ZBP1/DAI is an innate sensor of influenza virus triggering the NLRP3 inflammasome and programmed cell death pathways

Science Immunology

Volumn 1, Issue 2, 2016, Pages

  Kuriakose, Teneema ^a   Man, Si Ming ^a   Subbarao Malireddi, R K ^a   Karki, Rajendra ^a   Kesavardhana, Sannula ^a   Place, David E ^a   Neale, Geoffrey ^a   Vogel, Peter ^a   Kanneganti, Thirumala Devi ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85022040336     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aag2045     Document Type: Article

References (49)

1. World Health Organization (WHO), “Influenza (seasonal)” (Fact sheet no. 211, WHO, 2014); www.who.int/mediacentre/factsheets/fs211/en/index.html.
2. A. Iwasaki, P. S. Pillai, Innate immunity to influenza virus infection. Nat. Rev. Immunol. 14, 315–328 (2014).
3. I. Jorgensen, E. A. Miao, Pyroptotic cell death defends against intracellular pathogens. Immunol. Rev. 265, 130–142 (2015).
4. C. J. Sanders, P. Vogel, J. L. McClaren, R. Bajracharya, P. C. Doherty, P. G. Thomas, Compromised respiratory function in lethal influenza infection is characterized by the depletion of type I alveolar epithelial cells beyond threshold levels. Am. J. Physiol. Lung Cell. Mol. Physiol. 304, L481–L488 (2013).
5. S. Herold, S. Ludwig, S. Pleschka, T. Wolff, Apoptosis signaling in influenza virus propagation, innate host defense, and lung injury. J. Leukoc. Biol. 92, 75–82 (2012).
6. S. Herold, T. S. Tabar, H. Janßen, K. Hoegner, M. Cabanski, P. Lewe-Schlosser, J. Albrecht, F. Driever, I. Vadasz, W. Seeger, M. Steinmueller, J. Lohmeyer, Exudate macrophages attenuate lung injury by the release of IL-1 receptor antagonist in gram-negative pneumonia. Am. J. Respir. Crit. Care Med. 183, 1380–1390 (2011).
7. I. G. Rodrigue-Gervais, K. Labbé, M. Dagenais, J. Dupaul-Chicoine, C. Champagne, A. Morizot, A. Skeldon, E. L. Brincks, S. M. Vidal, T. S. Griffith, M. Saleh, Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival. Cell Host Microbe 15, 23–35 (2014).
8. P. G. Thomas, P. Dash, J. R. Aldridge Jr., A. H. Ellebedy, C. Reynolds, A. J. Funk, W. J. Martin, M. Lamkanfi, R. J. Webby, K. L. Boyd, P. C. Doherty, T.-D. Kanneganti, The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30, 566–575 (2009).
9. I. C. Allen, M. A. Scull, C. B. Moore, E. K. Holl, E. McElvania-TeKippe, D. J. Taxman, E. H. Guthrie, R. J. Pickles, J. P.-Y. Ting, The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30, 556–565 (2009).
10. A. Takaoka, Z. Wang, M. K. Choi, H. Yanai, H. Negishi, T. Ban, Y. Lu, M. Miyagishi, T. Kodama, K. Honda, Y. Ohba, T. Taniguchi, DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448, 501–505 (2007).
11. T. Schwartz, J. Behlke, K. Lowenhaupt, U. Heinemann, A. Rich, Structure of the DLM-1–Z-DNA complex reveals a conserved family of Z-DNA-binding proteins. Nat. Struct. Biol. 8, 761–765 (2001).
12. Z. Wang, M. K. Choi, T. Ban, H. Yanai, H. Negishi, Y. Lu, T. Tamura, A. Takaoka, K. Nishikura, T. Taniguchi, Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc. Natl. Acad. Sci. U.S.A. 105, 5477–5482 (2008).
13. K. J. Ishii, T. Kawagoe, S. Koyama, K. Matsui, H. Kumar, T. Kawai, S. Uematsu, O. Takeuchi, F. Takeshita, C. Coban, S. Akira, TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 451, 725–729 (2008).
14. J. W. Upton, W. J. Kaiser, E. S. Mocarski, DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11, 290–297 (2012).
15. S. M. Man, T.-D. Kanneganti, Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat. Rev. Immunol. 16, 7–21 (2016).
16. T.-D. Kanneganti, M. Body-Malapel, A. Amer, J.-H. Park, J. Whitfield, L. Franchi, Z. F. Taraporewala, D. Miller, J. T. Patton, N. Inohara, G. Núñez, Critical role for Cryopyrin/ Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281, 36560–36568 (2006).
17. T. Ichinohe, H. K. Lee, Y. Ogura, R. Flavell, A. Iwasaki, Inflammasome recognition of influenza virus is essential for adaptive immune responses. J. Exp. Med. 206, 79–87 (2009).
18. T. Ichinohe, I. K. Pang, A. Iwasaki, Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 11, 404–410 (2010).
19. X. Wang, W. Jiang, Y. Yan, T. Gong, J. Han, Z. Tian, R. Zhou, RNA viruses promote activation of the NLRP3 inflammasome through a RIP1-RIP3-DRP1 signaling pathway. Nat. Immunol. 15, 1126–1133 (2014).
20. W. J. Kaiser, J. W. Upton, E. S. Mocarski, Receptor-interacting protein homotypic interaction motif-dependent control of NF-kB activation via the DNA-dependent activator of IFN regulatory factors. J. Immunol. 181, 6427–6434 (2008).
21. M. Rebsamen, L. X. Heinz, E. Meylan, M.-C. Michallet, K. Schroder, K. Hofmann, J. Vazquez, C. A. Benedict, J. Tschopp, DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-kB. EMBO Rep. 10, 916–922 (2009).
22. M. Yabal, N. Müller, H. Adler, N. Knies, C. J. Groß, R. B. Damgaard, H. Kanegane, M. Ringelhan, T. Kaufmann, M. Heikenwälder, A. Strasser, O. Groß, J. Ruland, C. Peschel, M. Gyrd-Hansen, P. J. Jost, XIAP restricts TNF- and RIP3-dependent cell death and inflammasome activation. Cell Rep. 7, 1796–1808 (2014).
23. K. Moriwaki, J. Bertin, P. J. Gough, F. K.-M. Chan, A RIPK3–caspase 8 complex mediates atypical pro–IL-1b processing. J. Immunol. 194, 1938–1944 (2015).
24. K. Newton, D. L. Dugger, K. E. Wickliffe, N. Kapoor, M. C. de Almagro, D. Vucic, L. Komuves, R. E. Ferrando, D. M. French, J. Webster, M. Roose-Girma, S. Warming, V. M. Dixit, Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 343, 1357–1360 (2014).
25. P. Mandal, S. B. Berger, S. Pillay, K. Moriwaki, C. Huang, H. Guo, J. D. Lich, J. Finger, V. Kasparcova, B. Votta, M. Ouellette, B. W. King, D. Wisnoski, A. S. Lakdawala, M. P. DeMartino, L. N. Casillas, P. A. Haile, C. A. Sehon, R. W. Marquis, J. Upton, L. P. Daley-Bauer, L. Roback, N. Ramia, C. M. Dovey, J. E. Carette, F. K.-M. Chan, J. Bertin, P. J. Gough, E. S. Mocarski, W. J. Kaiser, RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol. Cell 56, 481–495 (2014).
26. L. Sun, H. Wang, Z. Wang, S. He, S. Chen, D. Liao, L. Wang, J. Yan, W. Liu, X. Lei, X. Wang, Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148, 213–227 (2012).
27. J. M. Hildebrand, M. C. Tanzer, I. S. Lucet, S. N. Young, S. K. Spall, P. Sharma, C. Pierotti, J.-M. Garnier, R. C. J. Dobson, A. I. Webb, A. Tripaydonis, J. J. Babon, M. D. Mulcair, M. J. Scanlon, W. S. Alexander, A. F. Wilks, P. E. Czabotar, G. Lessene, J. M. Murphy, J. Silke, Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc. Natl. Acad. Sci. U.S.A. 111, 15072–15077 (2014).
28. J. K. Taubenberger, D. M. Morens, 1918 Influenza: The mother of all pandemics. Emerg. Infect. Dis. 12, 15–22 (2006).
29. S. Balachandran, P. C. Roberts, T. Kipperman, K. N. Bhalla, R. W. Compans, D. R. Archer, G. N. Barber, Alpha/beta interferons potentiate virus-induced apoptosis through activation of the FADD/caspase-8 death signaling pathway. J. Virol. 74, 1513–1523 (2000).
30. R. J. Thapa, S. Nogusa, P. Chen, J. L. Maki, A. Lerro, M. Andrake, G. F. Rall, A. Degterev, S. Balachandran, Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc. Natl. Acad. Sci. U.S.A. 110, E3109–E3118 (2013).
31. S. McComb, E. Cessford, N. A. Alturki, J. Joseph, B. Shutinoski, J. B. Startek, A. M. Gamero, K. L. Mossman, S. Sad, Type-I interferon signaling through ISGF3 complex is required for sustained Rip3 activation and necroptosis in macrophages. Proc. Natl. Acad. Sci. U.S.A. 111, E3206–E3213 (2014).
32. S. Davidson, S. Crotta, T. M. McCabe, A. Wack, Pathogenic potential of interferon ab in acute influenza infection. Nat. Commun. 5, 3864 (2014).
33. S. Nogusa, R. J. Thapa, C. P. Dillon, S. Liedmann, T. H. Oguin III, J. P. Ingram, D. A. Rodriguez, R. Kosoff, S. Sharma, O. Sturm, K. Verbist, P. J. Gough, J. Bertin, B. M. Hartmann, S. C. Sealfon, W. J. Kaiser, E. S. Mocarski, C. B. López, P. G. Thomas, A. Oberst, D. R. Green, S. Balachandran, RIPK3 activates parallel pathways of MLKL-driven necroptosis and FADD-mediated apoptosis to protect against influenza A virus. Cell Host Microbe 20, 13–24 (2016).
34. J. Pothlichet, I. Meunier, B. K. Davis, J. P.-Y. Ting, E. Skamene, V. von Messling, S. M. Vidal, Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLOS Pathog. 9, e1003256 (2013).
35. J. L. McAuley, M. D. Tate, C. J. MacKenzie-Kludas, A. Pinar, W. Zeng, A. Stutz, E. Latz, L. E. Brown, A. Mansell, Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLOS Pathog. 9, e1003392 (2013).
36. A. Chakrabarti, S. Banerjee, L. Franchi, Y.-M. Loo, M. Gale Jr., G. Núñez, R. H. Silverman, RNase L activates the NLRP3 inflammasome during viral infections. Cell Host Microbe 17, 466–477 (2015).
37. W. Chen, P. A. Calvo, D. Malide, J. Gibbs, U. Schubert, I. Bacik, S. Basta, R. O’Neill, J. Schickli, P. Palese, P. Henklein, J. R. Bennink, J. W. Yewdell, A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 7, 1306–1312 (2001).
38. M. D. de Jong, C. P. Simmons, T. T. Thanh, V. M. Hien, G. J. D. Smith, T. N. B. Chau, D. M. Hoang, N. V. V. Chau, T. H. Khanh, V. C. Dong, P. T. Qui, B. V. Cam, D. Q. Ha, Y. Guan, J. S. M. Peiris, N. T. Chinh, T. T. Hien, J. Farrar, Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12, 1203–1207 (2006).
39. A. R. Everitt, S. Clare, T. Pertel, S. P. John, R. S. Wash, S. E. Smith, C. R. Chin, E. M. Feeley, J. S. Sims, D. J. Adams, H. M. Wise, L. Kane, D. Goulding, P. Digard, V. Anttila, J. K. Baillie, T. S. Walsh, D. A. Hume, A. Palotie, Y. Xue, V. Colonna, C. Tyler-Smith, J. Dunning, S. B. Gordon; GenISIS Investigators; MOSAIC Investigators, R. L. Smyth, P. J. Openshaw, G. Dougan, A. L. Brass, P. Kellam, IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484, 519–523 (2012).
40. M. Brandes, F. Klauschen, S. Kuchen, R. N. Germain, A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154, 197–212 (2013).
41. J. C. Kash, T. M. Tumpey, S. C. Proll, V. Carter, O. Perwitasari, M. J. Thomas, C. F. Basler, P. Palese, J. K. Taubenberger, A. García-Sastre, D. E. Swayne, M. G. Katze, Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443, 578–581 (2006).
42. S. Li, L. Wang, M. Berman, Y. Y. Kong, M. E. Dorf, Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 35, 426–440 (2011).
43. T. H. Pham, K. M. Kwon, Y.-E. Kim, K. K. Kim, J.-H. Ahn, DNA sensing-independent inhibition of herpes simplex virus 1 replication by DAI/ZBP1. J. Virol. 87, 3076–3086 (2013).
44. V. R. DeFilippis, D. Alvarado, T. Sali, S. Rothenburg, K. Früh, Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J. Virol. 84, 585–598 (2010).
45. W. J. Kaiser, J. W. Upton, A. B. Long, D. Livingston-Rosanoff, L. P. Daley-Bauer, R. Hakem, T. Caspary, E. S. Mocarski, RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471, 368–372 (2011).
46. L complex inhibits RIPK3-dependent necrosis. Nature 471, 363–367 (2011).
47. J. M. Murphy, P. E. Czabotar, J. M. Hildebrand, I. S. Lucet, J.-G. Zhang, S. Alvarez-Diaz, R. Lewis, N. Lalaoui, D. Metcalf, A. I. Webb, S. N. Young, L. N. Varghese, G. M. Tannahill, E. C. Hatchell, I. J. Majewski, T. Okamoto, R. C. J. Dobson, D. J. Hilton, J. J. Babon, N. A. Nicola, A. Strasser, J. Silke, W. S. Alexander, The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39, 443–453 (2013).
48. N.-J. Chen, I. I. C. Chio, W.-J. Lin, G. Duncan, H. Chau, D. Katz, H.-L. Huang, K. A. Pike, Z. Hao, Y.-W. Su, K. Yamamoto, R. F. de Pooter, J. C. Zúñiga-Pflücker, A. Wakeham, W.-C. Yeh, T. W. Mak, Beyond tumor necrosis factor receptor: TRADD signaling in toll-like receptors. Proc. Natl. Acad. Sci. U.S.A. 105, 12429–12434 (2008).
49. N. Kayagaki, I. B. Stowe, B. L. Lee, K. O’Rourke, K. Anderson, S. Warming, T. Cuellar, B. Haley, M. Roose-Girma, Q. T. Phung, P. S. Liu, J. R. Lill, H. Li, J. Wu, S. Kummerfeld, J. Zhang, W. P. Lee, S. J. Snipas, G. S. Salvesen, L. X. Morris, L. Fitzgerald, Y. Zhang, E. M. Bertram, C. C. Goodnow, V. M. Dixit, Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526, 666–671 (2015).