LRRC25 inhibits type I IFN signaling by targeting ISG15-associated RIG-I for autophagic degradation

EMBO Journal

Volumn 37, Issue 3, 2018, Pages 351-366

  Du, Yang ^a,b   Duan, Tianhao ^a,b   Feng, Yanchun ^a,b   Liu, Qingxiang ^b   Lin, Meng ^b   Cui, Jun ^a,b   Wang, Rong Fu ^c,d,e  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

ISG15; LRRC25; p62; RIG I; selective autophagy

Indexed keywords

ANTIVIRUS AGENT; CYTOKINE; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON STIMULATED GENE 15; LEUCINE RICH REPEAT CONTAINING PROTEIN 25; PATTERN RECOGNITION RECEPTOR; REGULATOR PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RIG I LIKE RECEPTOR; SEQUESTOSOME 1; UNCLASSIFIED DRUG; DDX58 PROTEIN, HUMAN; ISG15 PROTEIN, HUMAN; LRRC25 PROTEIN, HUMAN; MEMBRANE PROTEIN; P62 PROTEIN, HUMAN; PROTEIN BINDING; RNA BINDING PROTEIN; SMALL INTERFERING RNA; UBIQUITIN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; HUMAN; HUMAN CELL; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA VIRUS; SIGNAL TRANSDUCTION; VIRUS INFECTION; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; CV-1 CELL LINE; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; RNA INTERFERENCE; VESICULAR STOMATITIS INDIANA VIRUS;

ANIMALS; AUTOPHAGY; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOKINES; DEAD BOX PROTEIN 58; HEK293 CELLS; HUMANS; INTERFERON TYPE I; MEMBRANE PROTEINS; PROTEIN BINDING; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; UBIQUITINS; VESICULAR STOMATITIS INDIANA VIRUS;

EID: 85039558340     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201796781     Document Type: Article

References (47)

1. Allen IC, Moore CB, Schneider M, Lei Y, Davis BK, Scull MA, Gris D, Roney KE, Zimmermann AG, Bowzard JB, Ranjan P, Monroe KM, Pickles RJ, Sambhara S, Ting JP (2011) NLRX1 protein attenuates inflammatory responses to infection by interfering with the RIG-I-MAVS and TRAF6-NF-kappaB signaling pathways. Immunity 34: 854–865
2. 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
3. Arsov I, Adebayo A, Kucerova-Levisohn M, Haye J, MacNeil M, PapavasiliouFN, Yue Z, Ortiz BD (2011) A role for autophagic protein beclin 1 early in lymphocyte development. J Immunol 186: 2201–2209
4. Chen W, Han C, Xie B, Hu X, Yu Q, Shi L, Wang Q, Li D, Wang J, Zheng P, Liu Y, Cao X (2013) Induction of Siglec-G by RNA viruses inhibits the innate immune response by promoting RIG-I degradation. Cell 152: 467–478
5. Cui J, Zhu L, Xia X, Wang HY, Legras X, Hong J, Ji J, Shen P, Zheng S, Chen ZJ, Wang RF (2010) NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways. Cell 141: 483–496
6. Cui J, Li Y, Zhu L, Liu D, Songyang Z, Wang HY, Wang RF (2012) NLRP4 negatively regulates type I interferon signaling by targeting the kinase TBK1 for degradation via the ubiquitin ligase DTX4. Nat Immunol 13: 387–395
7. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, Kreymborg K, Altenberend F, Brandenburg J, Kalbacher H, Brock R, Driessen C, Rammensee HG, Stevanovic S (2005) Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci USA 102: 7922–7927
8. He S, Zhao J, Song S, He X, Minassian A, Zhou Y, Zhang J, Brulois K, Wang Y, Cabo J, Zandi E, Liang C, Jung JU, Zhang X, Feng P (2015) Viral pseudo-enzymes activate RIG-I via deamidation to evade cytokine production. Mol Cell 58: 134–146
9. Hermann M, Bogunovic D (2017) ISG15. In sickness and in health. Trends Immunol 38: 79–93
10. Inohara N, Chamaillard M, McDonald C, Nunez G (2005) NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu Rev Biochem 74: 355–383
11. Jin S, Tian S, Chen Y, Zhang C, Xie W, Xia X, Cui J, Wang RF (2016) USP19 modulates autophagy and antiviral immune responses by deubiquitinating Beclin-1. EMBO J 35: 866–880
12. Jounai N, Takeshita F, Kobiyama K, Sawano A, Miyawaki A, Xin KQ, Ishii KJ, Kawai T, Akira S, Suzuki K, Okuda K (2007) The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci USA 104: 14050–14055
13. 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: 1601–1610
14. 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
15. Kim MJ, Hwang SY, Imaizumi T, Yoo JY (2008) Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J Virol 82: 1474–1483
16. Kuma A, Matsui M, Mizushima N (2007) LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: caution in the interpretation of LC3 localization. Autophagy 3: 323–328
17. Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A (2007) Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315: 1398–1401
18. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T, Osiak A, Levine B, Schmidt RE, Garcia-Sastre A, Leib DA, Pekosz A, Knobeloch KP, Horak I, Virgin HW IV (2007) IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc Natl Acad Sci USA 104: 1371–1376
19. Liang Q, Seo GJ, Choi YJ, Kwak MJ, Ge J, Rodgers MA, Shi M, Leslie BJ, Hopfner KP, Ha T, Oh BH, Jung JU (2014) Crosstalk between the cGAS DNA sensor and Beclin-1 autophagy protein shapes innate antimicrobial immune responses. Cell Host Microbe 15: 228–238
20. Lin M, Zhao Z, Yang Z, Meng Q, Tan P, Xie W, Qin Y, Wang RF, Cui J (2016) USP38 inhibits type I interferon signaling by editing TBK1 ubiquitination through NLRP4 signalosome. Mol Cell 64: 267–281
21. Loo YM, Gale M Jr (2011) Immune signaling by RIG-I-like receptors. Immunity 34: 680–692
22. Maharaj NP, Wies E, Stoll A, Gack MU (2012) Conventional protein kinase C-α (PKC-α) and PKC-β negatively regulate RIG-I antiviral signal transduction. J Virol 86: 1358–1371
23. Matsumoto G, Shimogori T, Hattori N, Nukina N (2015) TBK1 controls autophagosomal engulfment of polyubiquitinated mitochondria through p62/SQSTM1 phosphorylation. Hum Mol Genet 24: 4429–4442
24. 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
25. Morales DJ, Lenschow DJ (2013) The antiviral activities of ISG15. J Mol Biol 425: 4995–5008
26. Ng AC, Eisenberg JM, Heath RJ, Huett A, Robinson CM, Nau GJ, Xavier RJ (2011) Human leucine-rich repeat proteins: a genome-wide bioinformatic categorization and functional analysis in innate immunity. Proc Natl Acad Sci USA 108(Suppl 1): 4631–4638
27. O'Neill LAJ (2006) How Toll-like receptors signal: what we know and what we don't know. Curr Opin Immunol 18: 3–9
28. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131–24145
29. 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: 669–682
30. Shapira SD, Gat-Viks I, Shum BO, Dricot A, de Grace MM, Wu L, Gupta PB, Hao T, Silver SJ, Root DE, Hill DE, Regev A, Hacohen N (2009) A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 139: 1255–1267
31. Shin DM, Jeon BY, Lee HM, Jin HS, Yuk JM, Song CH, Lee SH, Lee ZW, Cho SN, Kim JM, Friedman RL, Jo EK (2010) Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog 6: e1001230
32. Skaug B, Chen ZJ (2010) Emerging role of ISG15 in antiviral immunity. Cell 143: 187–190
33. Speer SD, Li Z, Buta S, Payelle-Brogard B, Qian L, Vigant F, Rubino E, Gardner TJ, Wedeking T, Hermann M, Duehr J, Sanal O, Tezcan I, Mansouri N, Tabarsi P, Mansouri D, Francois-Newton V, Daussy CF, Rodriguez MR, Lenschow DJ et al (2016) ISG15 deficiency and increased viral resistance in humans but not mice. Nat Commun 7: 11496
34. Starr TK, Jameson SC, Hogquist KA (2003) Positive and negative selection of T cells. Annu Rev Immunol 21: 139–176
35. Stolz A, Ernst A, Dikic I (2014) Cargo recognition and trafficking in selective autophagy. Nat Cell Biol 16: 495–501
36. 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
37. Sun L, Wu J, Du F, Chen X, Chen ZJ (2013) Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339: 786–791
38. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, Ban T, Lu Y, Miyagishi M, Kodama T, Honda K, Ohba Y, Taniguchi T (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448: 501–505
39. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140: 805–820
40. Tang Y, Zhong G, Zhu L, Liu X, Shan Y, Feng H, Bu Z, Chen H, Wang C (2010) Herc5 attenuates influenza A virus by catalyzing ISGylation of viral NS1 protein. J Immunol 184: 5777–5790
41. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois CM, Jin T, Latz E, Xiao TS, Fitzgerald KA, Paludan SR, Bowie AG (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11: 997–1004
42. Xia X, Cui J, Wang HY, Zhu L, Matsueda S, Wang Q, Yang X, Hong J, Songyang Z, Chen Z, Wang R-F (2011) NLRX1 negatively regulates TLR-induced NF-κB signaling by targeting TRAF6 and IKK. Immunity 34: 843–853
43. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727–740
44. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ (2011) The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12: 959–965
45. Zhang X, Bogunovic D, Payelle-Brogard B, Francois-Newton V, Speer SD, Yuan C, Volpi S, Li Z, Sanal O, Mansouri D, Tezcan I, Rice GI, Chen C, Mansouri N, Mahdaviani SA, Itan Y, Boisson B, Okada S, Zeng L, Wang X et al (2015) Human intracellular ISG15 prevents interferon-alpha/beta over-amplification and auto-inflammation. Nature 517: 89–93
46. Zhao C, Denison C, Huibregtse JM, Gygi S, Krug RM (2005) Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc Natl Acad Sci USA 102: 10200–10205
47. Zhao K, Zhang Q, Li X, Zhao D, Liu Y, Shen Q, Yang M, Wang C, Li N, Cao X (2016) Cytoplasmic STAT4 promotes antiviral type I IFN production by blocking CHIP-mediated degradation of RIG-I. J Immunol 196: 1209–1217