-stranded RNA in TLR3 and consequences for interferon activation Nat Struct Mol Biol 15 2008 761 763
49. Y. Wang, L. Liu, D.R. Davies, and D.M. Segal Dimerization of Till-like receptor 3 (TLR3) is required for ligand binding J Biol Chem 285 2010 36836 36841
50. J.N. Leonard, R. Ghirlando, J. Askins, J.K. Bell, D.H. Margulies, and D.R. Davies The TLR3 signaling complex forms by cooperative receptor dimerization Proc Natl Acad Sci USA 105 2008 258 263
51. I. Jelinek, J.N. Leonard, G.E. Price, K.N. Brown, A. Meyer-Manlapat, and P.K. Goldsmith TLR3-specific double-stranded RNA oligonucleotide adjuvants induce dendritic cell cross-presentation, CTL responses, and antiviral protection J Immunol 186 2011 2422 2429
52. K. Itoh, A. Watanabe, K. Funami, T. Seya, and M. Matsumoto The clathrin-mediated endocytic pathway participates in dsRNA-induced IFN-β production J Immunol 181 2008 5522 5529
53. A. Watanabe, M. Tatematsu, K. Saeki, S. Shibata, H. Shime, and A. Yoshimura Raftlin is involved in the nucleocapture complex to induce poly(I:C)-mediated TLR3 activation J Biol Chem 286 2011 10702 10711
54. H.K.S. Lee, K. Dunzendorfer, K. Soldau, and P.S. Tobias Double-stranded RNA-mediated TLR3 activation is enhanced by CD14 Immunity 24 2006 153 163
55. G.V. Limmon, M. Arredouani, K.L. McCann, R.A.C. Minor, L. Kobzik, and F. Imani Scavenger receptor class-A is a novel cell surface receptor for double-stranded RNA FASEB J 22 2008 159 167
56. C. Weber, C. Müller, A. Podszuweit, C. Montino, J. Vollmer, and A. Forsbach Toll-like receptor (TLR) 3 immune modulation by unformulated small interfering RNA or DNA and the role of CD14 (in TLR-mediated effects) Immunology 136 2012 64 77
57. S. Akashi, S. Saitoh, Y. Wakabayashi, T. Kikuchi, N. Takamura, and Y. Nagai Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14 J Exp Med 198 2003 1035 1042
58. J.C. Kagan, and R. Medzhitov Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling Cell 125 2006 943 955
59. J.C. Kagan, T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β Nat Immunol 9 2008 361 368
60. T. Seya, H. Oshiumi, M. Sasai, T. Akazawa, and M. Matsumoto TICAM-1 and TICAM-2: toll-like receptor adapters that participate in induction of type I interferons Int J Biochem Cell Biol 37 2005 524 529
61. K. Funami, M. Sasai, H. Oshiumi, T. Seya, and M. Matsumoto Homo-oligomerization is essential for Toll/IL-1 receptor domain-containing adaptor molecule-1 mediated NF-κB and IRF-3 activation J Biol Chem 283 2008 18283 18291
62. S. Sato, M. Sugiyama, M. Yamamoto, Y. Watanabe, T. Kawai, and K. Takeda Toll/IL-1 receptor domain-containing adaptor-inducing IFN-β (TRIF) associates with TNFR-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-κB and IFN-regulatory factor 3, in the Toll-like receptor signaling J Immunol 171 2003 4304 4310
63. M. Sasai, M. Tatematsu, H. Oshiumi, K. Funami, M. Matsumoto, and S. Hatakeyama Direct binding of TRAF2 and TRAF6 to TICAM-1/TRIF adaptor participates in activation of the Toll-like receptor 3/4 pathway Mol Immunol 47 2010 1283 1291
64. M. Tatematsu, A. Ishii, H. Oshiumi, M. Horiuchi, F. Inagaki, and T. Seya A molecular mechanism for Toll/IL-1 receptor domain-containing adaptor molecule-1-mediated IRF-3 activation J Biol Chem 285 2010 20128 20136
65. E. Meylan, K. Burns, K. Hofmann, V. Blancheteau, F. Martinon, and M. Kelliher RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation Nat Immunol 5 2004 503 507
66. K.J. Han, X. Su, L.G. Xu, L.H. Bin, J. Zhang, and H.B. Shu Mechanisms of the TRIF-induced interferon-stimulated response element and NF-kappaB activation and apoptosis pathways J Biol Chem 279 2004 15652 15661
67. W.J. Kaiser, and M.K. Offermann Apoptosis induced by the Toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif J Immunol 174 2005 4942 4952
68. K. Funami, M. Sasai, Y. Ohba, H. Oshiumi, T. Seya, and M. Matsumoto Spatiotemporal mobilization of Toll-IL-1 receptor domain-containing adaptor molecule 1 in response to dsRNA J Immunol 179 2007 6867 6872
69. S. Sharma, B.R. tenOever, N. Grandvaux, G.P. Zhou, R. Lin, and J. Hiscott Triggering the interferon antiviral response through an IKK-related pathway Science 300 2003 1148 1151
70. K.A. Fitzgerald, S.M. McWhirter, K.L. Faia, D.C. Rowe, E. Latz, and D.T. Golenbock IKKε and TBK1 are essential components of the IRF3 signaling pathway Nat Immunol 4 2003 491 496
71. H. Hacker, V. Redecke, B. Blagoev, I. Kratchmarova, L.C. Hsu, and G.G. Wang Specificity in Toll-like receptor signaling through distinct effector functions of TRAF3 and TRAF6 Nature 439 2006 204 207
72. G. Oganesyan, S.K. Saha, B. Guo, J.Q. He, A. Shahangian, and B. Zarnegar Critical role of TRAF3 in the Toll-like recepror-dependent and -independent antiviral response Nature 439 2006 208 211
73. M. Sasai, H. Oshiumi, and M. Matsumoto Cutting Edge: NF-kappaB-activating kinase-associated protein 1 participates in TLR3/Toll-IL-1 homology domain-containing adapter molecule-1-mediated IFN regulatory factor 3 activation J Immunol 174 2005 27 30
74. J. Gohda, T. Matsumura, and J. Inoue Cutting Edge: TNFR-associated factor (TRAF) 6 is essential for MyD88-dependent pathway but not Toll/IL-1 receptor domain-containing adaptor-inducing IFN-β (TRIF)-dependent pathway in TLR signaling J Immunol 173 2004 2913 2917
75. N. Kayagaki, Q. Phung, S. Chan, R. Chaudhari, C. Quan, and K.M. O'Rourke DUBA: a deubiquitinase that regulates type I interferon production Science 318 2007 1628 1632
76. D.L. Boone, E.E. Turer, E.G. Lee, R.C. Ahmad, M.T. Wheeler, and C. Tsui The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses Nat Immunol 5 2004 1052 1060
77. M. Feoktistova, P. Geserick, B. Kellert, D.P. Dimitrova, C. Langlais, and M. Hupe cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms Mol Cell 43 2011 449 463
78. L. Galluzzi, O. Kepp, and G. Kroemer RIP Kinases initiate programmed necrosis J Mol Cell Biol 1 2009 8 10
79. Y.S. Cho, S. Challa, D. Moquin, R. Genga, T.D. Ray, and M. Guildford Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation Cell 137 2009 1112 1123
80. Edward S. Mocarski, Jason W. Upton, and William J. Kaiser Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways Nat Rev Immunol 12 2012 79 88
81. S. He, Y. Liang, F. Shao, and X. Wang Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway Proc Natl Acad Sci USA 108 2011 20054 20059
82. B. Salaun, L. Zitvogel, C. Asselin-Paturel, Y. Morel, K. Chemin, and C. Dubois TLR3 as a biomarker for the therapeutic efficacy of double-stranded RNA in breast cancer Cancer Res 71 2011 1607 1614
83. Y. Estornes, F. Toscano, F. Virard, G. Jacquemin, A. Pierrot, and B. Vanbervliet dsRNA induces apoptosis through an atypical death complex associating TLR3 to caspase-8 Cell Death Differ 19 2012 1482 1494
84. T. Seya, H. Shime, H. Takaki, M. Azuma, H. Oshiumi, and M. Matsumoto TLR3/TICAM-1 signaling in tumor cell RIP3-dependent necroptosis Oncoimmunology 1 2012 917 923
85. C.E. Samuel Antiviral actions of interferon, Interferon-regulated cellular proteins and their surprisingly selective antiviral activities Virology 183 1991 1 11
86. H. Lauterbach, B. Bathke, and S. Gilles Mouse CD8a + DCs and human BDCA3 + DCs are major producers of IFN-λ in response to poly(I:C) J Exp Med 207 2010 2703 2717
87. H. Kato, O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, and K. Matsui Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature 441 2006 101 105
88. T. Akazawa, T. Ebihara, M. Okuno, Y. Okuda, M. Shingai, and K. Tsujimura Antitumor NK activation induced by the TLR3-TICAM-1 (TRIF) pathway in myeloid dendritic cells Proc Natl Acad Sci USA 104 2007 252 257
89. T. Seya, J. Kasamatsu, M. Azuma, H. Shime, and M. Matsumoto Natural killer cell activation secondary to innate pattern sensing J Innate Immun 3 2011 264 273
90. T. Ebihara, M. Azuma, H. Oshiumi, J. Kasamatsu, K. Iwabuchi, and K. Matsumoto Identification of a polyI:C-inducible membrane protein that participates in dendritic cell-mediated natural killer cell activation J Exp Med 207 2010 2675 2687
91. W.R. Heath, G.T. Belz, G.M. Behrens, C.M. Smith, S.P. Forehan, and I.A. Parish Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens Immunol Rev 199 2004 9 26
92. L. Shen, and K.L. Lock Priming of T cells by exogenous antigen cross-presented on MHC class I molecules Curr Opin Immunol 18 2006 85 91
93. O. Schulz, S.S. Diebold, M. Chen, T.I. Näslund, M.A. Nolte, and L. Alexopoulou Toll-like receptor 3 promotes cross-priming to virus-infected cells Nature 433 2005 887 892
94. A. Le Bon, N. Etchart, C. Rossmann, M. Ashton, S. Hou, and D. Gewert Cross-priming of CD8 + T cells stimulated by virus-induced type I interferon Nat Immunol 4 2003 1009 1015
95. F. Weber, V. Wagner, S.B. Rasmussen, R. Hartmann, and S.R. Paludan Double-stranded RNA is produced by positive-stranded RNA viruses and DNA viruses but not in detectable amounts by negative-stranded RNA viruses J Virol 80 2006 5059 5064
96. H. Oshiumi, M. Okamoto, K. Fujii, T. Kawanishi, M. Matsumoto, and S. Koike The TLR3-TICAM-1 pathway is mandatory for innate immune responses to poliovirus infection J Immunol 187 2011 5320 5327
97. Y. Abe, K. Fujii, N. Nagata, O. Takeuchi, S. Akira, and H. Oshiumi The Toll-like receptor 3-mediayed antiviral response is important for protection against poliovirus infection in poliovirus receptor transgenic mice J Virol 86 2012 185 194
98. H. Negishi, T. Osawa, K. Ogami, X. Ouyang, S. Sakaguchi, and R. Koshiba A critical link between Toll-like receptor 3 and type II interferon signaling pathways in antiviral innate immunity Proc Natl Acad Sci USA 105 2008 20446 20451
99. S.-Y. Zhang, E. Jouanguy, S. Ugolini, A. Smahi, G. Elain, and P. Romero TLR3 deficiency in patients with Herpes Simplex encephalitis Science 317 2007 1522 1527
100. Y. Guo, M. Audry, M. Ciancanelli, L. Alsina, J. Azevedo, and M. Herman Herpes simplex virus encephalitis in a patient with complete TLR3 deficiency: TLR3 is otherwise redundant in protective immunity J Exp Med 208 2011 2083 2098
101. V. Sancho-Shimizu, R. Pérez de Diego, L. Lorenzo, R. Halwani, A. Alangari, and E. Israelsson Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency J Clin Invest 121 2011 4889 4902
102. T. Wang, T. Town, L. Alexopoulou, J.F. Anderson, E. Fikrig, and R.A. Flavell Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis Nat Med 10 2004 1366 1373
103. R. Le Goffic, V. Balloy, M. Lagranderie, L. Alexopoulou, N. Escriou, and R. Flavell Detrimental contribution of the Toll-like receptor (TLR) 3 to influenza A virus-induced acute pneumonia PLoS Pathog 2 2006 526 535
104. B.B. Gowen, J.D. Hoopes, M.H. Wong, K.H. Jung, K.C. Isakson, and L. Alexopoulou TLR3 deletion limits mortality and disease severity due to phlebovirus infection J Immunol 177 2006 6301 6307
105. B.D. Rudd, J.J. Smit, R.A. Flavell, L. Alexopoulou, M.A. Schller, and A. Gruber Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection J Immunol 176 2006 1937 1942
106. K. Tabeta, P. Georgel, E. Janssen, X. Du, K. Hoebe, and K. Crozat Toll-like receptor 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection Proc Natl Acad Sci USA 101 2004 3516 3521
107. J. Pott, S. Stockinger, N. Torow, A. Smoczek, C. Lindner, and G. McInerney Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility PLoS Pathog 8 2012 e1002670
108. T. Ebihara, M. Shingai, M. Matsumoto, T. Wakita, and T. Seya Hepatitis C virus (HCV)-infected apoptotic cells extrinsically modulate dendritic cell function to activate T cells and NK cells Hepatology 48 2008 48 58
109. M. Azuma, T. Ebihara, H. Oshiumi, M. Matsumoto, and T. Seya Cross-priming for anti-tumor CTL induced by soluble Ag + polyI:C depends on the TICAM-1 pathway in mouse CD11c +/CD8α + dendritic cells Oncoimmunology 1 2012 581 592
110. H. Shime, M. Matsumoto, H. Oshiumi, S. Tanaka, A. Nakane, and Y. Iwakura Toll-like receptor 3 signaling converts tumor-supporting myeloid cells to tumoricidal effectors Proc Natl Acad Sci USA 109 2012 2066 2071
111. T. Seya, H. Shime, and M. Matsumoto TAMable tumor-associated macrophages in response to innate RNA sensing Oncoimmunology 1 2012 1000 1001
112. M. Absher, and W.R. Stinebring Toxic properties of a synthetic double-stranded RNA. Endotoxin-like properties of poly I. poly C, an interferon stimulator Nature 223 1969 715 717
113. K.J. Champney, D.P. Levine, H.B. Levy, and A.M. Lerner Modified polyriboinosinic-polyribocytidylic acid complex: sustained interferonemia and its physiological associates in humans Infect Immun 25 1979 831 837