Links between recognition and degradation of cytoplasmic viral RNA in innate immune response

Reviews in Medical Virology

Volumn , Issue , 2016, Pages 90-101

  Oshiumi, Hiroyuki ^a   Mifsud, Edin J ^a   Daito, Takuji ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; SMALL CYTOPLASMIC RNA; VIRUS RNA; ZINC FINGER PROTEIN;

ENZYME ACTIVATION; ENZYME ACTIVITY; EXOSOME; INFLAMMATION; INNATE IMMUNITY; MOLECULAR RECOGNITION; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; REVIEW; RNA DEGRADATION;

EID: 84987806920     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.1865     Document Type: Review

References (112)

1. Loo YM, Gale M Jr. Immune signaling by RIG-I-like receptors. Immunity 2011; 34: 680–692.
2. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 2006; 25: 373–381.
3. Zhou A, Hassel BA, Silverman RH. Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell 1993; 72: 753–765.
4. Gao G, Guo X, Goff SP. Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 2002; 297: 1703–1706.
5. Guo X, Ma J, Sun J, Gao G. The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proceedings of the National Academy of Sciences of the United States of America 2007; 104: 151–156.
6. Houseley J, LaCava J, Tollervey D. RNA-quality control by the exosome. Nature Reviews Molecular Cell Biology 2006; 7: 529–539.
7. Zhang Y, Burke CW, Ryman KD, Klimstra WB. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. Journal of Virology 2007; 81: 11246–11255.
8. Muller S, Moller P, Bick MJ, et al. Inhibition of filovirus replication by the zinc finger antiviral protein. Journal of Virology 2007; 81: 2391–2400.
9. Bick MJ, Carroll JW, Gao G, Goff SP, Rice CM, MacDonald MR. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. Journal of Virology 2003; 77: 11555–11562.
10. Miyashita M, Oshiumi H, Matsumoto M, Seya T. DDX60, a DEXD/H box helicase, is a novel antiviral factor promoting RIG-I-like receptor-mediated signaling. Molecular and Cellular Biology 2011; 31: 3802–3819.
11. Oshiumi H, Miyashita M, Okamoto M, et al. DDX60 is involved in RIG-I-dependent and independent antiviral responses and its function is attenuated by virus-induced EGFR activation. Cell Reports 2015; 11: 1193–1207.
12. Yoneyama M, Fujita T. RNA recognition and signal transduction by RIG-I-like receptors. Immunology Reviews 2009; 227: 54–65.
13. Kato H, Takeuchi O, Sato S, et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441: 101–105.
14. Goubau D, Schlee M, Deddouche S, et al. Antiviral immunity via RIG-I-mediated recognition of RNA bearing 5′-diphosphates. Nature 2014; 514: 372–375.
15. Schlee M, Roth A, Hornung V, et al. Recognition of 5′ triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 2009; 31: 25–34.
16. Hornung V, Ellegast J, Kim S, et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science 2006; 314: 994–997.
17. Malathi K, Dong B, Gale M Jr, Silverman RH. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 2007; 448: 816–819.
18. Kato H, Takeuchi O, Mikamo-Satoh E, et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. Journal of Experimental Medicine 2008; 205: 1601–1610.
19. Loo YM, Fornek J, Crochet N, et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. Journal of Virology 2008; 82: 335–345.
20. Davis ME, Wang MK, Rennick LJ, et al. Antagonism of the phosphatase PP1 by the measles virus V protein is required for innate immune escape of MDA5. Cell Host & Microbe 2014; 16: 19–30.
21. Plumet S, Herschke F, Bourhis JM, Valentin H, Longhi S, Gerlier D. Cytosolic 5′-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2007; 2: e279.
22. Anderson P, Kedersha N. Stress granules: the Tao of RNA triage. Trends in Biochemical Sciences 2008; 33: 141–150.
23. Onomoto K, Yoneyama M, Fung G, Kato H, Fujita T. Antiviral innate immunity and stress granule responses. Trends in Immunology 2014; 35: 420–428.
24. Yoo JS, Takahasi K, Ng CS, et al. DHX36 enhances RIG-I signaling by facilitating PKR-mediated antiviral stress granule formation. PLoS Pathogens 2014; 10: e1004012.
25. Ng CS, Jogi M, Yoo JS, et al. Encephalomyocarditis virus disrupts stress granules, the critical platform for triggering antiviral innate immune responses. Journal of Virology 2013; 87: 9511–9522.
26. Onomoto K, Jogi M, Yoo JS, et al. Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity. PLoS One 2012; 7: e43031.
27. Oshiumi H, Matsumoto M, Hatakeyama S, Seya T. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. Journal of Biological Chemistry 2009; 284: 807–817.
28. Gack MU, Shin YC, Joo CH, et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007; 446: 916–920.
29. Oshiumi H, Miyashita M, Matsumoto M, Seya T. A distinct role of Riplet-mediated K63-Linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathogens 2013; 9: e1003533.
30. Langereis MA, Feng Q, van Kuppeveld FJ. MDA5 localizes to stress granules, but this localization is not required for the induction of type I interferon. Journal of Virology 2013; 87: 6314–6325.
31. Wu B, Peisley A, Richards C, et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 2013; 152: 276–289.
32. Peisley A, Wu B, Yao H, Walz T, Hur S. RIG-I forms signaling-competent filaments in an ATP-dependent, ubiquitin-independent manner. Molecular Cell 2013; 51: 573–583.
33. Wu B, Peisley A, Tetrault D, et al. Molecular imprinting as a signal-activation mechanism of the viral RNA sensor RIG-I. Molecular Cell 2014; 55: 511–523.
34. Peisley A, Wu B, Xu H, Chen ZJ, Hur S. Structural basis for ubiquitin-mediated antiviral signal activation by RIG-I. Nature 2014; 509: 110–114.
35. Liu HM, Loo YM, Horner SM, Zornetzer GA, Katze MG, Gale M Jr. The mitochondrial targeting chaperone 14-3-3epsilon regulates a RIG-I translocon that mediates membrane association and innate antiviral immunity. Cell Host & Microbe 2012; 11: 528–537.
36. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Molecular Cell 2005; 19: 727–740.
37. Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 2005; 122: 669–682.
38. Meylan E, Curran J, Hofmann K, et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005; 437: 1167–1172.
39. Kawai T, Takahashi K, Sato S, et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nature Immunology 2005; 6: 981–988.
40. Takashima K, Oshiumi H, Takaki H, Matsumoto M, Seya T. RIOK3-mediated phosphorylation of MDA5 interferes with its assembly and attenuates the innate immune response. Cell Reports 2015; 11: 192–200.
41. Wies E, Wang MK, Maharaj NP, et al. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 2013; 38: 437–449.
42. 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: 448–461.
43. Rebouillat D, Hovanessian AG. The human 2′,5′-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. Journal of Interferon & Cytokine Research 1999; 19: 295–308.
44. Zhu J, Ghosh A, Sarkar SN. OASL-a new player in controlling antiviral innate immunity. Current Opinion in Virology 2015; 12C: 15–19.
45. Kristiansen H, Gad HH, Eskildsen-Larsen S, Despres P, Hartmann R. The oligoadenylate synthetase family: an ancient protein family with multiple antiviral activities. Journal of Interferon & Cytokine Research 2011; 31: 41–47.
46. Wreschner DH, McCauley JW, Skehel JJ, Kerr IM. Interferon action—sequence specificity of the ppp(A2'p)nA-dependent ribonuclease. Nature 1981; 289: 414–417.
47. Floyd-Smith G, Slattery E, Lengyel P. Interferon action: RNA cleavage pattern of a (2′-5′)oligoadenylate-dependent endonuclease. Science 1981; 212: 1030–1032.
48. Gaglia MM, Covarrubias S, Wong W, Glaunsinger BA. A common strategy for host RNA degradation by divergent viruses. Journal of Virology 2012; 86: 9527–9530.
49. Li Y, Masaki T, Yamane D, McGivern DR, Lemon SM. Competing and noncompeting activities of miR-122 and the 5′ exonuclease Xrn1 in regulation of hepatitis C virus replication. Proceedings of the National Academy of Sciences of the United States of America 2013; 110: 1881–1886.
50. Burgess HM, Mohr I. Cellular 5′-3′ mRNA exonuclease Xrn1 controls double-stranded RNA accumulation and anti-viral responses. Cell Host & Microbe 2015; 17: 332–344.
51. Nguyen LH, Espert L, Mechti N, Wilson DM 3rd. The human interferon- and estrogen-regulated ISG20/HEM45 gene product degrades single-stranded RNA and DNA in vitro. Biochemistry 2001; 40: 7174–7179.
52. Lu X, Qin B, Ma Q, Yang C, Gong XY, Chen LM. Differential expression of ISG20 in chronic hepatitis B patients and relation to interferon-alpha therapy response. Journal of Medical Virology 2013; 85: 1506–1512.
53. Gongora C, David G, Pintard L, et al. Molecular cloning of a new interferon-induced PML nuclear body-associated protein. Journal of Biological Chemistry 1997; 272: 19457–19463.
54. Zhou Z, Wang N, Woodson SE, et al. Antiviral activities of ISG20 in positive-strand RNA virus infections. Virology 2011; 409: 175–188.
55. Pitha PM. Multiple effects of interferon on the replication of human immunodeficiency virus type 1. Antiviral Research 1994; 24: 205–219.
56. Januszyk K, Lima CD. The eukaryotic RNA exosome. Current Opinion in Structural Biology 2014; 24: 132–140.
57. Schmid M, Jensen TH. The exosome: a multipurpose RNA-decay machine. Trends in Biochemical Sciences 2008; 33: 501–510.
58. Gherzi R, Lee KY, Briata P, et al. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Molecular Cell 2004; 14: 571–583.
59. Chen CY, Gherzi R, Ong SE, et al. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 2001; 107: 451–464.
60. Mao R, Nie H, Cai D, et al. Inhibition of hepatitis B virus replication by the host zinc finger antiviral protein. PLoS Pathogens 2013; 9: e1003494.
61. Guo X, Carroll JW, Macdonald MR, Goff SP, Gao G. The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. Journal of Virology 2004; 78: 12781–12787.
62. Schoggins JW, Wilson SJ, Panis M, et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011; 472: 481–485.
63. Johnson SJ, Jackson RN. Ski2-like RNA helicase structures: common themes and complex assemblies. RNA Biology 2013; 10: 33–43.
64. Yoneyama M, Onomoto K, Jogi M, Akaboshi T, Fujita T. Viral RNA detection by RIG-I-like receptors. Current Opinion in Immunology 2015; 32: 48–53.
65. Zhu J, Zhang Y, Ghosh A, et al. Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor. Immunity 2014; 40: 936–948.
66. Lin WJ, Duffy A, Chen CY. Localization of AU-rich element-containing mRNA in cytoplasmic granules containing exosome subunits. Journal of Biological Chemistry 2007; 282: 19958–19968.
67. Lee H, Komano J, Saitoh Y, et al. Zinc-finger antiviral protein mediates retinoic acid inducible gene I-like receptor-independent antiviral response to murine leukemia virus. Proceedings of the National Academy of Sciences of the United States of America 2013; 110: 12379–12384.
68. Eckard SC, Rice GI, Fabre A, et al. The SKIV2L RNA exosome limits activation of the RIG-I-like receptors. Nature Immunology 2014; 15: 839–845.
69. Hayakawa S, Shiratori S, Yamato H, et al. ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses. Nature Immunology 2011; 12: 37–44.
70. Grunvogel O, Esser-Nobis K, Reustle A, et al. Dead box helicase 60-like (DDX60L) is an interferon stimulated gene restricting hepatitis C virus replication in cell culture. Journal of Virology 2015. DOI:10.1128/JVI.01297-15.
71. Goubau D, der Veen A, Chakravarty P, et al. Mouse superkiller-2-like helicases DDX60 is dispensable for type I IFN induction and immunity to multiple viruses. European Journal of Immunology 2015. DOI:10.1002/eji.201545794.
72. Sugimoto N, Mitoma H, Kim T, Hanabuchi S, Liu YJ. Helicase proteins DHX29 and RIG-I cosense cytosolic nucleic acids in the human airway system. Proceedings of the National Academy of Sciences of the United States of America 2014; 111: 7747–7752.
73. Oshiumi H, Sakai K, Matsumoto M, Seya T. DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-beta-inducing potential. European Journal of Immunology 2010; 40: 940–948.
74. Carney DS, Gale M: HCV regulation of host defense. In Hepatitis C Viruses: Genomes and Molecular Biology, Tan SL, (ed). Horizon Bioscience: Norfolk (UK), 2006.
75. Rajsbaum R, Albrecht RA, Wang MK, et al. Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathogens 2012; 8 e1003059.
76. Gack MU, Albrecht RA, Urano T, et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host & Microbe 2009; 5: 439–449.
77. Min JY, Krug RM. The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: inhibiting the 2′-5′ oligo (A) synthetase/RNase L pathway. Proceedings of the National Academy of Sciences of the United States of America 2006; 103: 7100–7105.
78. Zhao L, Jha BK, Wu A, et al. Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host & Microbe 2012; 11: 607–616.
79. Ueki IF, Min-Oo G, Kalinowski A, et al. Respiratory virus-induced EGFR activation suppresses IRF1-dependent interferon λ and antiviral defense in airway epithelium. Journal of Experimental Medicine 2013; 210: 1929–1936.
80. Lupberger J, Zeisel MB, Xiao F, et al. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nature Medicine 2011; 17: 589–595.
81. Qu X, Yang Z, Zhang S, et al. The human DEVH-box protein Ski2w from the HLA is localized in nucleoli and ribosomes. Nucleic Acids Research 1998; 26: 4068–4077.
82. Dangel AW, Shen L, Mendoza AR, Wu LC, Yu CY. Human helicase gene SKI2W in the HLA class III region exhibits striking structural similarities to the yeast antiviral gene SKI2 and to the human gene KIAA0052: emergence of a new gene family. Nucleic Acids Research 1995; 23: 2120–2126.
83. Fabre A, Charroux B, Martinez-Vinson C, et al. SKIV2L mutations cause syndromic diarrhea, or trichohepatoenteric syndrome. American Journal of Human Genetics 2012; 90: 689–692.
84. Crow MK. Advances in understanding the role of type I interferons in systemic lupus erythematosus. Current Opinion in Rheumatology 2014; 26: 467–474.
85. Fernando MM, Stevens CR, Sabeti PC, et al. Identification of two independent risk factors for lupus within the MHC in United Kingdom families. PLoS Genetics 2007; 3: e192.
86. Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006; 313: 104–107.
87. Dong B, Niwa M, Walter P, Silverman RH. Basis for regulated RNA cleavage by functional analysis of RNase L and Ire1p. RNA 2001; 7: 361–373.
88. Salomon R, Webster RG. The influenza virus enigma. Cell 2009; 136: 402–410.
89. Diebold SS. Recognition of viral single-stranded RNA by Toll-like receptors. Advanced Drug Delivery Reviews 2008; 60: 813–823.
90. Koyama S, Ishii KJ, Kumar H, et al. Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. Journal of Immunology 2007; 179: 4711–4720.
91. Satoh T, Kato H, Kumagai Y, et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proceedings of the National Academy of Sciences of the United States of America 2010; 107: 1512–1517.
92. Venkataraman T, Valdes M, Elsby R, et al. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. Journal of Immunology 2007; 178: 6444–6455.
93. Yoneyama M, Kikuchi M, Matsumoto K, et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. Journal of Immunology 2005; 175: 2851–2858.
94. Si-Tahar M, Blanc F, Furio L, et al. Protective role of LGP2 in influenza virus pathogenesis. Journal of Infectious Diseases 2014; 210: 214–223.
95. Stetson DB, Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 2006; 24: 93–103.
96. Ishii KJ, Coban C, Kato H, et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nature Immunology 2006; 7: 40–48.
97. Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013; 339: 786–791.
98. Kondo T, Kobayashi J, Saitoh T, et al. DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING trafficking. Proceedings of the National Academy of Sciences of the United States of America 2013; 110: 2969–2974.
99. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nature Immunology 2011; 12: 959–965.
100. Unterholzner L, Keating SE, Baran M, et al. IFI16 is an innate immune sensor for intracellular DNA. Nature Immunology 2010; 11: 997–1004.
101. Takaoka A, Wang Z, Choi MK, et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007; 448: 501–505.
102. Schoggins JW, MacDuff DA, Imanaka N, et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 2014; 505: 691–695.
103. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013; 341: 1390–1394.
104. Wu J, Sun L, Chen X, et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013; 339: 826–830.
105. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461: 788–792.
106. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008; 455: 674–678.
107. Abe T, Harashima A, Xia T, et al. STING recognition of cytoplasmic DNA instigates cellular defense. Molecular Cell 2013; 50: 5–15.
108. Burdette DL, Monroe KM, Sotelo-Troha K, et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011; 478: 515–518.
109. Roberts TL, Idris A, Dunn JA, et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009; 323: 1057–1060.
110. Burckstummer T, Baumann C, Bluml S, et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nature Immunology 2009; 10: 266–272.
111. Stetson DB, Ko JS, Heidmann T, Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008; 134: 587–598.
112. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nature Immunology 2010; 11: 1005–1013.