Multi-level regulation of cellular recognition of viral dsRNA

Cellular and Molecular Life Sciences

Volumn 70, Issue 11, 2013, Pages 1949-1963

  Peisley, Alys ^a,b   Hur, Sun ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

ADAR; Antiviral innate immunity; Double stranded RNA; MDA5; OAS; PKR; RIG I; TLR3

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; ADAPTOR PROTEIN; ADENOSINE DEAMINASE ACTING ON RNA; DDX1 PROTEIN; DHX9 PROTEIN; DOUBLE STRANDED RNA; HELICASE; MELANOMA DIFFERENTIATION ASSOCIATED GENE 5 PROTEIN; MICRORNA; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; PATTERN RECOGNITION RECEPTOR; PROTEIN KINASE RNA ACTIVATED; PROTEIN SERINE THREONINE KINASE; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VIRUS RNA;

ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; CONFORMATIONAL TRANSITION; CORONAVIRUS; DOUBLE STRANDED RNA BINDING DOMAIN; HOST RESISTANCE; HUMAN; INNATE IMMUNITY; NONHUMAN; OLIGOMERIZATION; PROTEIN DOMAIN; REVIEW; RNA BINDING; RNA EDITING; RNA SEQUENCE; RNA STRUCTURE; VIRUS INFECTION; VIRUS REPLICATION;

BASE SEQUENCE; IMMUNITY, INNATE; MODELS, IMMUNOLOGICAL; NUCLEIC ACID CONFORMATION; RECEPTORS, PATTERN RECOGNITION; RNA, DOUBLE-STRANDED; RNA, VIRAL; RNA-BINDING PROTEINS;

EID: 84878288930     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1149-4     Document Type: Review

References (158)

1. AJ Sadler BRG Williams 2008 Interferon-inducible antiviral effectors Nat Rev Immunol 8 559 568 18575461 1:CAS:528:DC%2BD1cXns1ehs78%3D
2. Pichlmair A, Reis e Sousa C (2007) Innate recognition of viruses. Immunity 27: 370-383
3. EC Borden BR Williams 2011 Interferon-stimulated genes and their protein products: what and how? J Interferon Cytokine Res 31 1 4 21226605 1:CAS:528:DC%2BC3MXlt1OmsQ%3D%3D
4. A Iwasaki R Medzhitov 2010 Regulation of adaptive immunity by the innate immune system Science 327 291 295 20075244 1:CAS:528:DC%2BC3cXktlWkuw%3D%3D
5. CE Samuel 2001 Antiviral actions of interferons Clin Microbiol Rev 14 778 809 11585785 1:CAS:528:DC%2BD3MXot1Wms7o%3D
6. Saenger W (1984) Principles of nucleic acid structure. Springer, New York, p 113
7. M Doyle MF Jantsch 2003 New and old roles of the double-stranded RNA-binding domain J Struct Biol 140 147 153
8. Saunders LR, Barber GN (2003) The dsRNA binding protein family: critical roles, diverse cellular functions. FASEB 961-983
9. CO Pabo RT Sauer 1984 Protein-DNA recognition Ann Rev Biochem 53 293 321 6236744 1:CAS:528:DyaL2cXkvVCltLw%3D
10. T Watanabe, et al. 2008 Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes Nature 453 539 543 18404146 1:CAS:528:DC%2BD1cXmt1OrtLk%3D
11. HR Chiang, et al. 2010 Mammalian microRNAs: experimental evaluation of novel and previously annotated genes Genes Dev 24 992 1009 20413612 1:CAS:528:DC%2BC3cXmsVKltbY%3D
12. A Athanasiadis A Rich S Maas 2004 Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome PLoS Biol 2 12 e391 15534692
13. Y Wang FCC Leung 2009 A study on genomic distribution and sequence features of human long inverted repeats reveals species-specific intronic inverted repeats FEBS J 276 1986 1998 19243432 1:CAS:528:DC%2BD1MXktVWks7g%3D
14. R Yelin, et al. 2003 Widespread occurrence of antisense transcription in the human genome Nat Biotechol 21 379 386 1:CAS:528:DC%2BD3sXisVGisLo%3D
15. O Rosok M Sioud 2004 Systematic identification of sense-antisense transcripts in mammalian cells Nat Biotechnol 22 104 108 14704709 1:CAS:528:DC%2BD2cXls1em
16. SA McKenna, et al. 2007 Viral dsRNA inhibitors prevent self-association and autophosphorylation of PKR J Mol Biol 372 103 113 17619024 1:CAS:528:DC%2BD2sXovFeru78%3D
17. P Vitali ADJ Scadden 2010 Double-stranded RNAs containing multiple IU pairs are sufficient to suppress interferon induction and apoptosis Nat Struct Mol Biol 17 9 1043 1050 20694008 1:CAS:528:DC%2BC3cXpvVWgsrY%3D
18. V Hornung, et al. 2006 5′-Triphosphate RNA is the ligand for RIG-I Science 314 994 997 17038590
19. SR Nallagatla PC Bevilacqua 2008 Nucleoside modifications modulate activation of the protein kinase PKR in an RNA structure-specific manner RNA 14 1201 1203 18426922 1:CAS:528:DC%2BD1cXntVCjsL8%3D
20. SR Nallagatla, et al. 2007 5′-Triphosphate-dependent activation of PKR by RNAs with short stem-loops Science 318 1455 1458 18048689 1:CAS:528:DC%2BD2sXhtlGmtLbM
21. Zust R et al (2011) Ribose 2′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat Immunol 12:137-143
22. K Malathi, et al. 2010 RNase L releases a small RNA from HCV RNA that refolds into a potent PAMP RNA 16 2108 2119 20833746 1:CAS:528: DC%2BC3cXhsVGhsL%2FN
23. BR Anderson, et al. 2011 Nucleoside modifications in RNA limit activation of 2′-5′-oligoadenylate synthetase and increase resistance to cleavage by RNase L Nucleic Acids Res 39 9329 9338 21813458 1:CAS:528: DC%2BC3MXhsFCisbzL
24. MA Garcia, et al. 2006 Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action Microbiol Mol Biol Rev 70 1032 1060 17158706 1:CAS:528:DC%2BD2sXmslOisQ%3D%3D
25. PA Lemaire JL Cole 2008 Mechanism of PKR activation by dsRNA J Mol Biol 381 351 360 18599071 1:CAS:528:DC%2BD1cXoslWqtr0%3D
26. CK Pfeller, et al. 2011 Protein kinase PKR and RNA adenosine deaminase ADAR1: new roles for old players as modulators of the interferon response Curr Opin Immunol 23 573 582
27. SA McKenna, et al. 2007 Biophysical and biochemical investigations of dsRNA-activated kinase PKR Methods Enzym 430 373 396 1:CAS:528: DC%2BD1cXhsVeqtbY%3D
28. JL Cole 2010 Analysis of PKR activation using analytical ultracentrifugation Macromol Biosci 10 703 713 20533534 1:CAS:528: DC%2BC3cXovFCgsr4%3D
29. PA Lemaire J Lary JL Cole 2005 Mechanism of PKR activation: dimerization and kinase activation in the absence of double-stranded RNA J Mol Biol 345 81 90 15567412 1:CAS:528:DC%2BD2cXhtVags73F
30. I Kim CW Liu JD Puglisi 2006 Specific recognition of HIV TAR RNA by the dsRNA binding domains (dsRBD1-dsRBD2) of PKR J Mol Biol 358 430 442 16516925 1:CAS:528:DC%2BD28XjvVamtL8%3D
31. PC Bevilacqua TR Cech 1996 Minor-groove recognition of double-stranded RNA by the double-stranded RNA-binding domain from the RNA-activated protein kinase PKR Biochemistry 35 9983 9994 8756460 1:CAS:528:DyaK28Xkt1ylu7o%3D
32. L Manche, et al. 1992 Interactions between double-stranded RNA regulators and the protein kinase DAI Mol Cell Biol 12 5238 5248 1357546 1:CAS:528:DyaK38XmsVOls7w%3D
33. JM Ryter SC Schultz 1998 Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA EMBO J 17 7505 7513 9857205 1:CAS:528:DyaK1MXksVGgug%3D%3D
34. J Gan, et al. 2006 Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III Cell 124 355 366 16439209 1:CAS:528:DC%2BD28Xht1Kktbw%3D
35. S Cohen-Chalamish, et al. 2009 Dynamic refolding of IFN-gamma mRNA enables it to function as PKR activator and translation template Nat Chem Biol 5 896 903 19801993 1:CAS:528:DC%2BD1MXht1WgsbzE
36. X Zheng PC Bevilacqua 2004 Activation of the protein kinase PKR by short double-stranded RNAs with single-stranded tails RNA 10 1934 1945 15547138 1:CAS:528:DC%2BD2cXhtVGisLvK
37. HA Hundley BL Bass 2010 ADAR editing in double-stranded UTRs and other noncoding RNA sequences Trends Biochem Sci 35 377 383 20382028 1:CAS:528:DC%2BC3cXosV2ltr4%3D
38. LP Keegan, et al. 2004 Adenosine deaminases acting on RNA (ADARs): RNA-editing enzymes Genome Biol 5 209 14759252
39. CX Chen, et al. 2000 A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains RNA 6 755 767 10836796 1:CAS:528:DC%2BD3cXjtlKmsLw%3D
40. SK Wong S Sato DW Lazinski 2001 Substrate recognition by ADAR1 and ADAR2 RNA 7 846 858 11421361 1:CAS:528:DC%2BD3MXksFertLs%3D
41. KA Lehmann BL Bass 2000 Double-stranded RNA adenosine deaminases ADAR1 and ADAR2 have overlapping specificities Biochemistry 39 12875 12884 11041852 1:CAS:528:DC%2BD3cXmsl2jsL4%3D
42. H Wahlstedt M Ohman 2011 Site-selective versus promiscuous A-to-I editing Wiley Interdiscip Rev RNA 2 761 771 21976281 1:CAS:528:DC%2BC3MXhtlyrsrvP
43. AG Polson BL Bass 1994 Preferential selection of adenosines for modification by double-stranded RNA adenosine deaminase EMBO J 13 5701 5711 7527340 1:CAS:528:DyaK2MXislGqsLo%3D
44. KA Lehmann BL Bass 1999 The importance of internal loops within RNA substrates of ADAR1 J Mol Biol 291 1 13 10438602 1:CAS:528:DyaK1MXkvFKjtLc%3D
45. TR Dawson CL Sansam RB Emeson 2004 Structure and sequence determinants required for the RNA editing of ADAR2 substrates J Biol Chem 279 4941 4951 14660658 1:CAS:528:DC%2BD2cXpslSjtQ%3D%3D
46. M Higuchi, et al. 1993 RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency Cell 75 1361 1370 8269514 1:CAS:528:DyaK2cXntVOqsA%3D%3D
47. CM Burns, et al. 1997 Regulation of serotonin-2C receptor G-protein coupling by RNA editing Nature 387 303 308 9153397 1:CAS:528:DyaK2sXjtlSgurw%3D
48. BL Bass H Weintraub 1988 An unwinding activity that covalently modifies its double-stranded RNA substrate Cell 55 1089 1098 3203381 1:CAS:528: DyaL1MXptFWgtw%3D%3D
49. K Nishikura 2010 Functions and regulation of RNA editing by ADAR deaminases Ann Rev Biochem 79 321 349 20192758 1:CAS:528:DC%2BC3cXpslShtr0%3D
50. CE Samuel 2011 Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral Virology 411 180 193 21211811 1:CAS:528: DC%2BC3MXjs1Gqurg%3D
51. SV Ward, et al. 2011 RNA editing enzyme adenosine deaminase is a restriction factor for controlling measles virus replication that also is required for embryogenesis Proc Natl Acad Sci USA 108 331 336 21173229 1:CAS:528:DC%2BC3MXmt1ejtA%3D%3D
52. R Cattaneo, et al. 1988 Biased hypermutation and other genetic changes in defective measles viruses in human brain infections Cell 55 255 265 3167982 1:CAS:528:DyaL1MXhvVeq
53. Y Nie GL Hammond JH Yang 2007 Double-stranded RNA deaminase ADAR1 increases host susceptibility to virus infection J Virol 81 917 923 17079286 1:CAS:528:DC%2BD2sXms1Slsg%3D%3D
54. Z Li KC Wolff CE Samuel 2010 RNA adenosine deaminase ADAR1 deficiency leads to increased activation of protein kinase PKR and reduced vesicular stomatitis virus growth following interferon treatment Virology 396 316 322 19913273 1:CAS:528:DC%2BD1MXhsFantbzF
55. JL Casey 2006 RNA editing in hepatitis delta virus Curr Top Microbiol Immunol 307 67 89 16903221 1:CAS:528:DC%2BD28XosFeqsrw%3D
56. SK Wong DW Lazinski 2002 Replicating hepatitis delta virus RNA is edited in the nucleus by the small form of ADAR1 Proc Natl Acad Sci USA 99 15118 15123 12399548 1:CAS:528:DC%2BD38Xpt1yru7c%3D
57. S Sato C Cornillez-Ty DW Lazinski 2004 By inhibiting replication, the large hepatitis delta antigen can indirectly regulate amber/W editing and its own expression J Virol 78 8120 8134 15254184 1:CAS:528:DC%2BD2cXmtFCjs7s%3D
58. Z Peng, et al. 2012 Comprehensive analysis of RNA-seq data reveals extensive RNA editing in a human transcriptome Nat Biotechol 30 253 260 1:CAS:528:DC%2BC38XitFaks7o%3D
59. N Paz-Yaacov, et al. 2010 Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates Proc Natl Acad Sci USA 107 12174 12179 20566853 1:CAS:528:DC%2BC3cXovFyit78%3D
60. Alon S et al (2012) Systematic identification of edited microRNAs in the human brain. Genome Res [Epub ahead]
61. S Carmi I Borukhov EY Levanon 2011 Identification of widespread ultra-edited human RNAs PLoS Genet 7 e1002317 22028664 1:CAS:528: DC%2BC3MXhsVCku7jI
62. BS Heale LP Keegan MA O'Connell 2010 The effect of RNA editing and ADARs on miRNA biogenesis and function Adv Exp Med Biol 700 76 84 1:CAS:528: DC%2BC3MXmtlOjsA%3D%3D
63. JEC Jepson RA Reenan 2008 RNA editing in regulating gene expression in the brain Biochim Biophys Acta 1779 459 470 18086576 1:CAS:528: DC%2BD1cXhtVent7nM
64. LL Chen GG Carmichael 2012 Nuclear editing of mRNA 3′-UTR Curr Top Microbiol Immunol 353 111 121 21725897 1:CAS:528:DC%2BC38XhsFCqsL7P
65. Q Wang GG Carmichael 2004 Effects of length and location on the cellular response to double-stranded RNA Microbiol Mol Biol Rev 68 3 432 452 15353564 1:CAS:528:DC%2BD2cXosVyhtLg%3D
66. JC Hartner, et al. 2008 ADAR1 is essential for the maintenance of hematopoiesis and suppression of interferon signaling Nat Immunol 10 109 115 19060901
67. Q Wang, et al. 2000 Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis Science 290 1765 1768 11099415 1:CAS:528: DC%2BD3cXovVOhur8%3D
68. JC Hartner, et al. 2004 J Biol Chem 279 4894 4902 14615479 1:CAS:528:DC%2BD2cXpslSjsA%3D%3D
69. Q Wang, et al. 2004 Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase J Biol Chem 279 4952 4961 14613934 1:CAS:528:DC%2BD2cXpslSjug%3D%3D
70. M Higuchi, et al. 2000 Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2 Nature 406 78 81 10894545 1:STN:280:DC%2BD3czltFSnsQ%3D%3D
71. MJ Palladino, et al. 2000 A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity Cell 102 437 10966106 1:CAS:528:DC%2BD3cXmtFOrsL0%3D
72. LA Tonkin, et al. 2002 RNA editing by ADARs is important for normal behavior in Caenorhabditis elegans EMBO J 21 6025 6035 12426375 1:CAS:528:DC%2BD38XptFOrtrk%3D
73. R Stefl, et al. 2010 The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove Cell 143 225 237 20946981 1:CAS:528:DC%2BC3cXht12qurnP
74. A Ramos, et al. 2000 RNA recognition by a Staufen double-stranded RNA-binding domain EMBO J 19 997 1009 10698941 1:CAS:528:DC%2BD3cXitVyrsrc%3D
75. H Wu, et al. 2004 Structural basis for recognition of the AGNN tetraloop RNA fold by the double-stranded RNA binding domain of Rnt1p RNase III Proc Natl Acad Sci USA 101 8307 8312 15150409 1:CAS:528:DC%2BD2cXkvFOms7c%3D
76. S Torralba J Sojat R Hartmann 2008 2′-5′ oligoadenylate synthetase shares active site architecture with the archaeal CCA-adding enzyme Cell Mol Life Sci 65 2613 2620 18604630 1:CAS:528:DC%2BD1cXhtVansr3M
77. AG Hovanessian, et al. 1987 Identification of 69-kd and 100-kd forms of 2-5A synthetase in interferon-treated human cells by specific monoclonal antibodies EMBO J 6 1273 1280 2440675 1:CAS:528:DyaL2sXkt1Wktro%3D
78. D Rebouillat I Marie AG Hovanessian 1998 Molecular cloning and characterization of two related and interferon-induced 56-kDa and 30-kDa proteins highly similar to 2-5 oligoadenylate synthetase Eur J Biochem 257 319 330 9826176 1:CAS:528:DyaK1cXntFWmu7w%3D
79. Kristiansen H et al (2011) The oligoadenylate synthetase family: an ancient protein family with multiple antiviral activities. J Interferon Cytokine Res 31:41-47
80. DH Wreschner, et al. 1981 Interferon action-sequence specificity of the ppp(A2′p)nA-dependent ribonuclease Nature 278 414 417
81. G Floyd-Smith E Slattery P Lengyel 1981 Interferon action: RNA cleavage pattern of a (2′-5′)oligoadenylate-dependent endonuclease Science 212 1030 1032 6165080 1:CAS:528:DyaL3MXktlOqur4%3D
82. A Chakrabarti BK Jha RH Silverman 2011 New insights into the role of RNase-L in innate immunity J Interferon Cytokine Res 31 49 57 21190483 1:CAS:528:DC%2BC3MXlt1Omuw%3D%3D
83. K Kubota, et al. 2004 Identification of 2′-phosphodiesterase, which plays a role in the 2-5A system regulated by interferon J Biol Chem 279 37832 37841 15231837 1:CAS:528:DC%2BD2cXntFSnsbs%3D
84. M Knight, et al. 1980 Radioimmune, radiobinding and HPLC analysis of 2-5A and related oligonucleotides from intact cells Nature 288 189 192 6159552 1:CAS:528:DyaL3MXhtlGmsrs%3D
85. D Rebouillat AG Hovanessian 1999 The human 2,5-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties J Interferon Cytokine Res 19 295 308 10334380 1:CAS:528:DyaK1MXjtVKrtrk%3D
86. JW Schoggins, et al. 2011 A diverse range of gene products are effectors of the type I interferon antiviral response Nature 472 481 485 21478870 1:CAS:528:DC%2BC3MXksFWgur0%3D
87. R Hartmann, et al. 2003 Crystal structure of the 2′-specific and double-stranded RNA-activated interferon-induced antiviral protein 2′-5′-oligoadenylate synthetase Mol Cell 12 1173 1185 14636576 1:CAS:528:DC%2BD3sXpvVGhtb0%3D
88. SN Sarkar, et al. 1999 The nature of the catalytic domain of 2′-5′-oligoadenylate synthetases J Biol Chem 274 25535 25542 10464285 1:CAS:528:DyaK1MXmtVWiu7c%3D
89. R Hartmann, et al. 1998 Activation of 2′-5′ oligoadenylate synthetase by single-stranded and double-stranded RNA aptamers J Biol Chem 273 3236 3246 9452437 1:CAS:528:DyaK1cXhtVymt7o%3D
90. SY Desai GC Sen 1997 Effects of varying lengths of double-stranded RNA on binding and activation of 2′-5′-oligoadenylate synthetase J Interferon Cytokine Res 17 531 536 9335430 1:CAS:528:DyaK2sXmvFaru7Y%3D
91. A Ghosh, et al. 1997 Enzymatic activity of 2′-5′- oligoadenylate synthetase is impaired by specific mutations that affect oligomerization of the protein J Biol Chem 272 33220 33226 9407111 1:CAS:528:DyaK1cXps1Gn
92. R Kodym E Kodym MD Story 2009 2′-5′-Oligoadenylate synthetase is activated by a specific RNA sequence motif Biochem Biophy Res Comm 388 317 322 1:CAS:528:DC%2BD1MXhtVOisrvE
93. Grosjean H, Benne R (1998) Modification and editing of RNA. American Society for Microbiology, Washington
94. TW Nilsen, et al. 1982 Heterogeneous nuclear RNA promotes synthesis of (2′5′)oligoadenylate and is cleaved by the (2′5′) oligoadenylate-activated endoribonuclease Mol Cell Biol 2 154 160 6180300 1:CAS:528:DyaL38Xhtlyitb8%3D
95. RJ Molinaro, et al. 2006 Selection and cloning of poly(rC)-binding protein 2 and Raf kinase inhibitor protein RNA activators of 2′5′-oligoadenylate synthetase from prostate cancer cells Nucleic Acids Res 34 6684 6695 17145707 1:CAS:528:DC%2BD28XhtlCqsrvN
96. Y Kumagai O Takeuchi S Akira 2008 Pathogen recognition by innate receptors J Infect Chemother 14 86 92 18622669 1:CAS:528:DC%2BD1cXlt1antr8%3D
97. AL Blasius B Beutler 2010 Intracellular Toll-like receptors Immunity 32 305 315 20346772 1:CAS:528:DC%2BC3cXlsVSntr4%3D
98. ND Temperley, et al. 2008 Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss BMC Genomics 9 62 18241342
99. SS Diebold, et al. 2004 Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA Science 303 1529 1531 14976261 1:CAS:528:DC%2BD2cXhslCgsb4%3D
100. F Heil, et al. 2004 Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8 Science 303 1526 1529 14976262 1:CAS:528:DC%2BD2cXhslCgsLc%3D
101. JM Lund, et al. 2004 Recognition of single-stranded RNA viruses by Toll-like receptor 7 Proc Natl Acad Sci USA 101 5598 5603 15034168 1:CAS:528:DC%2BD2cXjsVagu7c%3D
102. H Hemmi, et al. 2000 A Toll-like receptor recognizes bacterial DNA Nature 408 740 745 11130078 1:CAS:528:DC%2BD3cXptVCqsL0%3D
103. L Alexopoulou, et al. 2001 Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3 Nature 413 732 738 11607032 1:CAS:528:DC%2BD3MXnvFegsL0%3D
104. Y Wang, et al. 2010 Dimerization of Toll-like receptor 3 (TLR3) is required for ligand binding J Biol Chem 285 36836 36841 20861016 1:CAS:528:DC%2BC3cXhsVWgsrvE
105. JN Leonard, et al. 2008 The TLR3 signaling complex forms by cooperative receptor dimerization Proc Natl Acad Sci USA 105 1 258 263 18172197 1:CAS:528:DC%2BD1cXpvFSitQ%3D%3D
106. H Oshiumi, et al. 2003 TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-bold beta induction Nat Immunol 4 161 167 12539043 1:CAS:528:DC%2BD3sXmslKisA%3D%3D
107. JK Bell, et al. 2005 The molecular structure of the Toll-like receptor 3 ligand-binding domain Proc Natl Acad Sci USA 102 10976 10980 16043704 1:CAS:528:DC%2BD2MXnvVWjur4%3D
108. MS Jim J-O Lee 2008 Structures of the Toll-like receptor family and its ligand complexes Immunity 29 182 191
109. L Liu, et al. 2008 Structural basis of Toll-like receptor 3 signaling with double-stranded RNA Science 320 379 381 18420935 1:CAS:528: DC%2BD1cXks1GhsLk%3D
110. M Sioud 2006 Innate sensing of self and non-self RNAs by Toll-like receptors Trends Mol Med 12 167 176 16530484 1:CAS:528:DC%2BD28XjvFWltrw%3D
111. M Schroder AG Bowie 2005 TLR3 in antiviral immunity: key player or bystander? Trends Immunol 26 462 468 16027039
112. K Kariko, et al. 2004 mRNA is an endogenous ligand for Toll-like receptor 3 J Biol Chem 279 12542 12550 14729660 1:CAS:528:DC%2BD2cXitl2gsbs%3D
113. KA Cavassani, et al. 2008 TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events J Exp Med 205 2609 2621 18838547 1:CAS:528:DC%2BD1cXhtlWntL7L
114. Duffy K.E et al (2012) Lateral clustering of TLR3:dsRNA signaling units revealed by TLR3ecd:3Fabs quaternary structure. J Mol Biol [Epub ahead]
115. ME Kleinman, et al. 2008 Sequence- and target-independent angiogenesis suppression by siRNA via TLR3 Nature 452 591 597 18368052 1:CAS:528: DC%2BD1cXktFCgs7s%3D
116. K Karikó et al. 2004 Small interfering RNAs mediate sequence independent gene suppression and induce immune activation by signaling through Toll-like receptor 3 J Immunol 172 6545 6549 15153468
117. N Pirher, et al. 2008 A second binding site for double-stranded RNA in TLR3 and consequences for interferon activation Nat Struc Mol Biol 15 761 763 1:CAS:528:DC%2BD1cXotVeqtrs%3D
118. K Kariko, et al. 2005 Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA Immunity 23 165 175 16111635 1:CAS:528:DC%2BD2MXpvVCnu74%3D
119. M Yoneyama, et al. 2004 The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nat Immunol 5 7 730 737 15208624 1:CAS:528:DC%2BD2cXlt1Wmu78%3D
120. M Yoneyama, et al. 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 16116171 1:CAS:528:DC%2BD2MXos1Gisb0%3D
121. RB Seth, et al. 2005 Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF3 Cell 122 699 782
122. LG Xu, et al. 2005 VISA is an adapter protein required for virus-triggered IFN-b signaling Mol Cell 19 727 740 16153868 1:CAS:528:DC%2BD2MXhtVyhtb%2FJ
123. T Kawai, et al. 2005 IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction Nat Immunol 6 10 981 988 16127453 1:CAS:528:DC%2BD2MXhtVajs7fJ
124. Satoh T et al (2010) LGP2 is a positive regulator of RIG-I and MDA5-mediated antiviral responses. Proc Natl Acad Sci USA 107:1512-1517
125. T Saito R Hirai YM Loo D Owen CL Johnson SC Sinha S Akira T Fujita M Gale Jr 2007 Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2 Proc Natl Acad Sci USA 104 2 582 587 17190814 1:CAS:528:DC%2BD2sXovFWktA%3D%3D
126. MU Gack, et al. 2007 TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity Nature 446 916 920 17392790 1:CAS:528:DC%2BD2sXktlSktbw%3D
127. X Jiang, et al. 2012 Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response Immunity 36 959 973 22705106 1:CAS:528:DC%2BC38Xos1enu7c%3D
128. F Hou, et al. 2011 MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response Cell 146 1 14
129. A Pichlmair, et al. 2006 RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates Science 314 997 1001 17038589 1:CAS:528:DC%2BD28XhtFyqtLbM
130. M Schlee, et al. 2009 Recognition of 5′triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus Immunity 31 1 25 34 19576794 1:CAS:528: DC%2BD1MXpsFOgurw%3D
131. JT Marques, et al. 2006 A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells Nat Biotechnol 24 559 565 16648842 1:CAS:528:DC%2BD28Xkt1Kitro%3D
132. T Saito, et al. 2008 Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA Nature 454 523 527 18548002 1:CAS:528:DC%2BD1cXovV2mtLk%3D
133. D Uzri L Gehrke 2009 Nucleotide sequences and modifications that determine RIG-I/RNA binding and signaling activities J Virol 83 4174 4184 19224987 1:CAS:528:DC%2BD1MXlt1Kqtbo%3D
134. K Malathi, et al. 2007 Small self-RNA generated by RNase L amplifies antiviral innate immunity Nature 448 816 819 17653195 1:CAS:528: DC%2BD2sXptVGrs7c%3D
135. K Takahasi, et al. 2008 Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses Mol Cell 29 4 428 440 18242112 1:CAS:528:DC%2BD1cXjtFCgsbY%3D
136. S Cui, et al. 2008 The C-terminal regulatory domain is the RNA 5′-triphosphate sensor of RIG-I Mol Cell 29 2 169 179 18243112 1:CAS:528:DC%2BD1cXhvVOks74%3D
137. C Lu, et al. 2010 The structural basis of 5′ triphosphate double-stranded RNA recognition by RIG-I C-terminal domain Structure 18 1032 1043 20637642 1:CAS:528:DC%2BC3cXpvFOhtLg%3D
138. Y Wang, et al. 2010 Structural and functional insights into 5′-ppp RNA pattern recognition by the innate immune receptor RIG-I Nat Struct Mol Biol 17 7 781 787 20581823 1:CAS:528:DC%2BC3cXnvFyktrc%3D
139. F Jiang, et al. 2011 Structural basis of RNA recognition and activation by innate immune receptor RIG-I Nature 479 7373 423 427 21947008 1:CAS:528:DC%2BC3MXht1WltLfL
140. D Luo, et al. 2011 Structural insights into RNA recognition by RIG-I Cell 147 409 422 22000018 1:CAS:528:DC%2BC3MXhtlaksbrJ
141. E Kowalinski, et al. 2011 Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA Cell 147 423 435 22000019 1:CAS:528:DC%2BC3MXhtlaksbrL
142. M Binder, et al. 2011 Molecular mechanism of signal perception and integration by the innate immune sensor retinoic acid inducible gene-I J Biol Chem 286 27278 27287 21659521 1:CAS:528:DC%2BC3MXpsVOntbg%3D
143. D Bamming CM Horvath 2009 Regulation of signal transduction by enzymatically inactive antiviral RNA helicase proteins MDA5, RIG-I, and LGP2 J Biol Chem 284 15 9700 9712 19211564 1:CAS:528:DC%2BD1MXjvFKktLs%3D
144. S Myong, et al. 2009 Cytosolic viral sensor RIG-I Is a 5′-triphosphate-dependent translocase on double-stranded RNA Science 323 1070 1074 19119185 1:CAS:528:DC%2BD1MXitVyntrs%3D
145. H Kato, et al. 2008 Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5 J Exp Med 205 7 1601 1610 18591409 1:CAS:528:DC%2BD1cXosVKkt7k%3D
146. A Peisley, et al. 2011 Cooperative assembly and dynamic disassembly of MDA5 filaments for viral dsRNA recognition Proc Natl Acad Sci USA 108 52 21010 21015 22160685 1:CAS:528:DC%2BC38XnvVGjsg%3D%3D
147. IC Berke Y Modis 2012 MDA5 cooperatively forms dimers and ATP-sensitive filaments upon binding double-stranded RNA EMBO J 7 1714 1726
148. SA McCartney, et al. 2008 MDA-5 recognition of a murine norovirus PLoS Pathog 4 7 e1000108 18636103
149. A Pichlmair, et al. 2009 Activation of MDA5 requires higher-order RNA structures generated during virus infection J Virol 83 20 10761 10769 19656871 1:CAS:528:DC%2BD1MXhtlCltr7J
150. Luthra P et al (2011) Activation of IFN-β expression by a viral mRNA through RNase L and MDA5. Proc Natl Acad Sci USA 108:2118-2123
151. H Kato, et al. 2006 Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature 441 101 105 16625202 1:CAS:528: DC%2BD28XktVGltLk%3D
152. T Kim, et al. 2010 Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells Proc Natl Acad Sci USA 107 15181 15186 20696886 1:CAS:528:DC%2BC3cXhtFSmt7bM
153. Z Zhang, et al. 2011 DHX9 pairs with IPS-1 to sense double-stranded RNA in myeloid dendritic cells J Immunol 187 4501 4508 21957149 1:CAS:528: DC%2BC3MXhtlChsbbE
154. Z Zhang, et al. 2011 DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cell Immunity 34 866 878 21703541 1:CAS:528:DC%2BC3MXnvFOksLs%3D
155. J Jin, et al. 2011 Evidence that Lin28 stimulates translation by recruiting RNA helicase A to polysomes Nucleic Acids Res 39 3724 3734 21247876 1:CAS:528:DC%2BC3MXlvVyisL4%3D
156. M Ishaq, et al. 2009 The DEAD-box RNA helicase DDX1 interacts with RelA and enhances nuclear factor kappaB-mediated transcription J Cell Biochem 106 297 305
157. EJ Hennessy AE Parker LAJ O'Neill 2010 Targeting Toll-like receptors: emerging therapeutics? Nat Rev Drug Discov 9 293 307 20380038 1:CAS:528:DC%2BC3cXksF2itb4%3D
158. RC Ireton M Gale Jr 2011 RIG-I like receptors in antiviral immunity and therapeutic applications Viruses 3 906 919 21994761 1:CAS:528: DC%2BC3MXotF2msr4%3D