Cytoplasmic nucleic acid sensors in antiviral immunity

Trends in Molecular Medicine

Volumn 15, Issue 8, 2009, Pages 359-368

  Ranjan, Priya ^a   Bowzard, J Bradford ^a   Schwerzmann, Joy W ^a   Jeisy Scott, Victoria ^b   Fujita, Takashi ^c   Sambhara, Suryaprakash ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b EMORY UNIVERSITY   (United States)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA DEPENDENT ACTIVATOR OF INTERFERON REGULATORY FACTOR; PATTERN RECOGNITION RECEPTOR; PROTEIN AIM2; REGULATOR PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RNA; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ENZYME ACTIVATION; HEPATITIS C VIRUS; HUMAN; INFLUENZA VIRUS; INNATE IMMUNITY; NONHUMAN; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS INFECTION;

ANIMALS; CYTOPLASM; DNA, VIRAL; HUMANS; RECEPTORS, PATTERN RECOGNITION; RNA, VIRAL; VIRUS DISEASES; VIRUSES;

BACTERIA (MICROORGANISMS);

EID: 68649096389     PISSN: 14714914     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmed.2009.06.003     Document Type: Review

References (107)

1. Pulendran B., and Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 124 (2006) 849-863
2. Kimbrell D.A., and Beutler B. The evolution and genetics of innate immunity. Nat. Rev. Genet. 2 (2001) 256-267
3. Sadler A.J., and Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8 (2008) 559-568
4. Akira S., et al. Pathogen recognition and innate immunity. Cell 124 (2006) 783-801
5. Janeway Jr. C.A., and Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 20 (2002) 197-216
6. Lemaitre B., et al. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86 (1996) 973-983
7. Gorden K.B., et al. Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol. 174 (2005) 1259-1268
8. Guillot L., et al. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J. Biol. Chem. 280 (2005) 5571-5580
9. Heil F., et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303 (2004) 1526-1529
10. Zucchini N., et al. Cutting edge: Overlapping functions of TLR7 and TLR9 for innate defense against a herpesvirus infection. J. Immunol. 180 (2008) 5799-5803
11. O'Neill L.A., and Bowie A.G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7 (2007) 353-364
12. Bonjardim C.A., et al. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 122 (2009) 1-11
13. Kawai T., and Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 1143 (2008) 1-20
14. Browne E.P., and Littman D.R. Myd88 is required for an antibody response to retroviral infection. PLoS Pathog. 5 (2009) e1000298
15. Heer A.K., et al. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. J. Immunol. 178 (2007) 2182-2191
16. Koyama S., et al. Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. J. Immunol. 179 (2007) 4711-4720
17. Le Goffic R., et al. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog. 2 (2006) e53
18. Yoneyama M., et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
19. Yoneyama M., et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175 (2005) 2851-2858
20. Rothenfusser S., et al. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 175 (2005) 5260-5268
21. Kato H., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441 (2006) 101-105
22. Loo Y.M., et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82 (2008) 335-345
23. Kato H., et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205 (2008) 1601-1610
24. Hornung V., et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314 (2006) 994-997
25. Pichlmair A., et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314 (2006) 997-1001
26. Li W.Y., et al. Nucleotide sequence of 7 S RNA. Homology to Alu DNA and La 4.5 S RNA. J. Biol. Chem. 257 (1982) 5136-5142
27. Zieve G., et al. Synthesis of two classes of small RNA species in vivo and in vitro. Biochemistry 16 (1977) 4520-4525
28. Saito T., et al. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454 (2008) 523-527
29. Bamming D., and Horvath C.M. Regulation of signal transduction by enzymatically inactive antiviral RNA helicase proteins MDA5, RIG-I and LGP2. J. Biol. Chem. 284 (2009) 9700-9712
30. Saito T., et al. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 582-587
31. Li X., et al. The RIG-I like receptor LGP2 recognizes the termini of double-stranded RNA. J. Biol. Chem. 284 (2009) 13881-13891
32. Takahasi K., et al. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 29 (2008) 428-440
33. Cui S., et al. The C-terminal regulatory domain is the RNA 5′-triphosphate sensor of RIG-I. Mol. Cell 29 (2008) 169-179
34. Takahasi K., et al. Solution structures of cytosolic RNA sensors MDA5 and LGP2 C-terminal domains: Identification of the RNA recognition loop in RIG-I like receptors. J. Biol. Chem. 284 (2009) 17465-17474
35. Myong S., et al. Cytosolic viral sensor RIG-I Is a 5′-triphosphate-dependent translocase on double-stranded RNA. Science 323 (2009) 1070-1074
36. Ranjith-Kumar C.T., et al. Agonist and antagonist recognition by RIG-I, a cytoplasmic innate immunity receptor. J. Biol. Chem. 284 (2009) 1155-1165
37. Kawai T., et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6 (2005) 981-988
38. Meylan E., et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437 (2005) 1167-1172
39. Seth R.B., et al. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 122 (2005) 669-682
40. Xu L.G., et al. VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol. Cell 19 (2005) 727-740
41. Panne D., et al. An atomic model of the interferon-β enhanceosome. Cell 129 (2007) 1111-1123
42. Hacker H., and Karin M. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006 (2006) re13
43. Malmgaard L. Induction and regulation of IFNs during viral infections. J. Interferon Cytokine Res. 24 (2004) 439-454
44. Chau T.L., et al. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated?. Trends Biochem. Sci. 33 (2008) 171-180
45. Michallet M.C., et al. TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 28 (2008) 651-661
46. Yoshida R., et al. TRAF6 and MEKK1 play a pivotal role in the RIG-I-like helicase antiviral pathway. J. Biol. Chem. 283 (2008) 36211-36220
47. Saha S.K., et al. Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J. 25 (2006) 3257-3263
48. Ishikawa H., and Barber G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455 (2008) 674-678
49. Jin L., et al. MPYS, a novel membrane tetraspanner, is associated with major histocompatibility complex class II and mediates transduction of apoptotic signals. Mol. Cell. Biol. 28 (2008) 5014-5026
50. Zhong B., et al. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29 (2008) 538-550
51. Kang D.C., et al. mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 637-642
52. Chen Z.J., and Sun L.J. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33 (2009) 275-286
53. Gack M.U., et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446 (2007) 916-920
54. Gack M.U., et al. Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 16743-16748
55. Oshiumi H., et al. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-β induction during the early phase of viral infection. J. Biol. Chem. 284 (2009) 807-817
56. Friedman C.S., et al. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 9 (2008) 930-936
57. Zhang M., et al. Regulation of IκB kinase-related kinases and antiviral responses by tumor suppressor CYLD. J. Biol. Chem. 283 (2008) 18621-18626
58. Arimoto K., et al. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 7500-7505
59. Komuro A., et al. Negative regulation of cytoplasmic RNA-mediated antiviral signaling. Cytokine 43 (2008) 350-358
60. O'Neill L.A. Innate immunity: squelching anti-viral signalling with NLRX1. Curr. Biol. 18 (2008) R302-R304
61. Moore C.B., and Ting J.P. Regulation of mitochondrial antiviral signaling pathways. Immunity 28 (2008) 735-739
62. Moore C.B., et al. NLRX1 is a regulator of mitochondrial antiviral immunity. Nature 451 (2008) 573-577
63. Xu L., et al. Inhibition of RIG-I and MDA5-dependent antiviral response by gC1qR at mitochondria. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 1530-1535
64. Mashima R., et al. FLN29, a novel interferon- and LPS-inducible gene acting as a negative regulator of toll-like receptor signaling. J. Biol. Chem. 280 (2005) 41289-41297
65. Sanada T., et al. FLN29 deficiency reveals its negative regulatory role in the Toll-like receptor (TLR) and retinoic acid-inducible gene I (RIG-I)-like helicase signaling pathway. J. Biol. Chem. 283 (2008) 33858-33864
66. Guo Z., et al. NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am. J. Respir. Cell Mol. Biol. 36 (2007) 263-269
67. Mibayashi M., et al. Inhibition of retinoic acid-inducible gene I-mediated induction of β interferon by the NS1 protein of influenza A virus. J. Virol. 81 (2007) 514-524
68. Opitz B., et al. IFNβ induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell. Microbiol. 9 (2007) 930-938
69. Bowie A.G., and Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 8 (2008) 911-922
70. Garcia M.A., et al. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 70 (2006) 1032-1060
71. Nallagatla S.R., et al. 5′-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318 (2007) 1455-1458
72. Takaoka A., et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448 (2007) 501-505
73. Rothenburg S., et al. Complex regulation of the human gene for the Z-DNA binding protein DLM-1. Nucleic Acids Res. 30 (2002) 993-1000
74. Wang Z., et al. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 5477-5482
75. Kaiser W.J., et al. Receptor-interacting protein homotypic interaction motif-dependent control of NF-κ B activation via the DNA-dependent activator of IFN regulatory factors. J. Immunol. 181 (2008) 6427-6434
76. Burckstummer T., et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10 (2009) 266-272
77. Fernandes-Alnemri T., et al. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458 (2009) 509-513
78. Hornung V., et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458 (2009) 514-518
79. Roberts T.L., et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323 (2009) 1057-1060
80. Ishizaki Y., et al. Association of toll-like receptor 3 gene polymorphism with subacute sclerosing panencephalitis. J. Neurovirol. (2008) 1-6
81. Moller-Larsen S., et al. Association analysis identifies TLR7 and TLR8 as novel risk genes in asthma and related disorders. Thorax 63 (2008) 1064-1069
82. Mockenhaupt F.P., et al. Toll-like receptor (TLR) polymorphisms in African children: Common TLR-4 variants predispose to severe malaria. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 177-182
83. Torok H.P., et al. Crohn's disease is associated with a toll-like receptor-9 polymorphism. Gastroenterology 127 (2004) 365-366
84. Nejentsev S., et al. Rare variants of IFIH1, a gene implicated in antiviral responses, protect against Type 1 diabetes. Science 324 (2009) 387-389
85. Shigemoto T., et al. Identification of loss of function mutations in human genes encoding RIG-I and mda5: Implications for resistance to type I diabetes. J. Biol. Chem. 284 (2009) 13348-13354
86. Komuro A., and Horvath C.M. RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J. Virol. 80 (2006) 12332-12342
87. Venkataraman T., et al. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 178 (2007) 6444-6455
88. Jounai N., et al. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 14050-14055
89. Kim M.J., et al. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J. Virol. 82 (2008) 1474-1483
90. Cardenas W.B., et al. Ebola virus VP35 protein binds double-stranded RNA and inhibits α/β interferon production induced by RIG-I signaling. J. Virol. 80 (2006) 5168-5178
91. Foy E., et al. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 2986-2991
92. Loo Y.M., et al. Viral and therapeutic control of IFN-β promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6001-6006
93. Lin R., et al. Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKepsilon molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J. Virol. 80 (2006) 6072-6083
94. Li X.D., et al. Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17717-17722
95. Diao F., et al. Negative regulation of MDA5- but not RIG-I-mediated innate antiviral signaling by the dihydroxyacetone kinase. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 11706-11711
96. Childs K.S., et al. Mechanism of mda-5 Inhibition by paramyxovirus V proteins. J. Virol. 83 (2009) 1465-1473
97. Andrejeva J., et al. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-β promoter. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 17264-17269
98. Pang Q., et al. Nucleophosmin interacts with and inhibits the catalytic function of eukaryotic initiation factor 2 kinase PKR. J. Biol. Chem. 278 (2003) 41709-41717
99. Lee T.G., et al. The 58,000-dalton cellular inhibitor of the interferon-induced double-stranded RNA-activated protein kinase (PKR) is a member of the tetratricopeptide repeat family of proteins. Mol. Cell. Biol. 14 (1994) 2331-2342
100. Lu Y., et al. Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 214 (1995) 222-228
101. Li S., et al. Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349 (2006) 13-21
102. Gale Jr. M.J., et al. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230 (1997) 217-227
103. Romano P.R., et al. Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: role of complex formation and the E3 N-terminal domain. Mol. Cell. Biol. 18 (1998) 7304-7316
104. Sharp T.V., et al. The vaccinia virus E3L gene product interacts with both the regulatory and the substrate binding regions of PKR: implications for PKR autoregulation. Virology 250 (1998) 302-315
105. Stehlik C., et al. The PAAD/PYRIN-only protein POP1/ASC2 is a modulator of ASC-mediated nuclear-factor-κB and pro-caspase-1 regulation. Biochem. J. 373 (2003) 101-113
106. Johnston J.B., et al. A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 23 (2005) 587-598
107. Dorfleutner A., et al. A Shope Fibroma virus PYRIN-only protein modulates the host immune response. Virus Genes 35 (2007) 685-694