Systems Analysis of a RIG-I Agonist Inducing Broad Spectrum Inhibition of Virus Infectivity

PLoS Pathogens

Volumn 9, Issue 4, 2013, Pages

  Goulet, Marie Line ^a   Olagnier, David ^b   Xu, Zhengyun ^a,c   Paz, Suzanne ^a   Belgnaoui, S Mehdi ^a   Lafferty, Erin I ^c   Janelle, Valérie ^d   Arguello, Meztli ^a   Paquet, Marilene ^e   Ghneim, Khader ^b   Richards, Stephanie ^b   Smith, Andrew ^b   Wilkinson, Peter ^b   Cameron, Mark ^b   Kalinke, Ulrich ^f   Qureshi, Salman ^c   Lamarre, Alain ^d   Haddad, Elias K ^b   Sekaly, Rafick Pierre ^b   Peri, Suraj ^g   Balachandran, Siddharth ^g   Lin, Rongtuan ^a,c   Hiscott, John ^b   more..

^a MCGILL UNIVERSITY   (Canada)

^b Vaccine and Gene Therapy Institute of Florida   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d INRS INSTITUT ARMAND FRAPPIER   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^g FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 TRIPHOSPHATE RNA; ANTIVIRUS AGENT; CASPASE 3; CHORIONIC GONADOTROPIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 28A; INTERLEUKIN 29; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN NOXA; RANTES; STAT1 PROTEIN; TRIAMCINOLONE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CELL ISOLATION; CONTROLLED STUDY; DIMERIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTOLOGY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOBLOTTING; INNATE IMMUNITY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PNEUMONIA; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIRUS INFECTIVITY; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; ENZYME ACTIVATION; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTOR-7; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, RETINOIC ACID; RNA INTERFERENCE; RNA, VIRAL; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR;

ANIMALIA; DNA VIRUSES; MUS; RNA VIRUSES;

EID: 84876854916     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003298     Document Type: Article

References (87)

1. Takeuchi O, Akira S, (2009) Innate immunity to virus infection. Immunol Rev 227: 75-86.
2. Yoneyama M, Fujita T, (2010) Recognition of viral nucleic acids in innate immunity. Rev Med Virol 20: 4-22.
3. Wilkins C, Gale M Jr, (2010) Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol 22: 41-47.
4. Brennan K, Bowie AG, (2010) Activation of host pattern recognition receptors by viruses. Curr Opin Microbiol 13: 503-507.
5. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
6. Liu SY, Sanchez DJ, Cheng G, (2011) New developments in the induction and antiviral effectors of type I interferon. Curr Opin Immunol 23: 57-64.
7. Akira S, Uematsu S, Takeuchi O, (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
8. Kumar H, Kawai T, Akira S, (2011) Pathogen recognition by the innate immune system. Int Rev Immunol 30: 16-34.
9. Loo YM, Gale M Jr, (2011) Immune signaling by RIG-I-like receptors. Immunity 34: 680-692.
10. Belgnaoui SM, Paz S, Hiscott J, (2011) Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Current Opinion in Immunology 23: 564-572.
11. Beutler BA, (2009) TLRs and innate immunity. Blood 113: 1399-1407.
12. Kawai T, Akira S, (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650.
13. Jiang F, Ramanathan A, Miller MT, Tang GQ, Gale M Jr, et al. (2011) Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 479: 423-427.
14. Yoneyama M, Fujita T, (2007) Function of RIG-I-like receptors in antiviral innate immunity. J Biol Chem 282: 15315-15318.
15. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988.
16. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172.
17. Schlee M, Roth AR, Hornung VH, Hagmann CA, Wimmenauer V, 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: 25-34.
18. Kowalinski E, Lunardi T, McCarthy AA, Louber J, Brunel J, et al. (2011) Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 147: 423-435.
19. Myong S, Cui S, Cornish PV, Kirchhofer A, Gack MU, et al. (2009) Cytosolic Viral Sensor RIG-I Is a 5′-Triphosphate-Dependent Translocase on Double-Stranded RNA. Science 323: 1070-1074.
20. Jiang X, Kinch LN, Brautigam CA, Chen X, Du F, et al. (2012) Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36: 959-973.
21. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin RT, et al. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151.
22. Xu LG, Wang YY, Han KJ, Li LY, Zhai ZH, et al. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Molecular Cell 19: 727-740.
23. Seth RB, Sun L, Ea CKaC, Z.J., (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
24. Tamassia N, Le Moigne V, Rossato M, Donini M, McCartney S, et al. (2008) Activation of an immunoregulatory and antiviral gene expression program in poly(I:C)-transfected human neutrophils. J Immunol 181: 6563-6573.
25. Kawai T, Akira S, (2008) Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143: 1-20.
26. Wang BX, Fish EN, (2012) The yin and yang of viruses and interferons. Trends Immunol 33: 190-197.
27. Nakhaei P, Paz S, Hiscott J (2006) Activation of Interferon Gene Expression Through Toll-like Receptor-dependent and-independent Pathways. The Interferons: Characterization and Application. Weinheim, FRG.: Wiley-VCH Verlag GmbH & Co. KGaA.
28. Sadler AJ, Williams BR, (2008) Interferon-inducible antiviral effectors. Nat Rev Immunol 8: 559-568.
29. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, et al. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485.
30. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 5′-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
31. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, et al. (2006) RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314: 997-1001.
32. Kim DH, Longo M, Han Y, Lundberg P, Cantin E, et al. (2004) Interferon induction by siRNAs and ssRNAs synthesized by phage polymerase. Nat Biotechnol 22: 321-325.
33. Fujita T, (2009) A nonself RNA pattern: tri-p to panhandle. Immunity 31: 4-5.
34. Schlee M, Hartmann G, (2010) The Chase for the RIG-I Ligand-Recent Advances. Molecular Therapy 18: 1254-1262.
35. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, 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: 1601-1610.
36. Baum A, Sachidanandam R, Garcia-Sastre A, (2010) Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc Natl Acad Sci U S A 107: 16303-16308.
37. Rehwinkel J, Sousa CRE, (2010) RIGorous Detection: Exposing Virus Through RNA Sensing. Science 327: 284-286.
38. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, et al. (2010) RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 140: 397-408.
39. Cui S, Katharina E, Kirchhofer A, Brzózka K, Lammens A, et al. (2008) The C-Terminal Regulatory Domain Is the RNA 5′-Triphosphate Sensor of RIG-I. Molecular Cell 29: 169-179.
40. Goubau D, Romieu-Mourez R, Solis M, Hernandez E, Mesplede T, et al. (2009) Transcriptional re-programming of primary macrophages reveals distinct apoptotic and anti-tumoral functions of IRF-3 and IRF-7. Eur J Immunol 39: 527-540.
41. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.
42. Akhurst RJ, Hata A, (2012) Targeting the TGFbeta signalling pathway in disease. Nature reviews Drug discovery 11: 790-811.
43. McNab FW, Rajsbaum R, Stoye JP, O'Garra A, (2011) Tripartite-motif proteins and innate immune regulation. Curr Opin Immunol 23: 46-56.
44. Ozato K, Shin DM, Chang TH, Morse HC 3rd, (2008) TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol 8: 849-860.
45. Barr SD, Smiley JR, Bushman FD, (2008) The interferon response inhibits HIV particle production by induction of TRIM22. PLoS Pathog 4: e1000007.
46. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, et al. (2009) The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139: 1243-1254.
47. Feeley EM, Sims JS, John SP, Chin CR, Pertel T, et al. (2011) IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog 7: e1002337.
48. Everitt AR, Clare S, Pertel T, John SP, Wash RS, et al. (2012) IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484: 519-523.
49. Haller O, Staeheli P, Kochs G, (2007) Interferon-induced Mx proteins in antiviral host defense. Biochimie 89: 812-818.
50. Haller O, Stertz S, Kochs G, (2007) The Mx GTPase family of interferon-induced antiviral proteins. Microbes Infect 9: 1636-1643.
51. Jiang D, Guo H, Xu C, Chang J, Gu B, et al. (2008) Identification of three interferon-inducible cellular enzymes that inhibit the replication of hepatitis C virus. J Virol 82: 1665-1678.
52. Helbig KJ, Lau DT, Semendric L, Harley HA, Beard MR, (2005) Analysis of ISG expression in chronic hepatitis C identifies viperin as a potential antiviral effector. Hepatology 42: 702-710.
53. Wang X, Hinson ER, Cresswell P, (2007) The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host Microbe 2: 96-105.
54. Maher SG, Sheikh F, Scarzello AJ, Romero-Weaver AL, Baker DP, et al. (2008) IFN-α and IFN-λ differ in their antiproliferative effects and duration of JAK/STAT signaling activity. Cancer Biology & Therapy 7: 1109-1115.
55. Mordstein M, Kochs G, Dumoutier L, Renauld JC, Paludan SR, et al. (2008) Interferon-lambda contributes to innate immunity of mice against influenza A virus but not against hepatotropic viruses. PLoS Pathog 4: e1000151.
56. Tian RR, Guo HX, Wei JF, Yang CK, He SH, et al. (2012) IFN-lambda inhibits HIV-1 integration and post-transcriptional events in vitro, but there is only limited in vivo repression of viral production. Antiviral Res 95: 57-65.
57. Pagliaccetti NE, Eduardo R, Kleinstein SH, Mu XJ, Bandi P, et al. (2008) Interleukin-29 functions cooperatively with interferon to induce antiviral gene expression and inhibit hepatitis C virus replication. J Biol Chem 283: 30079-30089.
58. Kelly C, Klenerman P, Barnes E, (2011) Interferon lambdas: the next cytokine storm. Gut 60: 1284-1293.
59. Yoshimura A, Yasukawa H, (2012) JAK's SOCS: a mechanism of inhibition. Immunity 36: 157-159.
60. Shembade N, Ma A, Harhaj EW, (2010) Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 327: 1135-1139.
61. Tak PP, Firestein GS, (2001) NF-kappaB: a key role in inflammatory diseases. J Clin Invest 107: 7-11.
62. Dejean AS, Beisner DR, Ch'en IL, Kerdiles YM, Babour A, et al. (2009) Transcription factor Foxo3 controls the magnitude of T cell immune responses by modulating the function of dendritic cells. Nat Immunol 10: 504-513.
63. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, et al. (2007) Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445: 319-323.
64. Ranjan P, Jayashankar L, Deyde V, Zeng H, Davis WG, et al. (2010) 5′PPP-RNA induced RIG-I activation inhibits drug-resistant avian H5N1 as well as 1918 and 2009 pandemic influenza virus replication. Virol J 7: 102.
65. Chakravarthy KV, Bonoiu AC, Davis WG, Ranjan P, Ding H, et al. (2010) Gold nanorod delivery of an ssRNA immune activator inhibits pandemic H1N1 influenza viral replication. Proc Natl Acad Sci U S A 107: 10172-10177.
66. Lin L, Liu Q, Berube N, Detmer S, Zhou Y, (2012) 5′ triphosphate-siRNA: potent inhibition of influenza A virus infection by gene silencing and RIG-I activation. J Virol 86: 10359-69.
67. Martinez-Gil L, Goff PH, Hai R, Garcia-Sastre A, Shaw ML, et al. (2013) A Sendai Virus-Derived RNA Agonist of RIG-I as a Virus Vaccine Adjuvant. Journal of Virology 87: 1290-1300.
68. Takaoka A, Hayakawa S, Yanai H, Stoiber D, Negishi H, et al. (2003) Integration of interferon-alpha/beta signalling to p53 responses in tumour suppression and antiviral defence. Nature 424: 516-523.
69. Kelchtermans H, Billiau A, Matthys P, (2008) How interferon-gamma keeps autoimmune diseases in check. Trends Immunol 29: 479-486.
70. Lotrich FE, Ferrell RE, Rabinovitz M, Pollock BG, (2009) Risk for depression during interferon-alpha treatment is affected by the serotonin transporter polymorphism. Biol Psychiatry 65: 344-348.
71. Caskey M, Lefebvre F, Filali-Mouhim A, Cameron MJ, Goulet JP, et al. (2011) Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J Exp Med 208: 2357-2366.
72. Mazaleuskaya L, Veltrop R, Ikpeze N, Martin-Garcia J, Navas-Martin S, (2012) Protective role of Toll-like Receptor 3-induced type I interferon in murine coronavirus infection of macrophages. Viruses 4: 901-923.
73. Zhao J, Wohlford-Lenane C, Zhao J, Fleming E, Lane TE, et al. (2012) Intranasal treatment with poly I:C protects aged mice from lethal respiratory viral infections. J Virol 86: 11416-24.
74. Gaucher D, Therrien R, Kettaf N, Angermann BR, Boucher G, et al. (2008) Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J Exp Med 205: 3119-3131.
75. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, et al. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity 23: 19-28.
76. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, et al. (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: 8459-8464.
77. McCartney S, Vermi W, Gilfillan S, Cella M, Murphy TL, et al. (2009) Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J Exp Med 206: 2967-2976.
78. Zhao T, Yang L, Sun Q, Arguello M, Ballard DW, et al. (2007) The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways. Nat Immunol 8: 592-600.
79. Stojdl D, Lichty B, tenOever B, Paterson J, Power A, et al. (2003) VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4: 263-275.
80. Tumilasci VF, Oliere S, Nguyen TL, Shamy A, Bell J, et al. (2008) Targeting the apoptotic pathway with BCL-2 inhibitors sensitizes primary chronic lymphocytic leukemia cells to vesicular stomatitis virus-induced oncolysis. J Virol 82: 8487-8499.
81. Myskiw C, Arsenio J, Hammett C, van Bruggen R, Deschambault Y, et al. (2011) Comparative analysis of poxvirus orthologues of the vaccinia virus E3 protein: modulation of protein kinase R activity, cytokine responses, and virus pathogenicity. J Virol 85: 12280-12291.
82. Arseniob J, Deschambaulta Y, Cao J, (2008) Antagonizing activity of vaccinia virus E3L against human interferons in Huh7 cells. Virology 377: 124-132.
83. Schindler M, Munch J, Kirchhoff F, (2005) Human immunodeficiency virus type 1 inhibits DNA damage-triggered apoptosis by a Nef-independent mechanism. J Virol 79: 5489-5498.
84. Schindler M, Wurfl S, Benaroch P, Greenough TC, Daniels R, et al. (2003) Down-modulation of mature major histocompatibility complex class II and up-regulation of invariant chain cell surface expression are well-conserved functions of human and simian immunodeficiency virus nef alleles. J Virol 77: 10548-10556.
85. Szretter KJ, Balish AL, Katz JM, (2006) Influenza: propagation, quantification, and storage. Curr Protoc Microbiol Chapter 15: Unit 15G.1.
86. Smyth GK, Gentleman R, Carey VC, Dudoit S, Irizarry R, et al. (2005) Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor. New York: Springer. pp. 397-420.
87. Benjamini YaH, Yosef, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289-300.