Ubiquitin-mediated modulation of the cytoplasmic viral RNA sensor RIG-I

Journal of Biochemistry

Volumn 151, Issue 1, 2012, Pages 5-11

  Oshiumi, Hiroyuki ^a   Matsumoto, Misako ^a   Seya, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

RIG I; type I interferon; ubiquitin; virus

Indexed keywords

POLYUBIQUITIN; PROTEASOME; RETINOIC ACID INDUCIBLE PROTEIN I; UBIQUITIN; VIRUS RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; UBIQUITINATION;

ALTERNATIVE SPLICING; CYTOPLASM; DEAD-BOX RNA HELICASES; HUMANS; MACROPHAGES; MODELS, BIOLOGICAL; RNA, VIRAL; TRANSCRIPTION FACTORS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84855218318     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvr111     Document Type: Article

References (62)

1. Takeuchi, O. and Akira, S. (2010) Pattern recognition receptors and inflammation. Cell 140, 805-820
2. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., Uematsu, S., Jung, A., Kawai, T., Ishii, K.J., Yamaguchi, O., Otsu, K., Tsujimura, T., Koh, C. S., Reis e Sousa, C., Matsuura, Y., Fujita, T., and Akira, S. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105
3. Satoh, T., Kato, H., Kumagai, Y., Yoneyama, M., Sato, S., Matsushita, K., Tsujimura, T., Fujita, T., Akira, S., and Takeuchi, O. (2010) LGP2 is a positive regulator of RIG-I-and MDA5-mediated antiviral responses. Proc. Natl Acad. Sci. USA 107, 1512-1517
4. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K., Akira, S., and 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)
5. Xu, L.G., Wang, Y.Y., Han, K.J., Li, L.Y., Zhai, Z., and Shu, H.B. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19, 727-740 (Pubitemid 41316668)
6. Seth, R.B., Sun, L., Ea, C.K., and Chen, Z.J. (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NFkappaB and IRF 3. Cell 122, 669-682 (Pubitemid 41242633)
7. Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R., and 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)
8. Kawai, T., Takahashi, K., Sato, S., Coban, C., Kumar, H., Kato, H., Ishii, K.J., Takeuchi, O., and Akira, S. (2005) IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat. Immunol. 6, 981-988 (Pubitemid 41486182)
9. Saito, T., Hirai, R., Loo, Y.M., Owen, D., Johnson, C.L., Sinha, S.C., Akira, S., Fujita, T., and 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)
10. Schmidt, A., Schwerd, T., Hamm, W., Hellmuth, J.C., Cui, S., Wenzel, M., Hoffmann, F.S., Michallet, M.C., Besch, R., Hopfner, K.P., Endres, S., and Rothenfusser, S. (2009) 50-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc. Natl. Acad. Sci. USA 106, 12067-12072
11. Myong, S., Cui, S., Cornish, P.V., Kirchhofer, A., Gack, M.U., Jung, J.U., Hopfner, K.P., and Ha, T. (2009) Cytosolic viral sensor RIG-I is a 50-triphosphate-dependent translocase on double-stranded RNA. Science 323, 1070-1074
12. Pichlmair, A., Schulz, O., Tan, C.P., Naslund, T.I., Liljestrom, P., Weber, F., and Reis e Sousa, C. (2006) RIG-I-mediated antiviral responses to single-stranded RNA bearing 50-phosphates. Science 314, 997-1001 (Pubitemid 44749946)
13. Hornung, V., Ellegast, J., Kim, S., Brzozka, K., Jung, A., Kato, H., Poeck, H., Akira, S., Conzelmann, K.K., Schlee, M., Endres, S., and Hartmann, G. (2006) 50-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997
14. Zhong, B., Yang, Y., Li, S., Wang, Y.Y., Li, Y., Diao, F., Lei, C., He, X., Zhang, L., Tien, P., and Shu, H.B. (2008) The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29, 538-550
15. Ishikawa, H. and Barber, G.N. (2008) STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455, 674-678
16. Sun, Q., Sun, L., Liu, H.H., Chen, X., Seth, R.B., Forman, J., and Chen, Z.J. (2006) The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24, 633-642 (Pubitemid 43728147)
17. Kumar, H., Kawai, T., Kato, H., Sato, S., Takahashi, K., Coban, C., Yamamoto, M., Uematsu, S., Ishii, K.J., Takeuchi, O., and Akira, S. (2006) Essential role of IPS-1 in innate immune responses against RNA viruses. J. Exp. Med. 203, 1795-1803 (Pubitemid 44036284)
18. Ishikawa, H., Ma, Z., and Barber, G.N. (2009) STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792
19. Kato, H., Sato, S., Yoneyama, M., Yamamoto, M., Uematsu, S., Matsui, K., Tsujimura, T., Takeda, K., Fujita, T., Takeuchi, O., and Akira, S. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity 23, 19-28 (Pubitemid 41019654)
20. Diebold, S.S., Kaisho, T., Hemmi, H., Akira, S., and Reis e Sousa, C. (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303, 1529-1531 (Pubitemid 38314425)
21. Honda, K., Takaoka, A., and Taniguchi, T. (2006) Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25, 349-360 (Pubitemid 44354220)
22. Gack, M.U., Shin, Y.C., Joo, C.H., Urano, T., Liang, C., Sun, L., Takeuchi, O., Akira, S., Chen, Z., Inoue, S., and Jung, J.U. (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446, 916-920 (Pubitemid 46633167)
23. Urano, T., Saito, T., Tsukui, T., Fujita, M., Hosoi, T., Muramatsu, M., Ouchi, Y., and Inoue, S. (2002) Efp targets 14-3-3 sigma for proteolysis and promotes breast tumour growth. Nature 417, 871-875
24. Gack, M.U., Kirchhofer, A., Shin, Y.C., Inn, K.S., Liang, C., Cui, S., Myong, S., Ha, T., Hopfner, K.P., and Jung, J.U. (2008) Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc. Natl. Acad. Sci. USA 105, 16743-16748
25. Sumpter, R. Jr, Loo, Y.M., Foy, E., Li, K., Yoneyama, M., Fujita, T., Lemon, S.M., and 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)
26. Zeng, W., Sun, L., Jiang, X., Chen, X., Hou, F., Adhikari, A., Xu, M., and Chen, Z.J. (2010) Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141, 315-330
27. Poeck, H., Bscheider, M., Gross, O., Finger, K., Roth, S., Rebsamen, M., Hannesschlager, N., Schlee, M., Rothenfusser, S., Barchet, W., Kato, H., Akira, S., Inoue, S., Endres, S., Peschel, C., Hartmann, G., Hornung, V., and Ruland, J. (2010) Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat. Immunol. 11, 63-69
28. Yu, H.B. and Finlay, B.B. (2008) The caspase-1 inflammasome: a pilot of innate immune responses. Cell Host Microbe 4, 198-208
29. Oshiumi, H., Matsumoto, M., Hatakeyama, S., and Seya, T. (2009) Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J. Biol. Chem. 284, 807-817
30. Oshiumi, H., Miyashita, M., Inoue, N., Okabe, M., Matsumoto, M., and 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
31. Hu, J., Nistal-Villan, E., Voho, A., Ganee, A., Kumar, M., Ding, Y., Garcia-Sastre, A., and Wetmur, J.G. (2010) A common polymorphism in the caspase recruitment domain of RIG-I modifies the innate immune response of human dendritic cells. J. Immunol. 185, 424-432
32. Gao, D., Yang, Y.K., Wang, R.P., Zhou, X., Diao, F.C., Li, M.D., Zhai, Z.H., Jiang, Z.F., and Chen, D.Y. (2009) REUL is a novel E3 ubiquitin ligase and stimulator of retinoic-acid-inducible gene-I. PLoS One 4, e5760
33. Wang, Y., Zhang, H.X., Sun, Y.P., Liu, Z.X., Liu, X.S., Wang, L., Lu, S.Y., Kong, H., Liu, Q.L., Li, X.H., Lu, Z.Y., Chen, S.J., Chen, Z., Bao, S.S., Dai, W., and Wang, Z.G. (2007) Rig-I-/-mice develop colitis associated with downregulation of G alpha i2. Cell Res 17, 858-868 (Pubitemid 47585114)
34. Douglas, J., Cilliers, D., Coleman, K., Tatton-Brown, K., Barker, K., Bernhard, B., Burn, J., Huson, S., Josifova, D., Lacombe, D., Malik, M., Mansour, S., Reid, E., Cormier-Daire, V., Cole, T., and Rahman, N. (2007) Mutations in RNF135, a gene within the NF1 microdeletion region, cause phenotypic abnormalities including overgrowth. Nat. Genet. 39, 963-965 (Pubitemid 47185181)
35. Choi, M.K., Wang, Z., Ban, T., Yanai, H., Lu, Y., Koshiba, R., Nakaima, Y., Hangai, S., Savitsky, D., Nakasato, M., Negishi, H., Takeuchi, O., Honda, K., Akira, S., Tamura, T., and Taniguchi, T. (2009) A selective contribution of the RIG-I-like receptor pathway to type I interferon responses activated by cytosolic DNA. Proc. Natl. Acad. Sci. USA 106, 17870-17875
36. Chiu, Y.H., Macmillan, J.B., and Chen, Z.J. (2009) RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138, 576-591
37. Ablasser, A., Bauernfeind, F., Hartmann, G., Latz, E., Fitzgerald, K.A., and Hornung, V. (2009) RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 10, 1065-1072
38. Chase, A., Ernst, T., Fiebig, A., Collins, A., Grand, F., Erben, P., Reiter, A., Schreiber, S., and Cross, N.C. (2010) TFG, a target of chromosome translocations in lymphoma and soft tissue tumors, fuses to GPR128 in healthy individuals. Haematologica 95, 20-26
39. Suzuki, H., Fukunishi, Y., Kagawa, I., Saito, R., Oda, H., Endo, T., Kondo, S., Bono, H., Okazaki, Y., and Hayashizaki, Y. (2001) Protein-protein interaction panel using mouse full-length cDNAs. Genome Res. 11, 1758-1765 (Pubitemid 33040503)
40. Hernandez, L., Pinyol, M., Hernandez, S., Bea, S., Pulford, K., Rosenwald, A., Lamant, L., Falini, B., Ott, G., Mason, D.Y., Delsol, G., and Campo, E. (1999) TRK-fused gene (TFG) is a new partner of ALK in anaplastic large cell lymphoma producing two structurally different TFG-ALK translocations. Blood 94, 3265-3268 (Pubitemid 29512738)
41. Pasmant, E., Masliah-Planchon, J., Levy, P., Laurendeau, I., Ortonne, N., Parfait, B., Valeyrie-Allanore, L., Leroy, K., Wolkenstein, P., Vidaud, M., Vidaud, D., and Bieche, I. (2011) Identification of genes potentially involved in the increased risk of malignancy in NF1-microdeleted patients. Mol. Med. 17, 79-87
42. Zhao, H., Li, C.C., Pardo, J., Chu, P.C., Liao, C.X., Huang, J., Dong, J.G., Zhou, X., Huang, Q., Huang, B., Bennett, M. K., Molineaux, S.M., Lu, H., Daniel-Issakani, S., Payan, D.G., and Masuda, E.S. (2005) A novel E3 ubiquitin ligase TRAC-1 positively regulates T cell activation. J. Immunol. 174, 5288-5297 (Pubitemid 40593167)
43. Arimoto, K., Takahashi, H., Hishiki, T., Konishi, H., Fujita, T., and 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)
44. Arimoto, K., Konishi, H., and Shimotohno, K. (2008) UbcH8 regulates ubiquitin and ISG15 conjugation to RIG-I. Mol. Immunol. 45, 1078-1084 (Pubitemid 350016330)
45. Trompouki, E., Hatzivassiliou, E., Tsichritzis, T., Farmer, H., Ashworth, A., and Mosialos, G. (2003) CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 424, 793-796 (Pubitemid 37021710)
46. Kovalenko, A., Chable-Bessia, C., Cantarella, G., Israel, A., Wallach, D., and Courtois, G. (2003) The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 424, 801-805 (Pubitemid 37021712)
47. Brummelkamp, T.R., Nijman, S.M., Dirac, A.M., and Bernards, R. (2003) Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424, 797-801 (Pubitemid 37021711)
48. Massoumi, R., Chmielarska, K., Hennecke, K., Pfeifer, A., and Fassler, R. (2006) Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling. Cell 125, 665-677
49. Friedman, C.S., O'Donnell, M.A., Legarda-Addison, D., Ng, A., Cardenas, W.B., Yount, J.S., Moran, T.M., Basler, C.F., Komuro, A., Horvath, C.M., Xavier, R., and Ting, A.T. (2008) The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 9, 930-936
50. Kirisako, T., Kamei, K., Murata, S., Kato, M., Fukumoto, H., Kanie, M., Sano, S., Tokunaga, F., Tanaka, K., and Iwai, K. (2006) A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25, 4877-4887 (Pubitemid 44607032)
51. Inn, K.S., Gack, M.U., Tokunaga, F., Shi, M., Wong, L.Y., Iwai, K., and Jung, J.U. (2011) Linear ubiquitin assembly complex negatively regulates RIG-I-and TRIM25-mediated type I interferon induction. Mol. Cell 41, 354-365
52. Diebold, S.S., Montoya, M., Unger, H., Alexopoulou, L., Roy, P., Haswell, L.E., Al-Shamkhani, A., Flavell, R., Borrow, P., and Reis e Sousa, C. (2003) Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424, 324-328 (Pubitemid 36899375)
53. Garcia-Sastre, A., Egorov, A., Matassov, D., Brandt, S., Levy, D.E., Durbin, J.E., Palese, P., and Muster, T. (1998) Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252, 324-330 (Pubitemid 29013414)
54. Gack, M.U., Albrecht, R.A., Urano, T., Inn, K.S., Huang, I.C., Carnero, E., Farzan, M., Inoue, S., Jung, J.U., and Garcia-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
55. Zhao, C., Denison, C., Huibregtse, J.M., Gygi, S., and Krug, R.M. (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 (Pubitemid 41023349)
56. Knobeloch, K.P., Utermohlen, O., Kisser, A., Prinz, M., and Horak, I. (2005) Reexamination of the role of ubiquitin-like modifier ISG15 in the phenotype of UBP43-deficient mice. Mol. Cell Biol. 25, 11030-11034 (Pubitemid 41747144)
57. Sun, Z., Ren, H., Liu, Y., Teeling, J.L., and Gu, J. (2011) Phosphorylation of RIG-I by casein kinase II inhibits its antiviral response. J. Virol. 85, 1036-1047
58. Yanai, H., Ban, T., Wang, Z., Choi, M.K., Kawamura, T., Negishi, H., Nakasato, M., Lu, Y., Hangai, S., Koshiba, R., Savitsky, D., Ronfani, L., Akira, S., Bianchi, M. E., Honda, K., Tamura, T., Kodama, T., and Taniguchi, T. (2009) HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462, 99-103
59. Oshiumi, H., Sakai, K., Matsumoto, M., and Seya, T. (2010) DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-beta-inducing potential. Eur. J. Immunol. 40, 940-948
60. Soulat, D., Burckstummer, T.,Westermayer, S., Goncalves, A., Bauch, A., Stefanovic, A., Hantschel, O., Bennett, K.L., Decker, T., and Superti-Furga, G. (2008) The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. EMBO J. 27, 2135-2146
61. Schroder, M., Baran, M., and Bowie, A. G. (2008) Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J. 27, 2147-2157
62. Miyashita, M., Oshiumi, H., Matsumoto, M., and Seya, T. (2011) DDX60, a DExD/H box helicase, is a novel antiviral factor promoting RIG-I-like receptor-mediated signaling. Mol. Cell Biol. 31, 3802-3819