DsRNA-activation of TLR3 and RLR signaling: Gene induction-dependent and independent effects

Journal of Interferon and Cytokine Research

Volumn 34, Issue 6, 2014, Pages 427-436

  Chattopadhyay, Saurabh ^a   Sen, Ganes C ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSOME; BETA CATENIN; BETA INTERFERON; BINDING PROTEIN; CASPASE 9; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYTOCHROME C; DOUBLE STRANDED RNA; HISTONE DEACETYLASE 6; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; LGP2 PROTEIN; MDA 5 PROTEIN; PATTERN RECOGNITION RECEPTOR; PROTEIN; PROTEIN BAX; RETINOIC ACID INDUCIBLE PROTEIN I; RNA HELICASE; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; DEAD BOX PROTEIN;

ADAPTIVE IMMUNITY; AMINO TERMINAL SEQUENCE; ANTIVIRAL GENE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CYTOPLASM; DENDRITIC CELL; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENE INDUCTION; HEMATOPOIETIC CELL; HERPES SIMPLEX VIRUS 1; HUMAN; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OLIGOMERIZATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROCESSING; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SENDAI VIRUS INFECTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; VIRUS GENE; VIRUS REPLICATION; WEST NILE FEVER; ANIMAL; METABOLISM;

ANIMALS; DEAD-BOX RNA HELICASES; HUMANS; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 84902123970     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2014.0034     Document Type: Review

References (90)

1. Allikmets R, Bergen AA, Dean M, Guymer RH, Hageman GS, Klaver CC, Stefansson K, Weber BH; International Agerelated Macular Degeneration Genetics C. 2009. Geographic atrophy in age-related macular degeneration and TLR3. N Engl J Med 360(21):2252-2254; author reply 2255-2256
2. Bell JK, Botos I, Hall PR, Askins J, Shiloach J, Segal DM, Davies DR. 2005. The molecular structure of the Toll-like receptor 3 ligand-binding domain. Proc Natl Acad Sci U S A 102(31):10976-10980. (Pubitemid 41105978
3. Castano L, Eisenbarth GS. 1990. Type-I diabetes: A chronic autoimmune disease of human, mouse, and rat. Annu Rev Immunol 8:647-679. (Pubitemid 20135642
4. Chattopadhyay S, Fensterl V, Zhang Y, Veleeparambil M, Wetzel JL, Sen GC. 2013a. Inhibition of viral pathogenesis and promotion of the septic shock response to bacterial infection by IRF-3 are regulated by the acetylation and phosphorylation of its coactivators. MBio 4(2):e00636
5. Chattopadhyay S, Fensterl V, Zhang Y, Veleeparambil M, Yamashita M, Sen GC. 2013b. Role of interferon regulatory factor 3-mediated apoptosis in the establishment and maintenance of persistent infection by Sendai virus. J Virol 87(1):16-24
6. Chattopadhyay S, Marques JT, Yamashita M, Peters KL, Smith K, Desai A, Williams BR, Sen GC. 2010. Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J 29(10):1762-1773
7. Chattopadhyay S, Sen GC. 2010. IRF-3 and Bax: A deadly affair. Cell Cycle 9(13):2479-2480
8. Chattopadhyay S, Yamashita M, Sen GC. 2012. Antiviral actions of double-stranded RNA. In: Sambhara S, Fujita T, eds. Nucleic acid sensors and antiviral immunity. Austin (TX): Landes Bioscience. p 218-239
9. Chattopadhyay S, Yamashita M, Zhang Y, Sen GC. 2011. The IRF-3/Bax-mediated apoptotic pathway, activated by viral cytoplasmic RNA and DNA, inhibits virus replication. J Virol 85(8):3708-3716
10. Childs KS, Randall RE, Goodbourn S. 2013. LGP2 plays a critical role in sensitizing mda-5 to activation by doublestranded RNA. PLoS One 8(5):e64202
11. Chiu YH, Macmillan JB, Chen ZJ. 2009. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138(3):576-591
12. Choe J, Kelker MS, Wilson IA. 2005. Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 309(5734):581-585. (Pubitemid 41033635
13. Cui S, Eisenacher K, Kirchhofer A, Brzozka K, Lammens A, Lammens K, Fujita T, Conzelmann KK, Krug A, Hopfner KP. 2008. The C-Terminal regulatory domain is the RNA 5¢-Triphosphate sensor of RIG-I. Mol Cell 29(2):169-179. (Pubitemid 351172822
14. Der SD, Zhou A, Williams BR, Silverman RH. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci U S A 95(26):15623-15628. (Pubitemid 29018750
15. Dixit E, Boulant S, Zhang Y, Lee AS, Odendall C, Shum B, Hacohen N, Chen ZJ, Whelan SP, Fransen M, Nibert ML, Superti-Furga G, Kagan JC. 2010. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141(4): 668-681
16. Dixit E, Kagan JC. 2013. Intracellular pathogen Detection by RIG-I-like receptors. Adv Immunol 117:99-125
17. Elco CP, Guenther JM, Williams BR, Sen GC. 2005. Analysis of genes induced by Sendai virus infection of mutant cell lines reveals essential roles of interferon regulatory factor 3, NF-kappaB, and interferon but not toll-like receptor 3. J Virol 79(7):3920-3929. (Pubitemid 40388332
18. Errett JS, Suthar MS, McMillan A, Diamond MS, Gale M, Jr. 2013. The essential, nonredundant roles of RIG-I and MDA5 in Detecting and controlling West Nile virus infection. J Virol 87(21):11416-11425
19. Feng Q, Hato SV, Langereis MA, Zoll J, Virgen-Slane R, Peisley A, Hur S, Semler BL, van Rij RP, van Kuppeveld FJ. 2012. MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep 2(5):1187-1196
20. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao SM, Maniatis T. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4(5):491-496. (Pubitemid 36592443
21. Gack MU, Nistal-Villan E, Inn KS, Garcia-Sastre A, Jung JU. 2010. Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J Virol 84(7):3220-3229
22. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-Imediated antiviral activity. Nature 446(7138):916-920. (Pubitemid 46633167
23. Garcia M, Dogusan Z, Moore F, Sato S, Hartmann G, Eizirik DL, Rasschaert J. 2009. Regulation and function of the cytosolic viral RNA sensor RIG-I in pancreatic beta cells. Biochim Biophys Acta 1793(11):1768-1775
24. Geiss G, Jin G, Guo J, Bumgarner R, Katze MG, Sen GC. 2001. A comprehensive view of regulation of gene expression by double-stranded RNA-mediated cell signaling. J Biol Chem 276(32):30178-30182
25. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA, Diamond MS, Colonna M. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci U S A 103(22):8459-8464. (Pubitemid 43838477
26. Gitlin L, Benoit L, Song C, Cella M, Gilfillan S, Holtzman MJ, Colonna M. 2010. Melanoma differentiation-Associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog 6(1): E1000734
27. Goulet ML, Olagnier D, Xu Z, Paz S, Belgnaoui SM, Lafferty EI, Janelle V, Arguello M, Paquet M, Ghneim K, Richards S, Smith A, Wilkinson P, Cameron M, Kalinke U, Qureshi S, Lamarre A, Haddad EK, Sekaly RP, Peri S, Balachandran S, Lin R, Hiscott J. 2013. Systems analysis of a RIG-I agonist inducing broad spectrum inhibition of virus infectivity. PLoS Pathog 9(4):e1003298
28. Hartmann R, Justesen J, Sarkar SN, Sen GC, Yee VC. 2003. Crystal structure of the 2¢-specific and double-stranded RNAactivated interferon-induced antiviral protein 2¢-5¢-oligoadenylate synthetase. Mol Cell 12(5):1173-1185. (Pubitemid 37487926
29. Hiscott J. 2007. Triggering the innate antiviral response through IRF-3 activation. J Biol Chem 282(21):15325-15329. (Pubitemid 47093257
30. Horner SM, Liu HM, Park HS, Briley J, Gale M, Jr. 2011. Mitochondrial-Associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus. Proc Natl Acad Sci U S A 108(35):14590-14595
31. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G. 2006. 5¢-Triphosphate RNA is the ligand for RIG-I. Science 314(5801):994-997
32. Hou F, Sun L, Zheng H, Skaug B, Jiang QX, Chen ZJ. 2011. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146(3): 448-461
33. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, Hiiragi A, Dermody TS, Fujita T, Akira S. 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. (Pubitemid 351962024
34. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441(7089):101-105
35. Kawai T, Akira S. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143:1-20
36. Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat Immunol 11(5):373-384
37. Kawashima T, Kosaka A, Yan H, Guo Z, Uchiyama R, Fukui R, Kaneko D, Kumagai Y, You DJ, Carreras J, Uematsu S, Jang MH, Takeuchi O, Kaisho T, Akira S, Miyake K, Tsutsui H, Saito T, Nishimura I, Tsuji NM. 2013. Double-stranded RNA of intestinal commensal but not pathogenic bacteria triggers production of protective interferon-beta. Immunity 38(6): 1187-1197
38. Kleinman ME, Yamada K, Takeda A, Chandrasekaran V, Nozaki M, Baffi JZ, Albuquerque RJ, Yamasaki S, Itaya M, Pan Y, Appukuttan B, Gibbs D, Yang Z, Kariko K, Ambati BK, Wilgus TA, DiPietro LA, Sakurai E, Zhang K, Smith JR, Taylor EW, Ambati J. 2008. Sequence- and target-independent angiogenesis suppression by siRNA via TLR3. Nature 452(7187):591-597. (Pubitemid 351483358
39. Kumar H, Kawai T, Kato H, Sato S, Takahashi K, Coban C, Yamamoto M, Uematsu S, Ishii KJ, Takeuchi O, Akira S. 2006. Essential role of IPS-1 in innate immune responses against RNA viruses. J Exp Med 203(7):1795-1803. (Pubitemid 44036284
40. Kumar H, Koyama S, Ishii KJ, Kawai T, Akira S. 2008. Cutting edge: Cooperation of IPS-1- and TRIF-dependent pathways in poly IC-enhanced antibody production and cytotoxic T cell responses. J Immunol 180(2):683-687
41. Kuo RL, Kao LT, Lin SJ, Wang RY, Shih SR. 2013. MDA5 plays a crucial role in enterovirus 71 RNA-mediated IRF3 activation. PLoS One 8(5):e63431
42. Lazear HM, Pinto AK, Ramos HJ, Vick SC, Shrestha B, Suthar MS, Gale M, Jr., Diamond MS. 2013. Pattern recognition receptor MDA5 modulates CD8 + T cell-dependent clearance of West Nile virus from the central nervous system. J Virol 87(21):11401-11415
43. Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E, Chignard M, Si-Tahar M. 2007. Cutting edge: Influenza A virus activates TLR3-dependent inflammatory and RIG-Idependent antiviral responses in human lung epithelial cells. J Immunol 178(6):3368-3372. (Pubitemid 46417600
44. Li Y, Zhang X, Polakiewicz RD, Yao TP, Comb MJ. 2008. HDAC6 is required for epidermal growth factor-induced beta-catenin nuclear localization. J Biol Chem 283(19): 12686-12690
45. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez-Sobrido L, Akira S, Gill MA, Garcia-Sastre A, Katze MG, Gale M, Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82(1):335-345. (Pubitemid 350309149
46. Loo YM, Gale M, Jr. 2011. Immune signaling by RIG-I-like receptors. Immunity 34(5):680-692
47. Malathi K, Dong B, Gale M, Jr., Silverman RH. 2007. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 448(7155):816-819. (Pubitemid 47266340
48. Martinez-Gil L, Goff PH, Hai R, Garcia-Sastre A, Shaw ML, Palese P. 2013. A Sendai virus-derived RNA agonist of RIG-I as a virus vaccine adjuvant. J Virol 87(3):1290-1300
49. McCartney SA, Vermi W, Lonardi S, Rossini C, Otero K, Calderon B, Gilfillan S, Diamond MS, Unanue ER, Colonna M. 2011. RNA sensor-induced type I IFN prevents diabetes caused by a beta cell-Tropic virus in mice. J Clin Invest 121(4):1497-1507
50. Moresco EM, Beutler B. 2010. LGP2: Positive about viral sensing. Proc Natl Acad Sci U S A 107(4):1261-1262
51. Nakhaei P, Genin P, Civas A, Hiscott J. 2009. RIG-I-like receptors: Sensing and responding to RNA virus infection. Semin Immunol 21(4):215-222
52. Oshiumi H, Miyashita M, Inoue N, Okabe M, Matsumoto M, Seya T. 2010. The ubiquitin ligase Riplet is essential for RIGI-dependent innate immune responses to RNA virus infection. Cell Host Microbe 8(6):496-509
53. Pauli EK, Chan YK, Davis ME, Gableske S, Wang MK, Feister KF, Gack MU. 2014. The ubiquitin-specific protease USP15 promotes RIG-I-mediated antiviral signaling by deubiquitylating TRIM25. Sci Signal 7(307):ra3
54. Peters K, Chattopadhyay S, Sen GC. 2008. IRF-3 activation by Sendai virus infection is required for cellular apoptosis and avoidance of persistence. J Virol 82(7):3500-3508. (Pubitemid 351429925
55. Petrasek J, Iracheta-Vellve A, Csak T, Satishchandran A, Kodys K, Kurt-Jones EA, Fitzgerald KA, Szabo G. 2013. STINGIRF3 pathway links endoplasmic reticulum stress with hepatocyte apoptosis in early alcoholic liver disease. Proc Natl Acad Sci U S A 110(41):16544-16549
56. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5¢-phosphates. Science 314(5801):997-1001
57. Poeck H, Bscheider M, Gross O, Finger K, Roth S, Rebsamen M, Hannesschlager N, Schlee M, Rothenfusser S, Barchet W, Kato H, Akira S, Inoue S, Endres S, Peschel C, Hartmann G, Hornung V, Ruland J. 2010. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat Immunol 11(1):63-69
58. Rehwinkel J, Reis e Sousa C. 2010. RIGorous detection: Exposing virus through RNA sensing. Science 327(5963):284-286
59. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, Bier K, Robb N, Vreede F, Barclay W, Fodor E, Reis e Sousa C. 2010. RIG-I detects viral genomic RNA during negativestrand RNA virus infection. Cell 140(3):397-408
60. Reinert LS, Harder L, Holm CK, Iversen MB, Horan KA, Dagnaes-Hansen F, Ulhoi BP, Holm TH, Mogensen TH, Owens T, Nyengaard JR, Thomsen AR, Paludan SR. 2012. TLR3 deficiency renders astrocytes permissive to herpes simplex virus infection and facilitates establishment of CNS infection in mice. J Clin Invest 122(4):1368-1376
61. Rintahaka J, Wiik D, Kovanen PE, Alenius H, Matikainen S. 2008. Cytosolic antiviral RNA recognition pathway activates caspases 1 and 3. J Immunol 180(3):1749-1757
62. Sadler AJ, Williams BR. 2008. Interferon-inducible antiviral effectors. Nat Rev Immunol 8(7):559-568. (Pubitemid 351913674
63. Salaun B, Zitvogel L, Asselin-Paturel C, Morel Y, Chemin K, Dubois C, Massacrier C, Conforti R, Chenard MP, Sabourin JC, Goubar A, Lebecque S, Pierres M, Rimoldi D, Romero P, Andre F. 2011. TLR3 as a biomarker for the therapeutic efficacy of double-stranded RNA in breast cancer. Cancer Res 71(5):1607-1614
64. Samuel CE. 2011. Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology 411(2): 180-193
65. Sarkar SN, Elco CP, Peters KL, Chattopadhyay S, Sen GC. 2007. Two tyrosine residues of Toll-like receptor 3 trigger different steps of NF-kappa B activation. J Biol Chem 282(6): 3423-3427. (Pubitemid 47084419
66. Sarkar SN, Peters KL, Elco CP, Sakamoto S, Pal S, Sen GC. 2004. Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in Double-stranded RNA signaling. Nat Struct Mol Biol 11(11):1060-1067. (Pubitemid 39453334
67. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, Nakaya T, Katsuki M, Noguchi S, Tanaka N, Taniguchi T. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-Alpha/beta gene induction. Immunity 13(4):539-548
68. Satoh T, Kato H, Kumagai Y, Yoneyama M, Sato S, Matsushita K, Tsujimura T, Fujita T, Akira S, Takeuchi O. 2010. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc Natl Acad Sci U S A 107(4):1512-1517
69. Saunders LR, Barber GN. 2003. The dsRNA binding protein family: Critical roles, diverse cellular functions. FASEB J 17(9):961-983
70. Sen GC, Sarkar SN. 2005. Transcriptional signaling by doublestranded RNA: Role of TLR3. Cytokine Growth Factor Rev 16(1):1-14. (Pubitemid 40279114
71. Seth RB, Sun L, Ea CK, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122(5): 669-682. (Pubitemid 41242633
72. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, Hiscott J. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300(5622):1148-1151
73. Sherry B. 2009. Rotavirus and reovirus modulation of the interferon response. J Interferon Cytokine Res 29(9):559-567
74. Strahle L, Marq JB, Brini A, Hausmann S, Kolakofsky D, Garcin D. 2007. Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J Virol 81(22):12227-12237. (Pubitemid 350085838
75. Sun R, Zhang Y, Lv Q, Liu B, Jin M, Zhang W, He Q, Deng M, Liu X, Li G, Li Y, Zhou G, Xie P, Xie X, Hu J, Duan Z. 2011. Toll-like receptor 3 (TLR3) induces apoptosis via death receptors and mitochondria by up-regulating the transactivating p63 isoform alpha (TAP63alpha). J Biol Chem 286(18): 15918-15928
76. Sze A, Belgnaoui SM, Olagnier D, Lin R, Hiscott J, van Grevenynghe J. 2013. Host restriction factor SAMHD1 limits human T cell leukemia virus type 1 infection of monocytes via STING-mediated apoptosis. Cell Host Microbe 14(4):422-434
77. Tabeta K, Georgel P, Janssen E, Du X, Hoebe K, Crozat K, Mudd S, Shamel L, Sovath S, Goode J, Alexopoulou L, Flavell RA, Beutler B. 2004. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci U S A 101(10):3516-3521. (Pubitemid 38338227
78. Tormo D, Checinska A, Alonso-Curbelo D, Perez-Guijarro E, Canon E, Riveiro-Falkenbach E, Calvo TG, Larribere L, Megias D, Mulero F, Piris MA, Dash R, Barral PM, Rodriguez-Peralto JL, Ortiz-Romero P, Tuting T, Fisher PB, Soengas MS. 2009. Targeted activation of innate immunity for therapeutic induction of autophagy and apoptosis in melanoma cells. Cancer Cell 16(2):103-114
79. Vijay-Kumar M, Wu H, Aitken J, Kolachala VL, Neish AS, Sitaraman SV, Gewirtz AT. 2007. Activation of toll-like receptor 3 protects against DSS-induced acute colitis. Inflamm Bowel Dis 13(7):856-864. (Pubitemid 47203863
80. Wang P, Arjona A, Zhang Y, Sultana H, Dai J, Yang L, Le-Blanc PM, Doiron K, Saleh M, Fikrig E. 2010. Caspase-12 controls West Nile virus infection via the viral RNA receptor RIG-I. Nat Immunol 11(10):912-919
81. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. 2004. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10(12):1366-1373. (Pubitemid 40022719
82. White CL, Chattopadhyay S, Sen GC. 2011. Phosphatidylinositol 3-kinase signaling delays sendai virus-induced apoptosis by preventing XIAP degradation. J Virol 85(10): 5224-5227
83. Wies E, Wang MK, Maharaj NP, Chen K, Zhou S, Finberg RW, Gack MU. 2013. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 38(3):437-449
84. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, Takeuchi O, Sugiyama M, Okabe M, Takeda K, Akira S. 2003. Role of adaptor TRIF in the MyD88-independent tolllike receptor signaling pathway. Science 301(5633):640-643. (Pubitemid 36927946
85. Yamashita M, Chattopadhyay S, Fensterl V, Saikia P, Wetzel JL, Sen GC. 2012a. Epidermal growth factor receptor is essential for Toll-like receptor 3 signaling. Sci Signal 5(233):ra50
86. Yamashita M, Chattopadhyay S, Fensterl V, Zhang Y, Sen GC. 2012b. A TRIF-independent branch of TLR3 signaling. J Immunol 188(6):2825-2833
87. Yu M, Levine SJ. 2011. Toll-like receptor, RIG-I-like receptors and the NLRP3 inflammasome: Key modulators of innate immune responses to double-stranded RNA viruses. Cytokine Growth Factor Rev 22(2):63-72
88. Zeng W, Sun L, Jiang X, Chen X, Hou F, Adhikari A, Xu M, Chen ZJ. 2010. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141(2):315-330
89. Zhang SY, Herman M, Ciancanelli MJ, Perez de Diego R, Sancho-Shimizu V, Abel L, Casanova JL. 2013. TLR3 immunity to infection in mice and humans. Curr Opin Immunol 25(1):19-33
90. Zhang SY, Jouanguy E, Ugolini S, Smahi A, Elain G, Romero P, Segal D, Sancho-Shimizu V, Lorenzo L, Puel A, Picard C, Chapgier A, Plancoulaine S, Titeux M, Cognet C, von Bernuth H, Ku CL, Casrouge A, Zhang XX, Barreiro L, Leonard J, Hamilton C, Lebon P, Heron B, Vallee L, Quintana-Murci L, Hovnanian A, Rozenberg F, Vivier E, Geissmann F, Tardieu M, Abel L, Casanova JL. 2007. TLR3 deficiency in patients with herpes simplex encephalitis. Science 317(5844): 1522-1527. (Pubitemid 47417427