ATPase-driven oligomerization of RIG-I on RNA allows optimal activation of type-I interferon

EMBO Reports

Volumn 14, Issue 9, 2013, Pages 780-787

  Patel, Jenish R ^a   Jain, Ankur ^b,c   Chou, Yi Ying ^a   Baum, Alina ^d   Ha, Taekjip ^b,c   García Sastre, Adolfo ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

ATP; Defective interfering RNA; Interferon; Oligomerization; RIG I

Indexed keywords

ADENOSINE TRIPHOSPHATASE; INTERFERON; RETINOIC ACID INDUCIBLE PROTEIN I; RNA;

ARTICLE; ENZYME ACTIVITY; HYDROLYSIS; IN VITRO STUDY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; RNA SEQUENCE; SENDAI VIRUS;

SENDAI VIRUS;

ADENOSINE TRIPHOSPHATE; HEK293 CELLS; HUMANS; HYDROLYSIS; INTERFERON TYPE I; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RNA HELICASES; RNA, VIRAL; SENDAI VIRUS;

EID: 84883487585     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2013.102     Document Type: Article

References (29)

1. Ranjan P, Bowzard JB, Schwerzmann JW, Jeisy-Scott V, Fujita T, Sambhara S (2009) Cytoplasmic nucleic acid sensors in antiviral immunity. Trends Mol Med 15: 359-368
2. 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
3. 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
4. Schlee M, 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
5. Schmidt A, et al (2009) 5′-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc Natl Acad Sci USA 106: 12067-12072
6. Kowalinski E, Lunardi T, Mccarthy AA, Louber J, Brunel J, Grigorov B, Gerlier D, Cusack S (2011) Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 147: 423-435
7. Gack MU, et al (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446: 916-920
8. 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
9. Jiang X, Kinch LN, Brautigam Ca, Chen X, Du F, Grishin NV, Chen ZJ (2012) Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36: 959-973
10. Seth RB, Sun L, Ea C-K, Chen ZJ (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682
11. Xu L-G, Wang Y-Y, Han K-J, Li L-Y, Zhai Z, Shu H-B (2005) VISA is an adapter protein required for virus-triggered IFN-b signaling. Mol Cell 19: 727-740
12. 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
13. 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-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988
14. Hou F, Sun L, Zheng H, Skaug B, Jiang Q-X, Chen Zhijian J (2011) MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146: 448-461
15. Onoguchi K, Onomoto K, Takamatsu S, Jogi M, Takemura A, Morimoto S, Julkunen I, Namiki H, Yoneyama M, Fujita T (2010) Virus-infection or 5′ppp-RNA activates antiviral signal through redistribution of IPS-1 mediated by MFN1. PLoS Pathog 6: E1001012
16. Servant MJ, Grandvaux N, Hiscott J (2002) Multiple signaling pathways leading to the activation of interferon regulatory factor 3. Biochem Pharmacol 64: 985-992
17. Sharma S, tenOever BR, Grandvaux N, Zhou G-P, Lin R, Hiscott J (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151
18. Panne D (2008) The enhanceosome. Curr Opin Struct Biol 18: 236-242
19. Dixit E, et al (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141: 668-681
20. Myong S, Cui S, Cornish PV, Kirchhofer A, GackMU, Jung JU, Hopfner K-P, Ha T (2009) Cytosolic viral sensor RIG-I is a 5′-triphosphatedependent translocase on double-stranded RNA. Science 323: 1070-1074
21. Rehwinkel J, et al (2010) RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 140: 397-408
22. Baum A, García-Sastre A (2011) Differential recognition of viral RNA by RIG-I. Virulence 2: 166-169
23. Baum A, Sachidanandam R, García-Sastre A (2010) Preference of RIG-I for short viral RNA molecules in infected cells revealed by nextgeneration sequencing. Proc Natl Acad Sci USA 107: 16303-16308
24. Strahle L, Garcin D, Kolakofsky D (2006) Sendai virus defectiveinterfering genomes and the activation of interferon-beta. Virology 351: 101-111
25. 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 5′ triphosphate double-stranded RNA recognition by RIG-I C-terminal domain. Structure 18: 1032-1043
26. Cui S, Eisenächer K, Kirchhofer A, Brzözka 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: 169-179
27. Binder M, Eberle F, Seitz S, Mücke N, Hüber CM, Kiani N, Kaderali L, Lohmann V, Dalpke A, Bartenschlager R (2011) Molecular mechanism of signal perception and integration by the innate immune sensor retinoic acid-inducible gene-I (RIG-I). J Biol Chem 286: 27278-27287
28. Peisley A, Lin C, Wu B, Orme-Johnson M, Liu M, Walz T, Hur S (2011) Cooperative assembly and dynamic disassembly of MDA5 filaments for viral dsRNA recognition. Proc Natl Acad Sci USA 108: 21010-21015
29. Berke IC, Modis Y (2012) MDA5 cooperatively forms dimers and ATP sensitive filaments upon binding to dsRNA. EMBO J 31: 1714-1726