The Golgi apparatus acts as a platform for TBK1 activation after viral RNA sensing

BMC Biology

Volumn 14, Issue 1, 2016, Pages

  Pourcelot, Marie ^a,b,c   Zemirli, Naima ^a,b,c   Silva Da Costa, Leandro ^a,b,c   Loyant, Roxane ^a,b,c   Garcin, Dominique ^d   Vitour, Damien ^e   Munitic, Ivana ^f   Vazquez, Aimé ^a,b,c   Arnoult, Damien ^a,b,c  

^a HÔPITAL PAUL BROUSSE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Equipe Labellisée Ligue Nationale Contre le Cancer   (France)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^f University of Rijeka   (Croatia)

Author keywords

[No Author keywords available]

Indexed keywords

DDX58 PROTEIN, HUMAN; INTERFERON REGULATORY FACTOR 3; OPTN PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; RETINOIC ACID INDUCIBLE PROTEIN I; S10 PROTEIN, BLUETONGUE VIRUS; TBK1 PROTEIN, HUMAN; TLR3 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 3; TRANSCRIPTION FACTOR IIIA; VIRAL PROTEIN;

GENETIC TRANSFECTION; GENETICS; GOLGI COMPLEX; HEK293 CELL LINE; HELA CELL LINE; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PHOSPHORYLATION; RNA VIRUS; RNA VIRUS INFECTION; SIGNAL TRANSDUCTION; UBIQUITINATION; VIROLOGY;

DEAD BOX PROTEIN 58; GOLGI APPARATUS; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA VIRUS INFECTIONS; RNA VIRUSES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TRANSCRIPTION FACTOR TFIIIA; TRANSFECTION; UBIQUITINATION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84982239173     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-016-0292-z     Document Type: Article

References (47)

1. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124:783-801.
2. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140:805-20.
3. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol. 2014;14:36-49.
4. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M. Functional role of type I and type II interferons in antiviral defense. Science. 1994;264:1918-21.
5. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol. 2004;4:499-511.
6. Jiang X, Chen ZJ. The role of ubiquitylation in immune defence and pathogen evasion. Nat Rev Immunol. 2012;12:35-48.
7. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao SM, Maniatis T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol. 2003;4:491-6.
8. Hemmi H, Takeuchi O, Sato S, Yamamoto M, Kaisho T, Sanjo H, Kawai T, Hoshino K, Takeda K, Akira S. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J Exp Med. 2004;199:1641-50.
9. Perry AK, Chow EK, Goodnough JB, Yeh WC, Cheng G. Differential requirement for TANK-binding kinase-1 in type I interferon responses to toll-like receptor activation and viral infection. J Exp Med. 2004;199:1651-8.
10. Bonnard M, Mirtsos C, Suzuki S, Graham K, Huang J, Ng M, Itie A, Wakeham A, Shahinian A, Henzel WJ, et al. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kappaB-dependent gene transcription. EMBO J. 2000;19:4976-85.
11. Larabi A, Devos JM, Ng SL, Nanao MH, Round A, Maniatis T, Panne D. Crystal structure and mechanism of activation of TANK-binding kinase 1. Cell Rep. 2013;3:734-46.
12. Ma X, Helgason E, Phung QT, Quan CL, Iyer RS, Lee MW, Bowman KK, Starovasnik MA, Dueber EC. Molecular basis of Tank-binding kinase 1 activation by transautophosphorylation. Proc Natl Acad Sci U S A. 2012;109:9378-83.
13. Li S, Wang L, Berman M, Kong YY, Dorf ME. Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity. 2011;35:426-40.
14. Tu D, Zhu Z, Zhou AY, Yun CH, Lee KE, Toms AV, Li Y, Dunn GP, Chan E, Thai T, et al. Structure and ubiquitination-dependent activation of TANK-binding kinase 1. Cell Rep. 2013;3:747-58.
15. Goncalves A, Burckstummer T, Dixit E, Scheicher R, Gorna MW, Karayel E, Sugar C, Stukalov A, Berg T, Kralovics R, et al. Functional dissection of the TBK1 molecular network. PLoS One. 2011;6:e23971.
16. Helgason E, Phung QT, Dueber EC. Recent insights into the complexity of Tank-binding kinase 1 signaling networks: the emerging role of cellular localization in the activation and substrate specificity of TBK1. FEBS Lett. 2013;587:1230-7.
17. Kachaner D, Genin P, Laplantine E, Weil R. Toward an integrative view of Optineurin functions. Cell Cycle. 2012;11:2808-18.
18. Alexia C, Poalas K, Carvalho G, Zemirli N, Dwyer J, Dubois SM, Hatchi EM, Cordeiro N, Smith SS, Castanier C, et al. The endoplasmic reticulum acts as a platform for ubiquitylated components of nuclear factor kappaB signaling. Sci Signal. 2013;6:ra79.
19. Castanier C, Zemirli N, Portier A, Garcin D, Bidere N, Vazquez A, Arnoult D. MAVS ubiquitination by the E3 ligase TRIM25 and degradation by the proteasome is involved in type I interferon production after activation of the antiviral RIG-I-like receptors. BMC Biol. 2012;10:44.
20. Hou F, Sun L, Zheng H, Skaug B, Jiang QX, Chen ZJ. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell. 2011;146:448-61.
21. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, Hiiragi A, Dermody TS, Fujita T, Akira S. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med. 2008;205:1601-10.
22. Barber GN. STING-dependent cytosolic DNA sensing pathways. Trends Immunol. 2014;35:88-93.
23. Kachaner D, Filipe J, Laplantine E, Bauch A, Bennett KL, Superti-Furga G, Israel A, Weil R. Plk1-dependent phosphorylation of optineurin provides a negative feedback mechanism for mitotic progression. Mol Cell. 2012;45:553-66.
24. Gleason CE, Ordureau A, Gourlay R, Arthur JS, Cohen P. Polyubiquitin binding to optineurin is required for optimal activation of TANK-binding kinase 1 and production of interferon beta. J Biol Chem. 2011;286:35663-74.
25. Heo JM, Ordureau A, Paulo JA, Rinehart J, Harper JW. The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol Cell. 2015;60:7-20.
26. Lazarou M, Sliter DA, Kane LA, Sarraf SA, Wang C, Burman JL, Sideris DP, Fogel AI, Youle RJ. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015;524:309-14.
27. Munitic I, Giardino Torchia ML, Meena NP, Zhu G, Li CC, Ashwell JD. Optineurin insufficiency impairs IRF3 but not NF-kappaB activation in immune cells. J Immunol. 2013;191:6231-40.
28. Slowicka K, Vereecke L, McGuire C, Sze M, Maelfait J, Kolpe A, Saelens X, Beyaert R, van Loo G. Optineurin deficiency in mice is associated with increased sensitivity to Salmonella but does not affect proinflammatory NF-kappaB signaling. Eur J Immunol. 2016;46(4):971-80.
29. Zhao T, Yang L, Sun Q, Arguello M, Ballard DW, Hiscott J, Lin R. The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways. Nat Immunol. 2007;8:592-600.
30. Castanier C, Arnoult D. Mitochondrial localization of viral proteins as a means to subvert host defense. Biochim Biophys Acta. 2011;1813:575-83.
31. Chauveau E, Doceul V, Lara E, Breard E, Sailleau C, Vidalain PO, Meurs EF, Dabo S, Schwartz-Cornil I, Zientara S, Vitour D. NS3 of bluetongue virus interferes with the induction of type I interferon. J Virol. 2013;87:8241-6.
32. Han Z, Harty RN. The NS3 protein of bluetongue virus exhibits viroporin-like properties. J Biol Chem. 2004;279:43092-7.
33. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, Schinzel AC, Sandy P, Meylan E, Scholl C, et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature. 2009;462:108-12.
34. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, Du F, Ren J, Wu YT, Grishin NV, Chen ZJ. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science. 2015;347:aaa2630.
35. Genin P, Cuvelier F, Lambin S, Corte-Real Filipe J, Autrusseau E, Laurent C, Laplantine E, Weil R. Optineurin regulates the interferon response in a cell cycle-dependent manner. PLoS Pathog. 2015;11:e1004877.
36. Mankouri J, Fragkoudis R, Richards KH, Wetherill LF, Harris M, Kohl A, Elliott RM, Macdonald A. Optineurin negatively regulates the induction of IFNbeta in response to RNA virus infection. PLoS Pathog. 2010;6:e1000778.
37. Obaid R, Wani SE, Azfer A, Hurd T, Jones R, Cohen P, Ralston SH, Albagha OM. Optineurin negatively regulates osteoclast differentiation by modulating NF-kappaB and interferon signaling: implications for Paget's disease. Cell Rep. 2015;13(6):1096-102.
38. Unterholzner L, Sumner RP, Baran M, Ren H, Mansur DS, Bourke NM, Randow F, Smith GL, Bowie AG. Vaccinia virus protein C6 is a virulence factor that binds TBK-1 adaptor proteins and inhibits activation of IRF3 and IRF7. PLoS Pathog. 2011;7:e1002247.
39. Alff PJ, Sen N, Gorbunova E, Gavrilovskaya IN, Mackow ER. The NY-1 hantavirus Gn cytoplasmic tail coprecipitates TRAF3 and inhibits cellular interferon responses by disrupting TBK1-TRAF3 complex formation. J Virol. 2008;82:9115-22.
40. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, Richter B, Korac J, Waidmann O, Choudhary C, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science. 2011;333:228-33.
41. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol. 2009;10:1065-72.
42. Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell. 2009;138:576-91.
43. Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F. Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol. 2005;169:285-95.
44. Meena NP, Zhu G, Mittelstadt PR, Giardino Torchia ML, Pourcelot M, Arnoult D, Ashwell JD, Munitic I. The TBK1-binding domain of optineurin promotes type I interferon responses. FEBS Lett. 2016;590:1498-508.
45. Fujita F, Taniguchi Y, Kato T, Narita Y, Furuya A, Ogawa T, Sakurai H, Joh T, Itoh M, Delhase M, et al. Identification of NAP1, a regulatory subunit of IkappaB kinase-related kinases that potentiates NF-kappaB signaling. Mol Cell Biol. 2003;23:7780-93.
46. Ryzhakov G, Randow F. SINTBAD, a novel component of innate antiviral immunity, shares a TBK1-binding domain with NAP1 and TANK. EMBO J. 2007;26:3180-90.
47. Zemirli N, Pourcelot M, Dogan N, Vazquez A, Arnoult D. The E3 ubiquitin ligase RNF121 is a positive regulator of NF-kB activation. Cell Commun Signal. 2014;12:72.