Cytosolic innate immune sensing and signaling upon infection

Frontiers in Microbiology

Volumn 7, Issue MAR, 2016, Pages

  Radoshevich, Lilliana ^a,b,c   Dussurget, Olivier ^a,b,c,d  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c CEMAGREF   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

DNA; Immunity; Interferon; MAVS; Pathogen; RNA; STING

Indexed keywords

STAT6 PROTEIN;

ADAPTIVE IMMUNITY; CELL FUNCTION; CELLULAR IMMUNITY; CYTOSOL; CYTOSOLIC SENSING; DNA SENSING; GENE; HUMAN; INNATE IMMUNITY; NONHUMAN; REVIEW; RNA SENSING; STIMULATOR OF INTERFERON GENE;

EID: 84964354362     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00313     Document Type: Review

References (104)

1. Abdullah, Z., Schlee, M., Roth, S., Mraheil, M. A., Barchet, W., Boettcher, J., et al. (2012). RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J. 31, 4153-4164. doi: 10.1038/emboj.2012.274
2. Abe, T., Harashima, A., Xia, T., Konno, H., Konno, K., Morales, A., et al. (2013). STING recognition of cytoplasmic DNA instigates cellular defense. Mol. Cell 50, 5-15. doi: 10.1016/j.molcel.2013.01.039
3. Ablasser, A., Goldeck, M., Cavlar, T., Deimling, T., Witte, G., Röhl, I., et al. (2013). cGAS produces a 2'-5'-linked cyclic dinucleotide second messenger that activates STING. Nature 498, 380-384. doi: 10.1038/nature12306
4. Aguirre, S., Maestre, A. M., Pagni, S., Patel, J. R., Savage, T., Gutman, D., et al. (2012). DENV inhibits type I IFN production in infected cells by cleaving human STING. PLoS Pathog. 8:e1002934. doi: 10.1371/journal.ppat.1002934
5. Andrejeva, J., Childs, K. S., Young, D. F., Carlos, T. S., Stock, N., Goodbourn, S., et al. (2004). The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. U.S.A. 101, 17264-17269. doi: 10.1073/pnas.0407639101
6. Archer, K. A., Durack, J., and Portnoy, D. A. (2014). STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog. 10:e1003861. doi: 10.1371/journal.ppat.1003861
7. Bale, S., Julien, J.-P., Bornholdt, Z. A., Kimberlin, C. R., Halfmann, P., Zandonatti, M. A., et al. (2012). Marburg virus VP35 can both fully coat the backbone and cap the ends of dsRNA for interferon antagonism. PLoS Pathog. 8:e1002916. doi: 10.1371/journal.ppat.1002916
8. Bale, S., Julien, J.-P., Bornholdt, Z. A., Krois, A. S., Wilson, I. A., and Saphire, E. O. (2013). Ebolavirus VP35 coats the backbone of double-stranded RNA for interferon antagonism. J. Virol. 87, 10385-10388. doi: 10.1128/JVI.01452-13
9. Bruns, A. M., Leser, G. P., Lamb, R. A., 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. doi: 10.1016/j.molcel.2014.07.003
10. Burdette, D. L., Monroe, K. M., Sotelo-Troha, K., Iwig, J. S., Eckert, B., Hyodo, M., et al. (2011). STING is a direct innate immune sensor of cyclic di-GMP. Nature 478, 515-518. doi: 10.1038/nature10429
11. Burnaevskiy, N., Fox, T. G., Plymire, D. A., Ertelt, J. M., Weigele, B. A., Selyunin, A. S., et al. (2014). Proteolytic elimination of N-myristoyl modifications by the Shigella virulence factor IpaJ. Nature 496, 106-109. doi: 10.1038/nature12004
12. Cai, X., Chiu, Y.-H., and Chen, Z. J. (2014). The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol. Cell 54, 289-296. doi: 10.1016/j.molcel.2014.03.040
13. Cárdenas, W. B., Loo, Y.-M., Gale, M., Hartman, A. L., Kimberlin, C. R., Martínez-Sobrido, L., et al. (2006). Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 80, 5168-5178. doi: 10.1128/JVI.02199-05
14. Chen, H., Sun, H., You, F., Sun, W., Zhou, X., Chen, L., et al. (2011). Activation of STAT6 by STING is critical for antiviral innate immunity. Cell 147, 436-446. doi: 10.1016/j.cell.2011.09.022
15. Childs, K., Randall, R., and Goodbourn, S. (2012). Paramyxovirus V proteins interact with the RNA helicase LGP2 to inhibit RIG-I-dependent interferon induction. J. Virol. 86, 3411-3421. doi: 10.1128/JVI.06405-11
16. Collins, A. C., Cai, H., Li, T., Franco, L. H., Li, X.-D., Nair, V. R., et al. (2015). Cyclic GMP-AMP synthase is an innate immune DNA sensor for Mycobacterium tuberculosis. Cell Host Microbe 17, 820-828. doi: 10.1016/j.chom.2015.05.005
17. Diner, E. J., Burdette, D. L., Wilson, S. C., Monroe, K. M., Kellenberger, C. A., Hyodo, M., et al. (2013). The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING. Cell Rep. 3, 1355-1361. doi: 10.1016/j.celrep.2013.05.009
18. Dixit, E., Boulant, S., Zhang, Y., Lee, A. S. Y., Odendall, C., Shum, B., et al. (2010). Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141, 668-681. doi: 10.1016/j.cell.2010.04.018
19. Dobbs, N., Burnaevskiy, N., Chen, D., Gonugunta, V. K., Alto, N. M., and Yan, N. (2015). STING Activation by translocation from the ER is associated with infection and autoinflammatory disease. Cell Host Microbe 18, 157-168. doi: 10.1016/j.chom.2015.07.001
20. Fan, L., Briese, T., and Lipkin, W. I. (2010). Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J. Virol. 84, 1785-1791. doi: 10.1128/JVI.01362-09
21. Feng, Z., Cerveny, M., Yan, Z., and He, B. (2007). The VP35 protein of Ebola virus inhibits the antiviral effect mediated by double-stranded RNA-dependent protein kinase PKR. J. Virol. 81, 182-192. doi: 10.1128/JVI.01006-06
22. Fitzgerald, K. A., Mcwhirter, S. M., Faia, K. L., Rowe, D. C., Latz, E., Golenbock, D. T., et al. (2003). IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496. doi: 10.1038/ni921
23. Freundt, E. C., Yu, L., Park, E., Lenardo, M. J., and Xu, X.-N. (2009). Molecular determinants for subcellular localization of the severe acute respiratory syndrome coronavirus open reading frame 3b protein. J. Virol. 83, 6631-6640. doi: 10.1128/JVI.00367-09
24. Frias-Staheli, N., Giannakopoulos, N. V., Kikkert, M., Taylor, S. L., Bridgen, A., Paragas, J., et al. (2007). Ovarian tumor domain-containing viral proteases evade ubiquitin-and ISG15-dependent innate immune responses. Cell Host Microbe 2, 404-416. doi: 10.1016/j.chom.2007.09.014
25. Gack, M. U., Albrecht, R. A., Urano, T., Inn, K.-S., Huang, I.-C., Carnero, E., et al. (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. doi: 10.1016/j.chom.2009.04.006
26. Gack, M. U., Shin, Y. C., Joo, C.-H., Urano, T., Liang, C., Sun, L., et al. (2007). TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446, 916-920. doi: 10.1038/nature05732
27. Gao, P., Ascano, M., Wu, Y., Barchet, W., Gaffney, B. L., Zillinger, T., et al. (2013a). Cyclic [G(2', 5')pA(3', 5')p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell 153, 1094-1107. doi: 10.1016/j.cell.2013.04.046
28. Gao, P., Ascano, M., Zillinger, T., Wang, W., Dai, P., Serganov, A. A., et al. (2013b). Structure-function analysis of STING activation by c[G(2', 5')pA(3', 5')p] and targeting by antiviral DMXAA. Cell 154, 748-762. doi: 10.1016/j.cell.2013.07.023
29. Habjan, M., Andersson, I., Klingström, J., Schümann, M., Martin, A., Zimmermann, P., et al. (2008). Processing of genome 5' termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE 3:e2032. doi: 10.1371/journal.pone.0002032
30. Hagmann, C. A., Herzner, A. M., Abdullah, Z., Zillinger, T., Jakobs, C., Schuberth, C., et al. (2013). RIG-I detects triphosphorylated RNA of Listeria monocytogenes during infection in non-immune cells. PLoS ONE 8:e62872. doi: 10.1371/journal.pone.0062872
31. Hansen, K., Prabakaran, T., Laustsen, A., Jorgensen, S. E., Rahbaek, S. H., Jensen, S. B., et al. (2014). Listeria monocytogenes induces IFN expression through an IFI16-, cGAS-and STING-dependent pathway. EMBO J. 33, 1654-1666. doi: 10.15252/embj.201488029
32. Hasan, M., Koch, J., Rakheja, D., Pattnaik, A. K., Brugarolas, J., Dozmorov, I., et al. (2013). Trex1 regulates lysosomal biogenesis and interferon-independent activation of antiviral genes. Nat. Immunol. 14, 61-71. doi: 10.1038/ni.2475
33. Hemmi, H., Takeuchi, O., Sato, S., Yamamoto, M., Kaisho, T., Sanjo, H., et al. (2004). The roles of two I-kappa-B kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199, 1641-1650. doi: 10.1084/jem.20040520
34. Hornung, V., Ellegast, J., Kim, S., Brzózka, K., Jung, A., Kato, H., et al. (2006). 5'-triphosphate RNA is the ligand for RIG-I. Science 314, 994-997. doi: 10.1126/science.1132505
35. 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. doi: 10.1016/j.cell.2011.06.041
36. Inn, K.-S., Lee, S.-H., Rathbun, J. Y., Wong, L.-Y., Toth, Z., Machida, K., et al. (2011). Inhibition of RIG-I-mediated signaling by Kaposi's sarcoma-associated herpesvirus-encoded deubiquitinase ORF64. J. Virol. 85, 10899-10904. doi: 10.1128/JVI.00690-11
37. Ishikawa, H., and Barber, G. N. (2008). STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455, 674-678. doi: 10.1038/nature07317
38. Ishikawa, H., Ma, Z., and Barber, G. N. (2009). STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792. doi: 10.1038/nature08476
39. Iwai, A., Shiozaki, T., Kawai, T., Akira, S., Kawaoka, Y., Takada, A., et al. (2010). Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J. Biol. Chem. 285, 32064-32074. doi: 10.1074/jbc. M110.112458
40. Jiang, F., Ramanathan, A., Miller, M. T., Tang, G.-Q., Gale, M., Patel, S. S., et al. (2011). Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 479, 423-427. doi: 10.1038/nature10537
41. Jiang, X., Huang, Q., Wang, W., Dong, H., Ly, H., Liang, Y., et al. (2013). Structures of arenaviral nucleoproteins with triphosphate dsRNA reveal a unique mechanism of immune suppression. J. Biol. Chem. 288, 16949-16959. doi: 10.1074/jbc. M112.420521
42. Johnston, J. B., Barrett, J. W., Nazarian, S. H., Goodwin, M., Ricuttio, D., Wang, G., et al. (2005). A Poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 23, 587-598. doi: 10.1016/j.immuni.2005.10.003
43. Karaolis, D. K. R., Means, T. K., Yang, D., Takahashi, M., Yoshimura, T., Muraille, E., et al. (2007a). Bacterial c-di-GMP is an immunostimulatory molecule. J. Immunol. 178, 2171-2181. doi: 10.4049/jimmunol.178.4.2171
44. Karaolis, D. K. R., Newstead, M. W., Zeng, X., Hyodo, M., Hayakawa, Y., Bhan, U., et al. (2007b). Cyclic di-GMP stimulates protective innate immunity in bacterial pneumonia. Infect. Immun. 75, 4942-4950. doi: 10.1128/IAI.01762-06
45. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., et al. (2006). Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105. doi: 10.1038/nature04734
46. Kawai, T., Takahashi, K., Sato, S., Coban, C., Kumar, H., Kato, H., et al. (2005). IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat. Immunol. 6, 981-988. doi: 10.1038/ni1243
47. Kopecky-Bromberg, S. A., Martínez-Sobrido, L., Frieman, M., Baric, R. A., and Palese, P. (2007). Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J. Virol. 81, 548-557
48. Kowalinski, E., Lunardi, T., McCarthy, A. A., Louber, J., Brunel, J., Grigorov, B., et al. (2011). Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 147, 423-435. doi: 10.1016/j.cell.2011.09.039
49. Lau, L., Gray, E. E., Brunette, R. L., and Stetson, D. B. (2015). DNA tumor virus oncogenes antagonize the cGAS-STING DNA-sensing pathway. Science 350, 568-571. doi: 10.1126/science.aab3291
50. Li, T., Chen, J., and Cristea, I. M. (2013). Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14, 591-599. doi: 10.1016/j.chom.2013.10.007
51. Li, X., Ranjith-Kumar, C. T., Brooks, M. T., Dharmaiah, S., Herr, A. B., Kao, C., et al. (2009). The RIG-I-like receptor LGP2 recognizes the termini of double-stranded RNA. J. Biol. Chem. 284, 13881-13891. doi: 10.1074/jbc. M900818200
52. Lu, X., Pan, J., Tao, J., and Guo, D. (2011). SARS-CoV nucleocapsid protein antagonizes IFN-β response by targeting initial step of IFN-β induction pathway, and its C-terminal region is critical for the antagonism. Virus Genes 42, 37-45. doi: 10.1007/s11262-010-0544-x
53. Manzanillo, P. S., Shiloh, M. U., Portnoy, D. A., and Cox, J. S. (2012). Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11, 469-480. doi: 10.1016/j.chom.2012.03.007
54. Marq, J.-B., Hausmann, S., Veillard, N., Kolakofsky, D., and Garcin, D. (2011). Short double-stranded RNAs with an overhanging 5' ppp-nucleotide, as found in Arenavirus genomes, act as RIG-I decoys. J. Biol. Chem. 286, 6108-6116. doi: 10.1074/jbc. M110.186262
55. Mcwhirter, S. M., Barbalat, R., Monroe, K. M., Fontana, M. F., Hyodo, M., Joncker, N. T., et al. (2009). A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J. Exp. Med. 206, 1899-1911. doi: 10.1084/jem.20082874
56. Mcwhirter, S. M., Fitzgerald, K. A., Rosains, J., Rowe, D. C., Golenbock, D. T., and Maniatis, T. (2004). IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 101, 233-238. doi: 10.1073/pnas.2237236100
57. Mesman, A. W., Zijlstra-Willems, E. M., Kaptein, T. M., de Swart, R. L., Davis, M. E., Ludlow, M., et al. (2014). Measles virus suppresses RIG-I-like receptor activation in dendritic cells via DC-SIGN-mediated inhibition of PP1 phosphatases. Cell Host Microbe 16, 31-42. doi: 10.1016/j.chom.2014.06.008
58. Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R., et al. (2005). Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437, 1167-1172. doi: 10.1038/nature04193
59. Motz, C., Schuhmann, K. M., Kirchhofer, A., Moldt, M., Witte, G., Conzelmann, K. K., et al. (2013). Paramyxovirus V proteins disrupt the fold of the RNA sensor MDA5 to inhibit antiviral signaling. Science 339, 690-693. doi: 10.1126/science.1230949
60. Nan, Y., Yu, Y., Ma, Z., Khattar, S. K., Fredericksen, B., and Zhang, Y.-J. (2014). Hepatitis E virus inhibits type I interferon induction by ORF1 products. J. Virol. 88, 11924-11932. doi: 10.1128/JVI.01935-14
61. Odendall, C., Dixit, E., Stavru, F., Bierne, H., Franz, K. M., Durbin, A. F., et al. (2014). Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 15, 717-726. doi: 10.1038/ni.2915
62. Orzalli, M. H., DeLuca, N. A., and Knipe, D. M. (2012). Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. U.S.A. 109, E3008-E3017. doi: 10.1073/pnas.1211302109
63. Oshiumi, H., Ikeda, M., Matsumoto, M., Watanabe, A., Takeuchi, O., Akira, S., et al. (2010). Hepatitis C virus core protein abrogates the DDX3 function that enhances IPS-1-mediated IFN-beta induction. PLoS ONE 5:e14258. doi: 10.1371/journal.pone.0014258
64. 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. doi: 10.1371/journal.ppat.1003533
65. Paludan, S. R., and Bowie, A. G. (2013). Immune sensing of DNA. Immunity 38, 870-880. doi: 10.1016/j.immuni.2013.05.004
66. Parisien, J.-P., Bamming, D., Komuro, A., Ramachandran, A., Rodriguez, J. J., Barber, G., et al. (2009). A shared interface mediates paramyxovirus interference with antiviral RNA helicases MDA5 and LGP2. J. Virol. 83, 7252-7260. doi: 10.1128/JVI.00153-09
67. Perry, A. K., Chow, E. K., Goodnough, J. B., Yeh, W.-C., and Cheng, G. (2004). Differential requirement for TANK-binding kinase-1 in type I interferon responses to toll-like receptor activation and viral infection. J. Exp. Med. 199, 1651-1658. doi: 10.1084/jem.20040528
68. Peters, N. E., Ferguson, B. J., Mazzon, M., Fahy, A. S., Krysztofinska, E., Arribas-Bosacoma, R., et al. (2013). A mechanism for the inhibition of DNA-PK-mediated DNA sensing by a virus. PLoS Pathog. 9:e1003649. doi: 10.1371/journal.ppat.1003649
69. Pichlmair, A., Schulz, O., Tan, C. P., Näslund, T. I., Liljeström, P., Weber, F., et al. (2006). RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 314, 997-1001. doi: 10.1126/science.1132998
70. Pippig, D. A., Hellmuth, J. C., Cui, S., Kirchhofer, A., Lammens, K., Lammens, A., et al. (2009). The regulatory domain of the RIG-I family ATPase LGP2 senses double-stranded RNA. Nucleic Acids Res. 37, 2014-2025. doi: 10.1093/nar/gkp059
71. Radoshevich, L., Impens, F., Ribet, D., Quereda, J. J., Nam Tham, T., Nahori, M.-A., et al. (2015). ISG15 counteracts Listeria monocytogenes infection. Elife 4, e06848. doi: 10.7554/eLife.06848
72. Rebsamen, M., Heinz, L. X., Meylan, E., Michallet, M.-C. E. C., Schroder, K., Hofmann, K., et al. (2009). DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-kappaB. EMBO Rep. 10, 916-922. doi: 10.1038/embor.2009.109
73. Saitoh, T., Fujita, N., Hayashi, T., Takahara, K., Satoh, T., Lee, H., et al. (2009). Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl. Acad. Sci. U.S.A. 106, 20842-20846. doi: 10.1073/pnas.0911267106
74. Sauer, J.-D., Sotelo-Troha, K., von Moltke, J., Monroe, K. M., Rae, C. S., Brubaker, S. W., et al. (2011). The N-ethyl-N-nitrosourea-induced goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 79, 688-694. doi: 10.1128/IAI.00999-10
75. Schlee, M., Roth, A., Hornung, V., Hagmann, C. A., Wimmenauer, V., Barchet, W., et al. (2009). Recognition of 5' triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 31, 25-34. doi: 10.1016/j.immuni.2009.05.008
76. Schmidt, A., Schwerd, T., Hamm, W., Hellmuth, J. C., Cui, S., Wenzel, M., et al. (2009). 5'-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc. Natl. Acad. Sci. U.S.A. 106, 12067-12072. doi: 10.1073/pnas.0900971106
77. Schröder, 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. doi: 10.1038/emboj.2008.143
78. Seth, R., Sun, L., Ea, C., and Chen, Z. (2005). Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF3. Cell 122, 669-682. doi: 10.1016/j.cell.2005.08.012
79. Shah, S., Bohsali, A., Ahlbrand, S. E., Srinivasan, L., Rathinam, V. A. K., Vogel, S. N., et al. (2013). Cutting Edge: Mycobacterium tuberculosis but not nonvirulent mycobacteria inhibits IFN-beta and AIM2 inflammasome-dependent IL-1beta production via its ESX-1 secretion system. J. Immunol. 191, 3514-3518. doi: 10.4049/jimmunol.1301331
80. Sharma, S., Tenoever, B. R., Grandvaux, N., Zhou, G.-P., Lin, R., and Hiscott, J. (2003). Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151. doi: 10.1126/science.1081315
81. Siu, K.-L., Kok, K.-H., Ng, M.-H. J., Poon, V. K. M., Yuen, K.-Y., Zheng, B.-J., et al. (2009). Severe acute respiratory syndrome coronavirus M protein inhibits type I interferon production by impeding the formation of TRAF3.TANK.TBK1/IKKepsilon complex. J. Biol. Chem. 284, 16202-16209. doi: 10.1074/jbc. M109.008227
82. Stetson, D., and Medzhitov, R. (2006). Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24, 93-103. doi: 10.1016/j.immuni.2005.12.003
83. Stetson, D. B., Ko, J. S., Heidmann, T., and Medzhitov, R. (2008). Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134, 587-598. doi: 10.1016/j.cell.2008.06.032
84. Stracker, T. H., Carson, C. T., and Weitzman, M. D. (2002). Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418, 348-352. doi: 10.1038/nature00863
85. Sun, L., Wu, J., Du, F., Chen, X., and Chen, Z. J. (2013). Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339, 786-791. doi: 10.1126/science.1232458
86. Valentine, R., and Smith, G. L. (2010). Inhibition of the RNA polymerase III-mediated dsDNA-sensing pathway of innate immunity by vaccinia virus protein E3. J. Gen. Virol. 91, 2221-2229. doi: 10.1099/vir.0.021998-0
87. van Kasteren, P. B., Beugeling, C., Ninaber, D. K., Frias-Staheli, N., van Boheemen, S., García-Sastre, A., et al. (2012). Arterivirus and nairovirus ovarian tumor domain-containing deubiquitinases target activated RIG-I to control innate immune signaling. J. Virol. 86, 773-785. doi: 10.1128/JVI.06277-11
88. Varga, Z. T., Grant, A., Manicassamy, B., and Palese, P. (2012). Influenza virus protein PB1-F2 inhibits the induction of type I interferon by binding to MAVS and decreasing mitochondrial membrane potential. J. Virol. 86, 8359-8366. doi: 10.1128/JVI.01122-12
89. Wassermann, R., Gulen, M. F., Sala, C., Perin, S. G., Lou, Y., Rybniker, J., et al. (2015). Mycobacterium tuberculosis differentially activates cGAS-and inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 17, 799-810. doi: 10.1016/j.chom.2015.05.003
90. Watson, R. O., Bell, S. L., MacDuff, D. A., Kimmey, J. M., Diner, E. J., Olivas, J., et al. (2015). The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy. Cell Host Microbe 17, 811-819. doi: 10.1016/j.chom.2015.05.004
91. Weitzman, M. D., and Ornelles, D. A. (2005). Inactivating intracellular antiviral responses during adenovirus infection. Oncogene 24, 7686-7696. doi: 10.1038/sj.onc.1209063
92. Welsch, S., Miller, S., Romero-Brey, I., Merz, A., Bleck, C. K. E., Walther, P., et al. (2009). Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5, 365-375. doi: 10.1016/j.chom.2009.03.007
93. Woodward, J. J., Iavarone, A. T., and Portnoy, D. A. (2010). c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328, 1703-1705. doi: 10.1126/science.1189801
94. Wu, B., Peisley, A., Richards, C., Yao, H., Zeng, X., Lin, C., et al. (2013a). Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 152, 276-289. doi: 10.1016/j.cell.2012.11.048
95. Wu, J., Sun, L., Chen, X., Du, F., Shi, H., Chen, C., et al. (2013b). Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339, 826-830. doi: 10.1126/science.1229963
96. Wu, J.-J., Li, W., Shao, Y., Avey, D., Fu, B., Gillen, J., et al. (2015). Inhibition of cGAS DNA sensing by a Herpesvirus virion protein. Cell Host Microbe 18, 333-344. doi: 10.1016/j.chom.2015.07.015
97. Xing, J., Wang, S., Lin, R., Mossman, K. L., and Zheng, C. (2012). Herpes simplex virus 1 tegument protein US11 downmodulates the RLR signaling pathway via direct interaction with RIG-I and MDA-5. J. Virol. 86, 3528-3540. doi: 10.1128/JVI.06713-11
98. 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. doi: 10.1016/j.molcel.2005.08.014
99. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., et al. (2004). The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737. doi: 10.1038/ni1087
100. Zeng, W., Sun, L., Jiang, X., Chen, X., Hou, F., Adhikari, A., et al. (2010). Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141, 315-330. doi: 10.1016/j.cell.2010.03.029
101. Zeng, W., Xu, M., Liu, S., Sun, L., and Chen, Z. J. (2009). Key role of Ubc5 and lysine-63 polyubiquitination in viral activation of IRF3. Mol. Cell 36, 315-325. doi: 10.1016/j.molcel.2009.09.037
102. Zhang, X., Shi, H., Wu, J., Zhang, X., Sun, L., Chen, C., et al. (2013). Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol. Cell 51, 226-235. doi: 10.1016/j.molcel.2013.05.022
103. Zinzula, L., and Tramontano, E. (2013). Strategies of highly pathogenic RNA viruses to block dsRNA detection by RIG-I-like receptors: hide, mask, hit. Antiviral Res. 100, 615-635. doi: 10.1016/j.antiviral.2013.10.002
104. Züst, R., Cervantes-Barragan, L., Habjan, M., Maier, R., Neuman, B. W., Ziebuhr, J., et al. (2011). Ribose 2'-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. immunol. 12, 137-143. doi: 10.1038/ni.1979