Activation of RIG-I-like receptor signal transduction

Critical Reviews in Biochemistry and Molecular Biology

Volumn 47, Issue 2, 2012, Pages 194-206

  Bruns, Annie M ^a   Horvath, Curt M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

interferon; LGP2; MDA5; RIG I; RLR

Indexed keywords

CYTOKINE; CYTOPLASM PROTEIN; DOUBLE STRANDED RNA; HOMEODOMAIN PROTEIN; INTERFERON; LIGAND; PATTERN RECOGNITION RECEPTOR; PROTEIN LGP2; PROTEIN MDA5; RECEPTOR PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RIG I LIKE RECEPTOR; RNA HELICASE; UNCLASSIFIED DRUG; VIRUS RNA;

ADAPTIVE IMMUNITY; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL PROTECTION; ENZYME ACTIVATION; ENZYME ACTIVITY; INNATE IMMUNITY; MAMMAL CELL; MOLECULAR MODEL; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN RNA BINDING; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; VIRUS INFECTION;

ANIMALS; IMMUNITY, INNATE; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PATTERN RECOGNITION; RNA HELICASES; RNA, VIRAL; SIGNAL TRANSDUCTION; VIRUS DISEASES;

EID: 84857393830     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409238.2011.630974     Document Type: Review

References (102)

1. Abdelhaleem M. 2005. RNA helicases: Regulators of differentiation. Clin Biochem 38:499-503. (Pubitemid 40693460)
2. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N, Goodbourn S, Randall RE. 2004. The V proteins of paramyxoviruses bind the IFNinducible RNA helicase, mda-5, and inhibit its activation of the IFN-β promoter. Proc Natl Acad Sci USA 101:17264-17269. (Pubitemid 39627808)
3. Arimoto K, Takahashi H, Hishiki T, Konishi H, Fujita T, Shimotohno K. 2007. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc Natl Acad Sci USA 104:7500-7505. (Pubitemid 47185935)
4. Bamming D, Horvath CM. 2009. Regulation of signal transduction by enzymatically inactive antiviral RNA helicase proteins MDA5, RIG-I, and LGP2. J Biol Chem 284:9700-9712.
5. Barral P, Polzella P, Bruckbauer A, van Rooijen N, Besra GS, Cerundolo V, Batista FD. 2010. CD169 macrophages present lipid antigens to mediate early activation of iNKT cells in lymph nodes. Nat Immunol 11:303-312.
6. Baum A, Sachidanandam R, García-Sastre A. 2010. Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci USA 107:16303-16308.
7. Bouchier-Hayes L, Martin SJ. 2002. CARD games in apoptosis and immunity. EMBO Rep 3:616-621.
8. Breiman A, Grandvaux N, Lin R, Ottone C, Akira S, Yoneyama M, Fujita T, Hiscott J, Meurs EF. 2005. Inhibition of RIG-I-dependent signaling to the interferon pathway during hepatitis C virus expression and restoration of signaling by IKKepsilon. J Virol 79:3969-3978. (Pubitemid 40388337)
9. Childs K, Stock N, Ross C, Andrejeva J, Hilton L, Skinner M, Randall R, Goodbourn S. 2007. mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359:190-200. (Pubitemid 46223502)
10. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834-840.
11. Clément JF, Meloche S, Servant MJ. 2008. The IKK-related kinases: From innate immunity to oncogenesis. Cell Res 18:889-899.
12. Cordin O, Banroques J, Tanner NK, Linder P. 2006. The DEAD-box protein family of RNA helicases. Gene 367:17-37. (Pubitemid 43286737)
13. Cui S, Eisenächer K, Kirchhofer A, Brzózka K, Lammens A, Lammens K, Fujita T, Conzelmann KK, Krug A, Hopfner KP. 2008. The C-terminal regulatory domain is the RNA 59-triphosphate sensor of RIG-I. Mol Cell 29:169-179. (Pubitemid 351172822)
14. Cui Y, Li M, Walton KD, Sun K, Hanover JA, Furth PA, Hennighausen L. 2001. The Stat3/5 locus encodes novel endoplasmic reticulum and helicase-like proteins that are preferentially expressed in normal and neoplastic mammary tissue. Genomics 78:129-134. (Pubitemid 34001416)
15. De La Cruz J, Kressler D, Linder P. 1999 Unwinding RNA in Saccharomyces cerevisiae: Dead-box proteins and related families. Trends Biochem Sci 24:192-198. (Pubitemid 29348454)
16. Diao F, Li S, Tian Y, Zhang M, Xu LG, Zhang Y, Wang RP, Chen D, Zhai Z, Zhong B, Tien P, Shu HB. 2007. Negative regulation of MDA5-but not RIG-I-mediated innate antiviral signaling by the dihydroxyacetone kinase. Proc Natl Acad Sci USA 104:11706-11711. (Pubitemid 47175077)
17. Diebold SS, Montoya M, Unger H, Alexopoulou L, Roy P, Haswell LE, Al-Shamkhani A, Flavell R, Borrow P, Reis e Sousa C. 2003. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424:324-328. (Pubitemid 36899375)
18. 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 4:491-496. (Pubitemid 36592443)
19. Fodor E, Pritlove DC, Brownlee GG. 1994. The influenza virus panhandle is involved in the initiation of transcription. J Virol 68:4092-4096. (Pubitemid 24177444)
20. Foy E, Li K, Wang C, Sumpter R Jr, Ikeda M, Lemon SM, Gale M Jr. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300:1145-1148. (Pubitemid 36583099)
21. Fredericksen BL, Keller BC, Fornek J, Katze MG, Gale M Jr. 2008. Establishment and maintenance of the innate antiviral response to West Nile Virus involves both RIG-I and MDA5 signaling through IPS-1. J Virol 82:609-616.
22. Friedman CS, O'Donnell MA, Legarda-Addison D, Ng A, Cárdenas WB, Yount JS, Moran TM, Basler CF, Komuro A, Horvath CM, Xavier R, Ting AT. 2008. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep 9:930-936.
23. Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, Carnero E, Farzan M, Inoue S, Jung JU, García-Sastre A. 2009. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5:439-449.
24. 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-I-mediated antiviral activity. Nature 446:916-920. (Pubitemid 46633167)
25. Gao D, Yang YK, Wang RP, Zhou X, Diao FC, Li MD, Zhai ZH, Jiang ZF, Chen DY. 2009. REUL is a novel E3 ubiquitin ligase and stimulator of retinoic-acid-inducible gene-I. PLoS ONE 4:e5760.
26. 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 USA 103:8459-8464. (Pubitemid 43838477)
27. 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:e1000734.
28. Habjan M, Andersson I, Klingström J, Schümann M, Martin A, Zimmermann P, Wagner V, Pichlmair A, Schneider U, Mühlberger E, Mirazimi A, Weber F. 2008. Processing of genome 59 termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE 3:e2032.
29. Hayakawa S, Shiratori S, Yamato H, Kameyama T, Kitatsuji C, Kashigi F, Goto S, Kameoka S, Fujikura D, Yamada T, Mizutani T, Kazumata M, Sato M, Tanaka J, Asaka M, Ohba Y, Miyazaki T, Imamura M, Takaoka A. 2011. ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses. Nat Immunol 12:37-44.
30. Hiscott J. 2007. Triggering the innate antiviral response through IRF-3 activation. J Biol Chem 282:15325-15329. (Pubitemid 47093257)
31. Hofmann K, Bucher P, Tschopp J. 1997. The CARD domain: A new apoptotic signalling motif. Trends Biochem Sci 22:155-156. (Pubitemid 27199314)
32. Hornung V, Ellegast J, Kim S, Brzózka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G. 2006. 59-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
33. 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 146:448-461.
34. Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P. 1987. Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci USA 84:8140-8144.
35. Inn KS, Gack MU, Tokunaga F, Shi M, Wong LY, Iwai K, Jung JU. 2011. Linear ubiquitin assembly complex negatively regulates RIG-Iand TRIM25-mediated type I interferon induction. Mol Cell 41:354-365.
36. Jankowsky E, Bowers H. 2006. Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases. Nucleic Acids Res 34:4181-4188. (Pubitemid 44542197)
37. Johnston MD. 1981. The characteristics required for a Sendai virus preparation to induce high levels of interferon in human lymphoblastoid cells. J Gen Virol 56:175-184. (Pubitemid 12208661)
38. Kang DC, Gopalkrishnan RV, Wu Q, Jankowsky E, Pyle AM, Fisher PB. 2002. mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci USA 99:637-642. (Pubitemid 34106564)
39. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, Matsui K, Tsujimura T, Takeda K, Fujita T, Takeuchi O, Akira S. 2005. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23:19-28. (Pubitemid 41019654)
40. 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 acidinducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205:1601-1610. (Pubitemid 351962024)
41. 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 441:101-105.
42. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. 2005. IPS-1, an adaptor triggering RIG-Iand Mda5-mediated type I interferon induction. Nat Immunol 6:981-988. (Pubitemid 41486182)
43. Kim DH, Longo M, Han Y, Lundberg P, Cantin E, Rossi JJ. 2004. Interferon induction by siRNAs and ssRNAs synthesized by phage polymerase. Nat Biotechnol 22:321-325. (Pubitemid 38295765)
44. Komuro A, Bamming D, Horvath CM. 2008. Negative regulation of cytoplasmic RNA-mediated antiviral signaling. Cytokine 43:350-358.
45. Komuro A, Horvath CM. 2006. RNA-and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J Virol 80:12332-12342. (Pubitemid 44904383)
46. Krug RM, Yuan W, Noah DL, Latham AG. 2003. Intracellular warfare between human influenza viruses and human cells: The roles of the viral NS1 protein. Virology 309:181-189. (Pubitemid 36579212)
47. Li X, Lu C, Stewart M, Xu H, Strong RK, Igumenova T, Li P. 2009a. Structural basis of double-stranded RNA recognition by the RIG-I like receptor MDA5. Arch Biochem Biophys 488:23-33.
48. Li X, Ranjith-Kumar CT, Brooks MT, Dharmaiah S, Herr AB, Kao C, Li P. 2009b. The RIG-I-like receptor LGP2 recognizes the termini of double-stranded RNA. J Biol Chem 284:13881-13891.
49. Li XD, Sun L, Seth RB, Pineda G, Chen ZJ. 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. (Pubitemid 41803563)
50. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez-Sobrido L, Akira S, Gill MA, García-Sastre A, Katze MG, Gale M Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82:335-345. (Pubitemid 350309149)
51. Lu C, Ranjith-Kumar CT, Hao L, Kao CC, Li P. 2011. Crystal structure of RIG-I C-terminal domain bound to blunt-ended doublestrand RNA without 59 triphosphate. Nucleic Acids Res 39: 1565-1575.
52. Lu C, Xu H, Ranjith-Kumar CT, Brooks MT, Hou TY, Hu F, Herr AB, Strong RK, Kao CC.& Li P. (2010). The structural basis of 59 triphosphate double-stranded rna recognition by rig-i c-terminal domain. Structure, 1-12.
53. Marques JT, Devosse T, Wang D, Zamanian-Daryoush M, Serbinowski P, Hartmann R, Fujita T, Behlke MA, Williams BR. 2006. A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat Biotechnol 24:559-565.
54. McCartney SA, Thackray LB, Gitlin L, Gilfillan S, Virgin HW, Virgin Iv HW, Colonna M. 2008. MDA-5 recognition of a murine norovirus. PLoS Pathog 4:e1000108.
55. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, 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. (Pubitemid 41509355)
56. Moresco EM, Beutler B. 2010. LGP2: Positive about viral sensing. Proc Natl Acad Sci USA 107:1261-1262.
57. Myong S, Cui S, Cornish PV, Kirchhofer A, Gack MU, Jung JU, Hopfner KP, Ha T. 2009. Cytosolic viral sensor RIG-I is a 59-triphosphatedependent translocase on double-stranded RNA. Science 323:1070-1074.
58. Myong S, Ha T. 2010. Stepwise translocation of nucleic acid motors. Curr Opin Struct Biol 20:121-127.
59. Nishino T, Komori K, Tsuchiya D, Ishino Y, Morikawa K. 2005. Crystal structure and functional implications of Pyrococcus furiosus hef helicase domain involved in branched DNA processing. Structure 13:143-153. (Pubitemid 40092482)
60. Oganesyan G, Saha SK, Guo B, He JQ, Shahangian A, Zarnegar B, Perry A, Cheng G. 2006. Critical role of TRAF3 in the Toll-like receptor-dependent and-independent antiviral response. Nature 439:208-211. (Pubitemid 43083142)
61. Oshiumi H, Matsumoto M, Hatakeyama S, Seya T. 2009. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-β induction during the early phase of viral infection. J Biol Chem 284:807-817.
62. Oshiumi H, Miyashita M, Inoue N, Okabe M, Matsumoto M, Seya T. 2010. The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 8:496-509.
63. Parisien JP, Bamming D, Komuro A, Ramachandran A, Rodriguez JJ, Barber G, Wojahn RD, Horvath CM. 2009. A shared interface mediates paramyxovirus interference with antiviral RNA helicases MDA5 and LGP2. J Virol 83:7252-7260.
64. Pichlmair A, Schulz O, Tan CP, Rehwinkel J, Kato H, Takeuchi O, Akira S, Way M, Schiavo G, Reis e Sousa C. 2009. Activation of MDA5 requires higher-order RNA structures generated during virus infection. J Virol 83:10761-10769.
65. Pichlmair A, Schulz O, Tan CP, Näslund TI, Liljeström P, Weber F, Reis e Sousa C. 2006. RIG-I-mediated antiviral responses to singlestranded RNA bearing 59-phosphates. Science 314:997-1001. (Pubitemid 44749946)
66. Plumet S, Herschke F, Bourhis JM, Valentin H, Longhi S, Gerlier D. 2007. Cytosolic 59-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS ONE 2:e279.
67. Pollpeter D, Komuro A, Barber GN, Horvath CM. 2011. Impaired cellular responses to cytosolic DNA or infection with Listeria monocytogenes and vaccinia virus in the absence of the murine LGP2 protein. PLoS ONE 6:e18842.
68. Pyle AM. 2008. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu Rev Biophys 37:317-336.
69. Pyle AM, Fedorova O, Waldsich C. 2007. Folding of group II introns: A model system for large, multidomain RNAs? Trends Biochem Sci 32:138-145. (Pubitemid 46367692)
70. Randall RE, Goodbourn S. 2008. Interferons and viruses: An interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47.
71. 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 negative-strand RNA virus infection. Cell 140:397-408.
72. Rothenfusser S, Goutagny N, DiPerna G, Gong M, Monks BG, Schoenemeyer A, Yamamoto M, Akira S, Fitzgerald KA. 2005. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J Immunol 175:5260-5268. (Pubitemid 41456411)
73. Saha SK, Pietras EM, He JQ, Kang JR, Liu SY, Oganesyan G, Shahangian A, Zarnegar B, Shiba TL, Wang Y, Cheng G. 2006. Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J 25:3257-3263. (Pubitemid 44141784)
74. Saito T, Hirai R, Loo YM, Owen D, Johnson CL, Sinha SC, Akira S, Fujita T, Gale M Jr. 2007. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci USA 104:582-587. (Pubitemid 46123068)
75. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M Jr. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454:523-527.
76. 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 USA 107:1512-1517.
77. Schlee M, Hartmann G. 2010. The chase for the RIG-I ligand-recent advances. Mol Ther 18:1254-1262.
78. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834-840.
79. Schmidt A, Endres S, Rothenfusser S. 2011. Pattern recognition of viral nucleic acids by RIG-I-like helicases. J Mol Med 89:5-12.
80. Schmidt A, Schwerd T, Hamm W, Hellmuth JC, Cui S, Wenzel M, Hoffmann FS, Michallet MC, Besch R, Hopfner KP, Endres S, Rothenfusser S. 2009. 59-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc Natl Acad Sci USA 106:12067-12072.
81. Schneider U, Schwemmle M, Staeheli P. 2005. Genome trimming: A unique strategy for replication control employed by Borna disease virus. Proc Natl Acad Sci USA 102:3441-3446. (Pubitemid 40328064)
82. Seth RB, Sun L, Ea CK, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 122:669-682. (Pubitemid 41242633)
83. Sumpter R Jr, Loo YM, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79:2689-2699. (Pubitemid 40270547)
84. Sun YW. (1997) Rig-I, a human homolog gene of RNA helicase, is induced by retinoic acid during the differentiation of acute promyelocytic leukemia cell. Thesis, Shanghai Second Medical University.
85. Sun Z, Ren H, Liu Y, Teeling JL, Gu J. 2011. Phosphorylation of RIG-I by casein kinase II inhibits its antiviral response. J Virol 85:1036-1047.
86. Takahasi K, Kumeta H, Tsuduki N, Narita R, Shigemoto T, Hirai R, Yoneyama M, Horiuchi M, Ogura K, Fujita T, Inagaki F. 2009. Solution structures of cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: Identification of the RNA recognition loop in RIG-I-like receptors. J Biol Chem 284:17465-17474.
87. Takahasi K, Yoneyama M, Nishihori T, Hirai R, Kumeta H, Narita R, Gale M Jr, Inagaki F, Fujita T. 2008. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol Cell 29:428-440.
88. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820.
89. Uzri D, Gehrke L. 2009. Nucleotide sequences and modifications that determine RIG-I/RNA binding and signaling activities. J Virol 83:4174-4184.
90. Vartapetian AB, Drygin YF, Chumakov KM, Bogdanov AA. 1980. The structure of the covalent linkage between proteins and RNA in encephalomyocarditis virus. Nucleic Acids Res 8:3729-3742. (Pubitemid 11246366)
91. Venkataraman T, Valdes M, Elsby R, Kakuta S, Caceres G, Saijo S, Iwakura Y, Barber GN. 2007. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J Immunol 178:6444-6455. (Pubitemid 46717428)
92. Vitour D, Meurs EF. 2007. Regulation of interferon production by RIG-I and LGP2: A lesson in self-control. Sci STKE 2007:pe20.
93. Walker JE, Saraste M, Runswick MJ, Gay NJ. 1982. Distantly related sequences in the α-and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945-951.
94. Wang Y, Ludwig J, Schuberth C, Goldeck M, Schlee M, Li H, Juranek S, Sheng G, Micura R, Tuschl T, Hartmann G, Patel DJ. 2010. Structural and functional insights into 59-ppp RNA pattern recognition by the innate immune receptor RIG-I. Nat Struct Mol Biol 17:781-787.
95. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. 2005. VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol Cell 19:727-740. (Pubitemid 41316668)
96. Yoneyama M, Fujita T. 2009. RNA recognition and signal transduction by RIG-I-like receptors. Immunol Rev 227:54-65.
97. Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, Taira K, Foy E, Loo YM, Gale M Jr, Akira S, Yonehara S, Kato A, 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. (Pubitemid 41170502)
98. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, 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. (Pubitemid 39023305)
99. 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 141:315-330.
100. Zhang M, Wu X, Lee AJ, Jin W, Chang M, Wright A, Imaizumi T, Sun SC. 2008. Regulation of IκB kinase-related kinases and antiviral responses by tumor suppressor CYLD. J Biol Chem 283:18621-18626.
101. Zou J, Chang M, Nie P, Secombes CJ. 2009. Origin and evolution of the RIG-I like RNA helicase gene family. BMC Evol Biol 9:85.
102. Züst R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, Ziebuhr J, Szretter KJ, Baker SC, Barchet W, Diamond MS, Siddell SG, Ludewig B, Thiel V. 2011. Ribose 29-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.