Regulation of antiviral innate immune signaling by stress-induced RNA granules

Journal of Biochemistry

Volumn 159, Issue 3, 2015, Pages 279-286

  Yoneyama, Mitsutoshi ^a   Jogi, Michihiko ^a   Onomoto, Koji ^a  

^a CHIBA UNIVERSITY   (Japan)

Author keywords

innate immunity; retinoic acid inducible gene I like receptor; RNA; stress response; viral infection

Indexed keywords

POLYUBIQUITIN; PROTEIN; RETINOIC ACID INDUCIBLE GENE I LIKE RECEPTOR; RNA; UNCLASSIFIED DRUG; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; DHX58 PROTEIN, HUMAN; IFIH1 PROTEIN, HUMAN; INTERFERON INDUCED HELICASE C DOMAIN CONTAINING PROTEIN 1; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; RIBONUCLEOPROTEIN; RNA HELICASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VIRUS RNA; VISA PROTEIN, HUMAN;

ARTICLE; CELL GRANULE; ENZYME ACTIVATION; HUMAN; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; OLIGOMERIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRESS GRANULE; VIRUS IMMUNITY; ANIMAL; DNA VIRUS INFECTION; IMMUNOLOGY; METABOLISM; MOUSE; PHYSIOLOGICAL STRESS; RNA VIRUS INFECTION; VIROLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CYTOPLASMIC GRANULES; DEAD BOX PROTEIN 58; DEAD-BOX RNA HELICASES; DNA VIRUS INFECTIONS; HUMANS; IMMUNITY, INNATE; INTERFERON-INDUCED HELICASE, IFIH1; MICE; POLYUBIQUITIN; RECEPTORS, PATTERN RECOGNITION; RIBONUCLEOPROTEINS; RNA HELICASES; RNA VIRUS INFECTIONS; RNA, VIRAL; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84960488510     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvv122     Document Type: Article

References (81)

1. Yoneyama, M. and Fujita, T. (2010) Recognition of viral nucleic acids in innate immunity. Rev. Med. Virol. 20, 4-22
2. Lazear, H.M., Nice, T.J., and Diamond, M.S. (2015) Interferon-λ: immune functions at barrier surfaces and beyond. Immunity 43, 15-28
3. Schneider, W.M., Chevillotte, M.D., and Rice, C.M. (2014) Interferon-stimulated genes: a complex web of host defenses. Annu. Rev. Immunol. 32, 513-545
4. González-Navajas, J.M., Lee, J., David, M., and Raz, E. (2012) Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 12, 125-135
5. Goubau, D., Deddouche, S., and Reis e Sousa, C. (2013) Cytosolic sensing of viruses. Immunity 38, 855-869
6. Barber, G.N. (2014) STING-dependent cytosolic DNA sensing pathways. Trends Immunol. 35, 88-93
7. Cai, X., Chiu, Y.-H., and Chen, Z.J. (2014) The cGAScGAMP- STING pathway of cytosolic DNA sensing and signaling. Mol. Cell 54, 289-296
8. Dempsey, A. and Bowie, A.G. (2015) Innate immune recognition of DNA- A recent history. Virology 479-480, 146-152
9. Liu, S., Cai, X., Wu, J., Cong, Q., Chen, X., Li, T., Du, F., Ren, J., Wu, Y.-T., Grishin, N.V., and Chen, S.J. (2015) Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 347, aaa2630-1-14. http://www.ncbi.nlm. nih.gov/pubmed/25636800
10. Odendall, C., Dixit, E., Stavru, F., Bierne, H., Franz, K.M., Durbin, A.F., Boulant, S., Gehrke, L., Cossart, P., and Kagan, J.C. (2014) Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 15, 717-726
11. 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
12. Kowalinski, E., Lunardi, T., McCarthy, A.A., Louber, J., Brunel, J., Grigorov, B., Gerlier, D., and Cusack, S. (2011) Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 147, 423-435
13. Wies, E., Wang, M.K., Maharaj, N.P., Chen, K., Zhou, S., Finberg, R.W., and Gack, M.U. (2013) Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 38, 437-449
14. Funabiki, M., Kato, H., Miyachi, Y., Toki, H., Motegi, H., Inoue, M., Minowa, O., Yoshida, A., Deguchi, K., Sato, H., Ito, S., Shiroishi, T., Takeyasu, K., Noda, T., and Fujita, T. (2014) Autoimmune disorders associated with gain of function of the intracellular sensor MDA5. Immunity 40, 199-212
15. Oda, H., Nakagawa, K., Abe, J., Awaya, T., Funabiki, M., Hijikata, A., Nishikomori, R., Funatsuka, M., Ohshima, Y., Sugawara, Y., Yasumi, T., Kato, H., Shirai, T., Ohara, O., Fujita, T., and Heike, T. (2014) Aicardi-Goutie'res syndrome is caused by IFIH1 mutations. Am. J. Hum. Genet. 95, 121-125
16. Rice, G.I., del Toro Duany, Y., Jenkinson, E.M., Forte, G.M.A., Anderson, B.H., Ariaudo, G., Bader-Meunier, B., Baildam, E.M., Battini, R., Beresford, M.W., Casarano, M., Chouchane, M., Cimaz, R., Collins, A.E., Cordeiro, N.J.V., Dale, R.C., Davidson, J.E., De Waele, L., Desguerre, I., Faivre, L., Fazzi, E., Isidor, B., Lagae, L., Latchman, A.R., Lebon, P., Li, C., Livingston, J.H., Lourenço, C.M., Mancardi, M.M., Masurel-Paulet, A., McInnes, I.B., Menezes, M.P., Mignot, C., O'Sullivan, J., Orcesi, S., Picco, P.P., Riva, E., Robinson, R.A., Rodriguez, D., Salvatici, E., Scott, C., Szybowska, M., Tolmie, J.L., Vanderver, A., Vanhulle, C., Vieira, J.P., Webb, K., Whitney, R.N., Williams, S.G., Wolfe, L.A., Zuberi, S.M., Hur, S., and Crow, Y.J. (2014) Gain-offunction mutations in IFIH1 cause a spectrum of human disease phenotypes associated with upregulated type I interferon signaling. Nat. Genet. 46, 503-509
17. Rutsch, F., MacDougall, M., Lu, C., Buers, I., Mamaeva, O., Nitschke, Y., Rice, G.I., Erlandsen, H., Kehl, H.G., Thiele, H., Nürnberg, P., Höhne, W., Crow, Y.J., Feigenbaum, A., and Hennekam, R.C. (2015) A specific IFIH1 gain-of-function mutation causes Singleton-Merten syndrome. Am. J. Hum. Genet. 96, 275-282
18. Jang, M.-A., Kim, E.K., Now, H., Nguyen, N.T.H., Kim, W.-J., Yoo, J.-Y., Lee, J., Jeong, Y.-M., Kim, C.-H., Kim, O.-H., Sohn, S., Nam, S.-H., Hong, Y., Lee, Y.S., Chang, S.-A., Jang, S.Y., Kim, J.-W., Lee, M.-S., Lim, S.Y., Sung, K.-S., Park, K.-T., Kim, B.J., Lee, J.-H., Kim, D.-K., Kee, C., and Ki, C.-S. (2015) REPOR TMutations in DDX58, which encodes RIG-I, cause atypical Singleton-Merten syndrome. Am. J. Hum. Genet. 96, 266-274
19. Jiang, F., Ramanathan, A., Miller, M.T., Tang, G.-Q., Gale, M., Patel, S.S., and Marcotrigiano, J. (2011) Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 479, 423-427
20. Luo, D., Ding, S.C., Vela, A., Kohlway, A., Lindenbach, B.D., and Pyle, A.M. (2011) Structural insights into RNA recognition by RIG-I. Cell 147, 409-422
21. Wu, B., Peisley, A., Richards, C., Yao, H., Zeng, X., Lin, C., Chu, F., Walz, T., and Hur, S. (2013) Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 152, 276-289
22. Luo, D., Kohlway, A., Vela, A., and Pyle, A.M. (2012) Visualizing the determinants of viral RNA recognition by innate immune sensor RIG-I. Structure 20, 1983-1988
23. Yao, H., Dittmann, M., Peisley, A., Hoffmann, H.-H., Gilmore, R.H., Schmidt, T., Schmid-Burgk, J.L., Hornung, V., Rice, C.M., and Hur, S. (2015) ATPdependent effector-like functions of RIG-I-like receptors. Mol. Cell 58, 541-548
24. Sato, S., Li, K., Kameyama, T., Hayashi, T., Ishida, Y., Murakami, S., Watanabe, T., Iijima, S., Sakurai, Y., Watashi, K., Tsutsumi, S., Sato, Y., Akita, H., Wakita, T., Rice, C.M., Hrashima, H., Kohara, M., Tanaka, Y., and Takaoka, A. (2015) The RNA sensor RIG-I dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity 42, 123-132
25. Yoneyama, M., Kikuchi, M., Matsumoto, K., Imaizumi, T., Miyagishi, M., Taira, K., Foy, E., Loo, Y.-M., Gale, M., Akira, S., Yonehara, S., Kato, A., and Fujita, T. (2005) Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175, 2851-2858
26. 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
27. Venkataraman, T., Valdes, M., Elsby, R., Kakuta, S., Caceres, G., Saijo, S., Iwakura, Y., and Barber, G.N. (2007) Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 178, 6444-6455
28. Bruns, A.M., Bruns, A.M., Leser, G.P., Leser, G.P., Lamb, R.A., Lamb, R.A., Horvath, C.M., and Horvath, C.M. (2014) The innate immune sensor LGP2 activates antiviral signaling by regulating MDA5-RNA interaction and filament assembly. Mol. Cell 55, 771-781
29. Malur, M., Gale, M., and Krug, R.M. (2012) LGP2 downregulates interferon production during infection with seasonal human influenza A viruses that activate interferon regulatory factor 3. J. Virol. 86, 10733-10738
30. Schlee, M. (2013) Master sensors of pathogenic RNA - RIG-I like receptors. Immunobiology 218, 1322-1335
31. Goubau, D., Schlee, M., Deddouche, S., Pruijssers, A.J., Zillinger, T., Goldeck, M., Schuberth, C., Van der Veen, A.G., Fujimura, T., Rehwinkel, J., Iskarpatyoti, J.A., Barchet, W., Ludwig, J., Dermody, T.S., Hartmann, G., and Reis e Sousa, C. (2014) Antiviral immunity via RIG-I-mediated recognition of RNA bearing 50-diphosphates. Nature 514, 372-375
32. Schnell, G., Loo, Y.-M., Marcotrigiano, J., and Gale, M. (2012) Uridine composition of the poly-U/UC tract of HCV RNA defines non-self recognition by RIG-I. PLoS Pathog. 8, e1002839
33. Schuberth-Wagner, C., Ludwig, J., Bruder, A.K., Herzner, A.M., Zillinger, T., Goldeck, M., Schmidt, T., Schmid-Burgk, J.L., Kerber, R., Wolter, S., Stümpel, J.P., Roth, A., Bartok, E., Drosten, C., Coch, C., Hornung, V., Barchet, W., Kümmerer, B.M., Hartmann, G., and Schlee, M. (2015) A conserved histidine in the RNA sensor RIG-I controls immune tolerance to N1-2'O-Methylated self RNA. Immunity 43, 41-51
34. 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
35. Kato, H., Takeuchi, O., Mikamo-Satoh, E., Hirai, R., Kawai, T., Matsushita, K., Hiiragi, A., Dermody, T.S., Fujita, T., and 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
36. Takahasi, K., Yoneyama, M., Nishihori, T., Nishihori, T., Hirai, R., Hirai, R., Kumeta, H., Kumeta, H., Narita, R., Gale, M., Inagaki, F., and Fujita, T. (2008) Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 29, 428-440
37. Wang, Y., Ludwig, J., Schuberth, C., Goldeck, M., Schlee, M., Li, H., Juranek, S., Sheng, G., Micura, R., Tuschl, T., Hartmann, G., and Patel, D.J. (2010) Structural and functional insights into 50-ppp RNA pattern recognition by the innate immune receptor RIG-I. Nat. Struct. Mol. Biol. 17, 781-787
38. Lu, C., Xu, H., Ranjith-Kumar, C.T., Brooks, M.T., Hou, T.Y., Hu, F., Herr, A.B., Strong, R.K., Kao, C.C., and Li, P. (2010) The structural basis of 50triphosphate double-stranded RNA recognition by RIG-I Cterminal domain. Structure 18, 1032-1043
39. Lu, C., Ranjith-Kumar, C.T., Hao, L., Kao, C.C., and Li, P. (2011) Crystal structure of RIG-I C-terminal domain bound to blunt-ended double-strand RNA without 50 triphosphate. Nucleic Acids Res. 39, 1565-1575
40. Peisley, A., Wu, B., Yao, H., Walz, T., and Hur, S. (2013) RIG-I forms signaling-competent filaments in an ATP-dependent, ubiquitin-independent manner. Mol. Cell 51, 573-583
41. Patel, J.R., Jain, A., Chou, Y.-Y., Baum, A., Ha, T., and García-Sastre, A. (2013) ATPase-driven oligomerization of RIG-I on RNA allows optimal activation of type-I interferon. EMBO Rep. 14, 780-787
42. 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
43. Peisley, A., Wu, B., Xu, H., Chen, Z.J., and Hur, S. (2014) Structural basis for ubiquitin-mediated antiviral signal activation by RIG-I. Nature 509, 110-114
44. Takahasi, K., Kumeta, H., Tsuduki, N., Narita, R., Shigemoto, T., Hirai, R., Yoneyama, M., Horiuchi, M., Ogura, K., Fujita, T., and Inagaki, F. (2009) Solution structures of cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: identification of the RNA recognition loop in RIG-I-like receptors. J. Biol. Chem. 284, 17465-17474
45. Peisley, A., Lin, C., Wu, B., Orme-Johnson, M., Liu, M., Walz, T., and Hur, S. (2011) Cooperative assembly and dynamic disassembly of MDA5 filaments for viral dsRNA recognition. Proc. Natl. Acad. Sci. USA 108, 21010-21015
46. Peisley, A., Jo, M.H., Lin, C., Wu, B., Orme-Johnson, M., Walz, T., Hohng, S., and Hur, S. (2012) Kinetic mechanism for viral dsRNA length discrimination by MDA5 filaments. Proc. Natl. Acad. Sci. USA 109, E3340-E3349
47. del Toro Duany, Y., Wu, B., and Hur, S. (2015) MDA5 - filament, dynamics and disease. Curr. Opin. Virol. 12, 20-25
48. Hou, F., Sun, L., Zheng, H., Skaug, B., Jiang, Q.-X., and Chen, Z.J. (2011) MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146, 448-461
49. Xu, H., He, X., Zheng, H., Huang, L.J., Hou, F., Yu, Z., de la Cruz, M.J., Borkowski, B., Zhang, X., Chen, Z.J., and Jiang, Q.X. (2014) Structural basis for the prion-like MAVS filaments in antiviral innate immunity. eLife 3, e01489
50. Wu, B., Peisley, A., Tetrault, D., Li, Z., Egelman, E.H., Magor, K.E., Walz, T., Penczek, P.A., and Hur, S. (2014) Molecular imprinting as a signal-activation mechanism of the viral RNA sensor RIG-I. Mol. Cell 55, 511-523
51. Wu, B. and Hur, S. (2015) How RIG-I like receptors activate MAVS. Curr. Opin. Virol. 12, 91-98
52. Takamatsu, S., Onoguchi, K., Onomoto, K., Narita, R., Takahasi, K., Ishidate, F., Fujiwara, T.K., Yoneyama, M., Kato, H., and Fujita, T. (2013) Functional characterization of domains of IPS-1 using an inducible oligomerization system. PLoS One 8, e53578
53. Davis, M.E. and Gack, M.U. (2015) Ubiquitination in the antiviral immune response. Virology 479-480, 52-65
54. 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
55. 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
56. Jiang, X., Jiang, X., Kinch, L.N., Kinch, L.N., Brautigam, C.A., Brautigam, C.A., Chen, X., Chen, X., Du, F., Grishin, N.V., and Chen, Z.J. (2012) Ubiquitininduced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36, 959-973
57. Oshiumi, H., Miyashita, M., Matsumoto, M., and Seya, T. (2013) A distinct role of Riplet-mediated K63-Linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog. 9, e1003533
58. Kuniyoshi, K., Takeuchi, O., Pandey, S., Satoh, T., Iwasaki, H., Akira, S., and Kawai, T. (2014) Pivotal role of RNA-binding E3 ubiquitin ligase MEX3C in RIG-I-mediated antiviral innate immunity. Proc. Natl. Acad. Sci. USA 111, 5646-5651
59. Yan, J., Li, Q., Mao, A.-P., Hu, M.-M., and Shu, H.-B. (2014) TRIM4 modulates type I interferon induction and cellular antiviral response by targeting RIG-I for K63- linked ubiquitination. J. Mol. Cell Biol. 6, 154-163
60. Versteeg, G.A., Rajsbaum, R., Sánchez-Aparicio, M.T., Maestre, A.M., Valdiviezo, J., Shi, M., Inn, K.-S., Fernandez-Sesma, A., Jung, J., and García-Sastre, A. (2013) The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune patternrecognition receptors. Immunity 38, 384-398
61. Narayan, K., Waggoner, L., Pham, S.T., Hendricks, G.L., Waggoner, S.N., Conlon, J., Wang, J.P., Fitzgerald, K.A., and Kang, J. (2014) TRIM13 is a negative regulator of MDA5-mediated type I interferon production. J. Virol. 88, 10748-10757
62. Liu, S., Chen, J., Cai, X., Wu, J., Chen, X., Wu, Y.-T., Sun, L., and Chen, Z.J. (2013) MAVS recruits multiple ubiquitin E3 ligases to activate antiviral signaling cascades. eLife 2, e00785
63. Cui, J., Song, Y., Li, Y., Zhu, Q., Tan, P., Qin, Y., Wang, H.Y., and Wang, R.-F. (2014) USP3 inhibits type I interferon signaling by deubiquitinating RIG-Ilike receptors. Cell Res. 24, 400-416
64. Fan, Y., Mao, R., Yu, Y., Liu, S., Shi, Z., Cheng, J., Zhang, H., An, L., Zhao, Y., Xu, X., Chen, Z., Kogiso, M., Zhang, D., Zhang, H., Zhang, P., Jung, J.U., Li, X., Xu, G., and Yang, J. (2014) USP21 negatively regulates antiviral response by acting as a RIG-I deubiquitinase. J. Exp. Med. 211, 313-328
65. Wang, L., Zhao, W., Zhang, M., Wang, P., Zhao, K., Zhao, X., Yang, S., and Gao, C. (2013) USP4 positively regulates RIG-I-mediated antiviral response through deubiquitination and stabilization of RIG-I. J. Virol. 87, 4507-4515
66. Pauli, E.-K., Chan, Y.K., Davis, M.E., Gableske, S., Wang, M.K., Feister, K.F., and Gack, M.U. (2014) The ubiquitin-specific protease USP15 promotes RIG-Imediated antiviral signaling by deubiquitylating TRIM25. Sci. Signal. 7, ra3-1-11. http://www.ncbi.nlm. nih.gov/pubmed/?term=PMC4008495
67. Onomoto, K., Yoneyama, M., Fung, G., Kato, H., and Fujita, T. (2014) Antiviral innate immunity and stress granule responses. Trends Immunol. 35, 420-428
68. Onomoto, K., Jogi, M., Yoo, J.-S., Narita, R., Morimoto, S., Takemura, A., Sambhara, S., Kawaguchi, A., Osari, S., Nagata, K., Matsumiya, T., Namiki, H., Yoneyama, M., and Fujita, T. (2012) Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS One 7, e43031
69. Anderson, P. and Kedersha, N. (2008) Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141-150
70. White, J.P. and Lloyd, R.E. (2012) Regulation of stress granules in virus systems. Trends Microbiol. 20, 175-183
71. Berlanga, J.J., Ventoso, I., Harding, H.P., Deng, J., Ron, D., Sonenberg, N., Carrasco, L., and de Haro, C. (2006) Antiviral effect of the mammalian translation initiation factor 2alpha kinase GCN2 against RNA viruses. EMBO J. 25, 1730-1740
72. Yoo, J.-S., Takahasi, K., Ng, C.S., Ouda, R., Onomoto, K., Yoneyama, M., Lai, J.C., Lattmann, S., Nagamine, Y., Matsui, T., Iwabuchi, K., Kato, H., and Fujita, T. (2014) DHX36 enhances RIG-I signaling by facilitating PKR-mediated antiviral stress granule formation. PLoS Pathog. 10, e1004012
73. Narita, R., Takahasi, K., Murakami, E., Hirano, E., Yamamoto, S.P., Yoneyama, M., Kato, H., and Fujita, T. (2014) A novel function of human pumilio proteins in cytoplasmic sensing of viral infection. PLoS Pathog. 10, e1004417
74. Langereis, M.A., Feng, Q., and van Kuppeveld, F.J. (2013) MDA5 localizes to stress granules, but this localization is not required for the induction of type I interferon. J. Virol. 87, 6314-6325
75. White, J.P., Cardenas, A.M., Marissen, W.E., and Lloyd, R.E. (2007) Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2, 295-305
76. Fung, G., Ng, C.S., Zhang, J., Shi, J., Wong, J., Piesik, P., Han, L., Chu, F., Jagdeo, J., Jan, E., Fujita, T., and Luo, H. (2013) Production of a dominant-negative fragment due to G3BP1 cleavage contributes to the disruption of mitochondria-associated protective stress granules during CVB3 infection. PLoS One 8, e79546
77. Ng, C.S., Jogi, M., Yoo, J.-S., Onomoto, K., Koike, S., Iwasaki, T., Yoneyama, M., Kato, H., and Fujita, T. (2013) Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. J. Virol. 87, 9511-9522
78. Ariumi, Y., Kuroki, M., Kushima, Y., Osugi, K., Hijikata, M., Maki, M., Ikeda, M., and Kato, N. (2011) Hepatitis C virus hijacks P-body and stress granule components around lipid droplets. J. Virol. 85, 6882-6892
79. Garaigorta, U., Heim, M.H., Boyd, B., Wieland, S., and Chisari, F.V. (2012) Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress. J. Virol. 86, 11043-11056
80. Pène, V., Li, Q., Sodroski, C., Hsu, C.-S., and Liang, T.J. (2015) Dynamic interaction of stress granules, DDX3X, and IKK-a mediates multiple functions in hepatitis C virus infection. J. Virol. 89, 5462-5477
81. Yoneyama, M., Onomoto, K., Jogi, M., Akaboshi, T., and Fujita, T. (2015) Viral RNA detection by RIG-I-like receptors. Curr. Opin. Immunol. 32, 48-53