Hero turned villain: NLRP3 inflammasome-induced inflammation during influenza A virus infection

Journal of Leukocyte Biology

Volumn 101, Issue 4, 2017, Pages 863-874

  Ong, James D H ^a,b   Mansell, Ashley ^a,b   Tate, Michelle D ^a,b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Disease; Lung; Pathogenesis

Indexed keywords

CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; PROTEIN M2;

BACTERIAL PNEUMONIA; IMMUNE RESPONSE; INFLAMMATION; INFLUENZA A; INFLUENZA A VIRUS; MICROFLORA; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; ANIMAL; DISEASE MODEL; HUMAN; IMMUNOLOGY; INFLUENZA; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMASOMES; INFLAMMATION; INFLUENZA A VIRUS; INFLUENZA, HUMAN; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN;

EID: 85017320353     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.4MR0616-288R     Document Type: Review

References (105)

1. Johnson, N. P., Mueller, J. (2002) Updating the accounts: global mortality of the 1918-1920 “Spanish” influenza pandemic. Bull. Hist. Med. 76, 105–115.
2. World Health Organization. (2016) Influenza at the human-animal interface: summary and assessment, 21 January to 25 February 2016. In WHO Monthly Risk Assessment Summary, World Health Organization, Geneva, Switzerland, 1–8.
3. Fry, A. M., Goswami, D., Nahar, K., Sharmin, A. T., Rahman, M., Gubareva, L., Azim, T., Bresee, J., Luby, S. P., Brooks, W. A. (2014) Efficacy of oseltamivir treatment started within 5 days of symptom onset to reduce influenza illness duration and virus shedding in an urban setting in Bangladesh: a randomised placebo-controlled trial. Lancet Infect. Dis. 14, 109–118.
4. Short, K. R., Kroeze, E. J. B. V., Fouchier, R. A. M., Kuiken, T. (2014) Pathogenesis of influenza-induced acute respiratory distress syndrome. Lancet Infect. Dis. 14, 57–69.
5. Cox, N. J., Subbarao, K. (1999) Influenza. Lancet 354, 1277–1282.
6. Bouvier, N. M., Palese, P. (2008) The biology of influenza viruses. Vaccine 26 (Suppl 4), D49–D53.
7. Schrauwen, E. J., de Graaf, M., Herfst, S., Rimmelzwaan, G. F., Osterhaus, A. D., Fouchier, R. A. (2014) Determinants of virulence of influenza A virus. Eur. J. Clin. Microbiol. Infect. Dis. 33, 479–490.
8. Cheng, V. C., To, K. K., Tse, H., Hung, I. F., Yuen, K. Y. (2012) Two years after pandemic influenza A/2009/H1N1: what have we learned? Clin. Microbiol. Rev. 25, 223–263.
9. Tate, M. D., Pickett, D. L., van Rooijen, N., Brooks, A. G., Reading, P. C. (2010) Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J. Virol. 84, 7569–7580.
10. Tate, M. D., Schilter, H. C., Brooks, A. G., Reading, P. C. (2011) Responses of mouse airway epithelial cells and alveolar macrophages to virulent and avirulent strains of influenza A virus. Viral Immunol. 24, 77–88.
11. Hao, X., Kim, T. S., Braciale, T. J. (2008) Differential response of respiratory dendritic cell subsets to influenza virus infection. J. Virol. 82, 4908–4919.
12. Nair, H., Brooks, W. A., Katz, M., Roca, A., Berkley, J. A., Madhi, S. A., Simmerman, J. M., Gordon, A., Sato, M., Howie, S., Krishnan, A., Ope, M., Lindblade, K. A., Carosone-Link, P., Lucero, M., Ochieng, W., Kamimoto, L., Dueger, E., Bhat, N., Vong, S., Theodoratou, E., Chittaganpitch, M., Chimah, O., Balmaseda, A., Buchy, P., Harris, E., Evans, V., Katayose, M., Gaur, B., O’Callaghan-Gordo, C., Goswami, D., Arvelo, W., Venter, M., Briese, T., Tokarz, R., Widdowson, M. A., Mounts, A. W., Breiman, R. F., Feikin, D. R., Klugman, K. P., Olsen, S. J., Gessner, B. D., Wright, P. F., Rudan, I., Broor, S., Simões, E. A., Campbell, H. (2011) Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet 378, 1917–1930.
13. Gill, J. R., Sheng, Z. M., Ely, S. F., Guinee, D. G., Beasley, M. B., Suh, J., Deshpande, C., Mollura, D. J., Morens, D. M., Bray, M., Travis, W. D., Taubenberger, J. K. (2010) Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch. Pathol. Lab. Med. 134, 235–243.
14. Takiyama, A., Wang, L., Tanino, M., Kimura, T., Kawagishi, N., Kunieda, Y., Katano, H., Nakajima, N., Hasegawa, H., Takagi, T., Nishihara, H., Sata, T., Tanaka, S. (2010) Sudden death of a patient with pandemic influenza (A/H1N1pdm) virus infection by acute respiratory distress syndrome. Jpn. J. Infect. Dis. 63, 72–74.
15. Brundage, J. F., Shanks, G. D. (2008) Deaths from bacterial pneumonia during 1918–19 influenza pandemic. Emerg. Infect. Dis. 14, 1193–1199.
16. Morens, D. M., Taubenberger, J. K., Fauci, A. S. (2008) Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J. Infect. Dis. 198, 962–970.
17. Hussell, T., Cavanagh, M. M. (2009) The innate immune rheostat: influence on lung inflammatory disease and secondary bacterial pneumonia. Biochem. Soc. Trans. 37, 811–813.
18. Itoh, Y., Shinya, K., Kiso, M., Watanabe, T., Sakoda, Y., Hatta, M., Muramoto, Y., Tamura, D., Sakai-Tagawa, Y., Noda, T., Sakabe, S., Imai, M., Hatta, Y., Watanabe, S., Li, C., Yamada, S., Fujii, K., Murakami, S., Imai, H., Kakugawa, S., Ito, M., Takano, R., Iwatsuki-Horimoto, K., Shimojima, M., Horimoto, T., Goto, H., Takahashi, K., Makino, A., Ishigaki, H., Nakayama, M., Okamatsu, M., Takahashi, K., Warshauer, D., Shult, P. A., Saito, R., Suzuki, H., Furuta, Y., Yamashita, M., Mitamura, K., Nakano, K., Nakamura, M., Brockman-Schneider, R., Mitamura, H., Yamazaki, M., Sugaya, N., Suresh, M., Ozawa, M., Neumann, G., Gern, J., Kida, H., Ogasawara, K., Kawaoka, Y. (2009) In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460, 1021–1025.
19. Cilloniz, C., Pantin-Jackwood, M. J., Ni, C., Goodman, A. G., Peng, X., Proll, S. C., Carter, V. S., Rosenzweig, E. R., Szretter, K. J., Katz, J. M., Korth, M. J., Swayne, D. E., Tumpey, T. M., Katze, M. G. (2010) Lethal dissemination of H5N1 influenza virus is associated with dysregulation of inflammation and lipoxin signaling in a mouse model of infection. J. Virol. 84, 7613–7624.
20. Belser, J. A., Gustin, K. M., Pearce, M. B., Maines, T. R., Zeng, H., Pappas, C., Sun, X., Carney, P. J., Villanueva, J. M., Stevens, J., Katz, J. M., Tumpey, T. M. (2013) Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature 501, 556–559.
21. Li, C., Li, C., Zhang, A. J. X., To, K. K. W., Lee, A. C. Y., Zhu, H., Wu, H. W. L., Chan, J. F. W., Chen, H., Hung, I. F. N., Li, L., Yuen, K.-Y. (2014) Avian influenza A H7N9 virus induces severe pneumonia in mice without prior adaptation and responds to a combination of zanamivir and COX-2 inhibitor. PLoS One 9, e107966.
22. Taylor, R. M. (1941) Experimental infection with influenza A virus in mice: the increase in intrapulmonary virus after inoculation and the influence of various factors thereon. J. Exp. Med. 73, 43–55.
23. Fukushi, M., Ito, T., Oka, T., Kitazawa, T., Miyoshi-Akiyama, T., Kirikae, T., Yamashita, M., Kudo, K. (2011) Serial histopathological examination of the lungs of mice infected with influenza A virus PR8 strain. PLoS One 6, e21207.
24. Allen, I. C., Scull, M. A., Moore, C. B., Holl, E. K., McElvania-TeKippe, E., Taxman, D. J., Guthrie, E. H., Pickles, R. J., Ting, J. P. Y. (2009) The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30, 556–565.
25. Schmitz, N., Kurrer, M., Bachmann, M. F., Kopf, M. (2005) Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J. Virol. 79, 6441–6448.
26. Tate, M. D., Brooks, A. G., Reading, P. C. (2011) Specific sites of N-linked glycosylation on the hemagglutinin of H1N1 subtype influenza A virus determine sensitivity to inhibitors of the innate immune system and virulence in mice. J. Immunol. 187, 1884–1894.
27. Chan, M. C., Cheung, C. Y., Chui, W. H., Tsao, S. W., Nicholls, J. M., Chan, Y. O., Chan, R. W., Long, H. T., Poon, L. L., Guan, Y., Peiris, J. S. (2005) Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir. Res. 6, 135.
28. Ocaña-Macchi, M., Bel, M., Guzylack-Piriou, L., Ruggli, N., Liniger, M., McCullough, K. C., Sakoda, Y., Isoda, N., Matrosovich, M., Summerfield, A. (2009) Hemagglutinin-dependent tropism of H5N1 avian influenza virus for human endothelial cells. J. Virol. 83, 12947–12955.
29. Dash, P., Thomas, P. G. (2015) Host detection and the stealthy phenotype in influenza virus infection. Curr. Top. Microbiol. Immunol. 386, 121–147.
30. Tan, A. C., Mifsud, E. J., Zeng, W., Edenborough, K., McVernon, J., Brown, L. E., Jackson, D. C. (2012) Intranasal administration of the TLR2 agonist Pam2Cys provides rapid protection against influenza in mice. Mol. Pharm. 9, 2710–2718.
31. Shinya, K., Ito, M., Makino, A., Tanaka, M., Miyake, K., Eisfeld, A. J., Kawaoka, Y. (2012) The TLR4-TRIF pathway protects against H5N1 influenza virus infection. J. Virol. 86, 19–24.
32. Shirey, K. A., Lai, W., Scott, A. J., Lipsky, M., Mistry, P., Pletneva, L. M., Karp, C. L., McAlees, J., Gioannini, T. L., Weiss, J., Chen, W. H., Ernst, R. K., Rossignol, D. P., Gusovsky, F., Blanco, J. C., Vogel, S. N. (2013) The TLR4 antagonist Eritoran protects mice from lethal influenza infection. Nature 497, 498–502.
33. Jeisy-Scott, V., Davis, W. G., Patel, J. R., Bowzard, J. B., Shieh, W.-J., Zaki, S. R., Katz, J. M., Sambhara, S. (2011) Increased MDSC accumulation and Th2 biased response to influenza A virus infection in the absence of TLR7 in mice. PLoS One 6, e25242.
34. Leung, Y. H., Nicholls, J. M., Ho, C. K., Sia, S. F., Mok, C. K., Valkenburg, S. A., Cheung, P., Hui, K. P., Chan, R. W., Guan, Y., Akira, S., Peiris, J. S. (2014) Highly pathogenic avian influenza A H5N1 and pandemic H1N1 virus infections have different phenotypes in Toll-like receptor 3 knockout mice. J. Gen. Virol. 95, 1870–1879.
35. 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., Akira, S., Akira, S. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101–105.
36. Loo, Y. M., Fornek, J., Crochet, N., Bajwa, G., Perwitasari, O., Martinez-Sobrido, L., Akira, S., Gill, M. A., García-Sastre, A., Katze, M. G., Gale, M. Jr. (2008) Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82, 335–345.
37. Sládková, T., Kostolanský, F. (2006) The role of cytokines in the immune response to influenza A virus infection. Acta Virol. 50, 151–162.
38. Lauder, S. N., Jones, E., Smart, K., Bloom, A., Williams, A. S., Hindley, J. P., Ondondo, B., Taylor, P. R., Clement, M., Fielding, C., Godkin, A. J., Jones, S. A., Gallimore, A. M. (2013) Interleukin-6 limits influenza-induced inflammation and protects against fatal lung pathology. Eur. J. Immunol. 43, 2613–2625.
39. Dienz, O., Rud, J. G., Eaton, S. M., Lanthier, P. A., Burg, E., Drew, A., Bunn, J., Suratt, B. T., Haynes, L., Rincon, M. (2012) Essential role of IL-6 in protection against H1N1 influenza virus by promoting neutrophil survival in the lung. Mucosal Immunol. 5, 258–266.
40. Tisoncik, J. R., Korth, M. J., Simmons, C. P., Farrar, J., Martin, T. R., Katze, M. G. (2012) Into the eye of the cytokine storm. Microbiol. Mol. Biol. Rev. 76, 16–32.
41. Chiu, C., Ellebedy, A. H., Wrammert, J., Ahmed, R. (2015) B Cell responses to influenza infection and vaccination. Curr. Top. Microbiol. Immunol. 386, 381–398.
42. Hufford, M. M., Kim, T. S., Sun, J., Braciale, T. J. (2015) The effector T cell response to influenza infection. Curr. Top. Microbiol. Immunol. 386, 423–455.
43. Broz, P., Dixit, V. M. (2016) Inflammasomes: mechanism of assembly, regulation and signalling. Nat. Rev. Immunol. 16, 407–420.
44. De Nardo, D., De Nardo, C. M., Latz, E. (2014) New insights into mechanisms controlling the NLRP3 inflammasome and its role in lung disease. Am. J. Pathol. 184, 42–54.
45. Lamkanfi, M., Dixit, V. M. (2014) Mechanisms and functions of inflammasomes. Cell 157, 1013–1022.
46. Miller, D. K., Ayala, J. M., Egger, L. A., Raju, S. M., Yamin, T. T., Ding, G. J., Gaffney, E. P., Howard, A. D., Palyha, O. C., Rolando, A. M. (1993) Purification and characterization of active human interleukin-1 beta-converting enzyme from THP.1 monocytic cells. J. Biol. Chem. 268, 18062–18069.
47. Vince, J. E., Silke, J. (2016) The intersection of cell death and inflammasome activation. Cell. Mol. Life Sci. 73, 2349–2367.
48. Sutterwala, F. S., Haasken, S., Cassel, S. L. (2014) Mechanism of NLRP3 inflammasome activation. Ann. N. Y. Acad. Sci. 1319, 82–95.
49. Latz, E., Xiao, T. S., Stutz, A. (2013) Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13, 397–411.
50. McAuley, J. L., Tate, M. D., MacKenzie-Kludas, C. J., Pinar, A., Zeng, W., Stutz, A., Latz, E., Brown, L. E., Mansell, A. (2013) Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog. 9, e1003392.
51. Stout-Delgado, H. W., Vaughan, S. E., Shirali, A. C., Jaramillo, R. J., Harrod, K. S. (2012) Impaired NLRP3 inflammasome function in elderly mice during influenza infection is rescued by treatment with nigericin. J. Immunol. 188, 2815–2824.
52. Ichinohe, T., Pang, I. K., Iwasaki, A. (2010) Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 11, 404–410.
53. Fernandez, M. V., Miller, E., Krammer, F., Gopal, R., Greenbaum, B. D., Bhardwaj, N. (2016) Ion efflux and influenza infection trigger NLRP3 inflammasome signaling in human dendritic cells. J. Leukoc. Biol. 99, 723–734.
54. Ioannidis, L. J., Verity, E. E., Crawford, S., Rockman, S. P., Brown, L. E. (2012) Abortive replication of influenza virus in mouse dendritic cells. J. Virol. 86, 5922–5925.
55. Kanneganti, T. D., Body-Malapel, M., Amer, A., Park, J. H., Whitfield, J., Franchi, L., Taraporewala, Z. F., Miller, D., Patton, J. T., Inohara, N., Núñez, G. (2006) 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.
56. Ichinohe, T., Lee, H. K., Ogura, Y., Flavell, R., Iwasaki, A. (2009) Inflammasome recognition of influenza virus is essential for adaptive immune responses. J. Exp. Med. 206, 79–87.
57. Thomas, P. G., Dash, P., Aldridge, J. R., Jr.,Ellebedy, A. H., Reynolds, C., Funk, A. J., Martin, W. J., Lamkanfi, M., Webby, R. J., Boyd, K. L., Doherty, P. C., Kanneganti, T. D. (2009) The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30, 566–575.
58. Pirhonen, J., Sareneva, T., Kurimoto, M., Julkunen, I., Matikainen, S. (1999) Virus infection activates IL-1 beta and IL-18 production in human macrophages by a caspase-1-dependent pathway. J. Immunol. 162, 7322–7329.
59. Pirhonen, J., Sareneva, T., Julkunen, I., Matikainen, S. (2001) Virus infection induces proteolytic processing of IL-18 in human macrophages via caspase-1 and caspase-3 activation. Eur. J. Immunol. 31, 726–733.
60. Bauer, R. N., Brighton, L. E., Mueller, L., Xiang, Z., Rager, J. E., Fry, R. C., Peden, D. B., Jaspers, I. (2012) Influenza enhances caspase-1 in bronchial epithelial cells from asthmatic volunteers and is associated with pathogenesis. J. Allergy Clin. Immunol. 130, 958–967.e14.
61. Pothlichet, J., Meunier, I., Davis, B. K., Ting, J. P. Y., Skamene, E., von Messling, V., Vidal, S. M. (2013) Type I IFN triggers RIG-I/TLR3/ NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog. 9, e1003256.
62. Tiwari, N., Khare, D., Verma, S., Dhole, T. N. (2014) Potential role of NLRP3 inflammasome to combat pandemic 2009 (PH1N1) influenza virus infection in human lung a549 epithelial cells. Int. J. Pharm. Sci. Rev. Res. 27, 304–309.
63. Tzeng, T.-C., Schattgen, S., Monks, B., Wang, D., Cerny, A., Latz, E., Fitzgerald, K., Golenbock, D. T. (2016) A fluorescent reporter mouse for inflammasome assembly demonstrates an important role for cell-bound and free ASC specks during in vivo infection. Cell Reports 16, 571–582.
64. Tate, M. D., Ong, J. D., Dowling, J. K., McAuley, J. L., Robertson, A. B., Latz, E., Drummond, G. R., Cooper, M. A., Hertzog, P. J., Mansell, A. (2016) Reassessing the role of the NLRP3 inflammasome during pathogenic influenza A virus infection via temporal inhibition. Sci. Rep. 6, 27912.
65. Yu, M., Zhang, K., Qi, W., Huang, Z., Ye, J., Ma, Y., Liao, M., Ning, Z. (2014) Expression pattern of NLRP3 and its related cytokines in the lung and brain of avian influenza virus H9N2 infected BALB/c mice. Virol. J. 11, 229.
66. Lietzén, N., Ohman, T., Rintahaka, J., Julkunen, I., Aittokallio, T., Matikainen, S., Nyman, T. A. (2011) Quantitative subcellular proteome and secretome profiling of influenza A virus-infected human primary macrophages. PLoS Pathog. 7, e1001340.
67. Ichinohe, T., Yamazaki, T., Koshiba, T., Yanagi, Y. (2013) Mitochondrial protein mitofusin 2 is required for NLRP3 inflammasome activation after RNA virus infection. Proc. Natl. Acad. Sci. USA 110, 17963–17968.
68. Yoshizumi, T., Ichinohe, T., Sasaki, O., Otera, H., Kawabata, S., Mihara, K., Koshiba, T. (2014) Influenza A virus protein PB1-F2 translocates into mitochondria via Tom40 channels and impairs innate immunity. Nat. Commun. 5, 4713.
69. Lupfer, C., Thomas, P. G., Anand, P. K., Vogel, P., Milasta, S., Martinez, J., Huang, G., Green, M., Kundu, M., Chi, H., Xavier, R. J., Green, D. R., Lamkanfi, M., Dinarello, C. A., Doherty, P. C., Kanneganti, T. D. (2013) Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat. Immunol. 14, 480–488.
70. Chakrabarti, A., Banerjee, S., Franchi, L., Loo, Y. M., Gale, M., Jr., Núñez, G., Silverman, R. H. (2015) RNase L activates the NLRP3 inflammasome during viral infections. Cell Host Microbe 17, 466–477.
71. Pielak, R. M., Chou, J. J. (2011) Influenza M2 proton channels. Biochim. Biophys. Acta 1808, 522–529.
72. Friesenhagen, J., Boergeling, Y., Hrincius, E., Ludwig, S., Roth, J., Viemann, D. (2012) Highly pathogenic avian influenza viruses inhibit effective immune responses of human blood-derived macrophages. J. Leukoc. Biol. 92, 11–20.
73. Chen, C.-J., Chen, G.-W., Wang, C.-H., Huang, C.-H., Wang, Y.-C., Shih, S.-R. (2010) Differential localization and function of PB1-F2 derived from different strains of influenza A virus. J. Virol. 84, 10051–10062.
74. Zell, R., Krumbholz, A., Eitner, A., Krieg, R., Halbhuber, K. J., Wutzler, P. (2007) Prevalence of PB1-F2 of influenza A viruses. J. Gen. Virol. 88, 536–546.
75. McAuley, J. L., Chipuk, J. E., Boyd, K. L., Van De Velde, N., Green, D. R., McCullers, J. A. (2010) PB1-F2 proteins from H5N1 and 20 century pandemic influenza viruses cause immunopathology. PLoS Pathog. 6, e1001014.
76. Chevalier, C., Al Bazzal, A., Vidic, J., Février, V., Bourdieu, C., Bouguyon, E., Le Goffic, R., Vautherot, J.-F., Bernard, J., Moudjou, M., Noinville, S., Chich, J.-F., Da Costa, B., Rezaei, H., Delmas, B. (2010) PB1-F2 influenza A virus protein adopts a β-sheet conformation and forms amyloid fibers in membrane environments. J. Biol. Chem. 285, 13233–13243.
77. Vidic, J., Richard, C. A., Péchoux, C., Da Costa, B., Bertho, N., Mazerat, S., Delmas, B., Chevalier, C. (2016) Amyloid assemblies of influenza A virus PB1-F2 protein damage membrane and induce cytotoxicity. J. Biol. Chem. 291, 739–751.
78. Lee, P. H., Bird, N., MacKenzie-Kludas, C., Mansell, A., Kedzierska, K., Brown, L., McAuley, J. (2016) Induction of memory cytotoxic T cells to influenza A virus and subsequent viral clearance is not modulated by PB1-F2-dependent inflammasome activation. Immunol. Cell Biol. 94, 439–446.
79. Huang, C. H., Chen, C. J., Yen, C. T., Yu, C. P., Huang, P. N., Kuo, R. L., Lin, S. J., Chang, C. K., Shih, S. R. (2013) Caspase-1 deficient mice are more susceptible to influenza A virus infection with PA variation. J. Infect. Dis. 208, 1898–1905.
80. Coll, R. C., Robertson, A. A., Chae, J. J., Higgins, S. C., Muñoz-Planillo, R., Inserra, M. C., Vetter, I., Dungan, L. S., Monks, B. G., Stutz, A., Croker, D. E., Butler, M. S., Haneklaus, M., Sutton, C. E., Núñez, G., Latz, E., Kastner, D. L., Mills, K. H., Masters, S. L., Schroder, K., Cooper, M. A., O’Neill, L. A. (2015) A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat. Med. 21, 248–255.
81. Kochs, G., García-Sastre, A., Martínez-Sobrido, L. (2007) Multiple anti-interferon actions of the influenza A virus NS1 protein. J. Virol. 81, 7011–7021.
82. Stasakova, J., Ferko, B., Kittel, C., Sereinig, S., Romanova, J., Katinger, H., Egorov, A. (2005) Influenza A mutant viruses with altered NS1 protein function provoke caspase-1 activation in primary human macrophages, resulting in fast apoptosis and release of high levels of interleukins 1β and 18. J. Gen. Virol. 86, 185–195.
83. Cheong, W. C., Kang, H. R., Yoon, H., Kang, S. J., Ting, J. P., Song, M. J. (2015) Influenza A virus NS1 protein inhibits the NLRP3 inflammasome. PLoS One 10, e0126456.
84. Moriyama, M., Chen, I. Y., Kawaguchi, A., Koshiba, T., Nagata, K., Takeyama, H., Hasegawa, H., Ichinohe, T. (2016) The RNA- and TRIM25-binding domains of influenza virus NS1 protein are essential for suppression of NLRP3 inflammasome-mediated interleukin-1β secretion. J. Virol. 90, 4105–4114.
85. Ichinohe, T., Pang, I. K., Kumamoto, Y., Peaper, D. R., Ho, J. H., Murray, T. S., Iwasaki, A. (2011) Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 108, 5354–5359.
86. Palomo, J., Dietrich, D., Martin, P., Palmer, G., Gabay, C. (2015) The interleukin (IL)-1 cytokine family—balance between agonists and antagonists in inflammatory diseases. Cytokine 76, 25–37.
87. Roux, J., Kawakatsu, H., Gartland, B., Pespeni, M., Sheppard, D., Matthay, M. A., Canessa, C. M., Pittet, J. F. (2005) Interleukin-1β decreases expression of the epithelial sodium channel alpha-subunit in alveolar epithelial cells via a p38 MAPK-dependent signaling pathway. J. Biol. Chem. 280, 18579–18589.
88. Dolinay, T., Kim, Y. S., Howrylak, J., Hunninghake, G. M., An, C. H., Fredenburgh, L., Massaro, A. F., Rogers, A., Gazourian, L., Nakahira, K., Haspel, J. A., Landazury, R., Eppanapally, S., Christie, J. D., Meyer, N. J., Ware, L. B., Christiani, D. C., Ryter, S. W., Baron, R. M., Choi, A. M. (2012) Inflammasome-regulated cytokines are critical mediators of acute lung injury. Am. J. Respir. Crit. Care Med. 185, 1225–1234.
89. Novick, D., Kim, S., Kaplanski, G., Dinarello, C. A. (2013) Interleukin-18, more than a Th1 cytokine. Semin. Immunol. 25, 439–448.
90. Guo, J., Huang, F., Liu, J., Chen, Y., Wang, W., Cao, B., Zou, Z., Liu, S., Pan, J., Bao, C., Zeng, M., Xiao, H., Gao, H., Yang, S., Zhao, Y., Liu, Q., Zhou, H., Zhu, J., Liu, X., Liang, W., Yang, Y., Zheng, S., Yang, J., Diao, H., Su, K., Shao, L., Cao, H., Wu, Y., Zhao, M., Tan, S., Li, H., Xu, X., Wang, C., Zhang, J., Wang, L., Wang, J., Xu, J., Li, D., Zhong, N., Cao, X., Gao, G. F., Li, L., Jiang, C. (2015) The serum profile of hypercytokinemia factors identified in H7N9-infected patients can predict fatal outcomes. Sci. Rep. 5, 10942.
91. Yang, Z. F., Mok, C. K., Liu, X. Q., Li, X. B., He, J. F., Guan, W. D., Xu, Y. H., Pan, W. Q., Chen, L. Y., Lin, Y. P., Wu, S. G., Pan, S. H., Huang, J. C., Ding, G. Y., Zheng, K., Ke, C. W., Lin, J. Y., Zhang, Y. H., Lee, H. H., Liu, W. K., Yang, C. G., Zhou, R., Peiris, J. S., Li, Y. M., Chen, R. C., Chen, L., Zhong, N. S. (2015) Clinical, virological and immunological features from patients infected with re-emergent avian-origin human H7N9 influenza disease of varying severity in Guangdong province. PLoS One 10, e0117846.
92. Sun, G., Ota, C., Kitaoka, S., Chiba, Y., Takayanagi, M., Kitamura, T., Yamamoto, K., Fujie, H., Mikami, H., Uematsu, M., Hino-Fukuyo, N., Munakata, M., Kure, S., Haginoya, K. (2015) Elevated serum levels of neutrophil elastase in patients with influenza virus-associated encephalopathy. J. Neurol. Sci. 349, 190–195.
93. Liu, Y., Li, S., Zhang, G., Nie, G., Meng, Z., Mao, D., Chen, C., Chen, X., Zhou, B., Zeng, G. (2013) Genetic variants in IL1A and IL1B contribute to the susceptibility to 2009 pandemic H1N1 influenza A virus. BMC Immunol. 14, 37.
94. Morales-García, G., Falfán-Valencia, R., García-Ramírez, R. A., Camarena, Á., Ramirez-Venegas, A., Castillejos-López, M., Pérez-Rodríguez, M., González-Bonilla, C., Grajales-Muñíz, C., Borja-Aburto, V., Mejía-Aranguré, J. M. (2012) Pandemic influenza A/H1N1 virus infection and TNF, LTA, IL1B, IL6, IL8, and CCL polymorphisms in Mexican population: a case-control study. BMC Infect. Dis. 12, 299.
95. García-Ramírez, R. A., Ramírez-Venegas, A., Quintana-Carrillo, R., Camarena, A. E., Falfán-Valencia, R., Mejía-Aranguré, J. M. (2015) TNF, IL6, and IL1B polymorphisms are associated with severe influenza A (H1N1) virus infection in the Mexican population. PLoS One 10, e0144832.
96. Belisle, S. E., Tisoncik, J. R., Korth, M. J., Carter, V. S., Proll, S. C., Swayne, D. E., Pantin-Jackwood, M., Tumpey, T. M., Katze, M. G. (2010) Genomic profiling of tumor necrosis factor alpha (TNF-alpha) receptor and interleukin-1 receptor knockout mice reveals a link between TNF-alpha signaling and increased severity of 1918 pandemic influenza virus infection. J. Virol. 84, 12576–12588.
97. Szretter, K. J., Gangappa, S., Lu, X., Smith, C., Shieh, W. J., Zaki, S. R., Sambhara, S., Tumpey, T. M., Katz, J. M. (2007) Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81, 2736–2744.
98. Pang, I. K., Ichinohe, T., Iwasaki, A. (2013) IL-1R signaling in dendritic cells replaces pattern-recognition receptors in promoting CD8⁺ T cell responses to influenza A virus. Nat. Immunol. 14, 246–253.
99. Liu, B., Mori, I., Hossain, M. J., Dong, L., Takeda, K., Kimura, Y. (2004) Interleukin-18 improves the early defence system against influenza virus infection by augmenting natural killer cell-mediated cytotoxicity. J. Gen. Virol. 85, 423–428.
100. +T cells. Eur. J. Immunol. 37, 368–375.
101. Zhang, Y., Wang, Y., Gilmore, X., Xu, K., Mbawuike, I. N. (2001) Independent and synergistic effects of interleukin-18 and interleukin-12 in augmenting cytotoxic T lymphocyte responses and IFN-gamma production in aging. J. Interferon Cytokine Res. 21, 843–850.
102. Van Der Sluijs, K. F., Van Elden, L. J. R., Arens, R., Nijhuis, M., Schuurman, R., Florquin, S., Kwakkel, J., Akira, S., Jansen, H. M., Lutter, R., Van Der Polls, T. (2005) Enhanced viral clearance in interleukin-18 gene-deficient mice after pulmonary infection with influenza A virus. Immunology 114, 112–120.
103. Campigotto, A., Mubareka, S. (2015) Influenza-associated bacterial pneumonia; managing and controlling infection on two fronts. Expert Rev. Anti Infect. Ther. 13, 55–68.
104. Smith, M. W., Schmidt, J. E., Rehg, J. E., Orihuela, C. J., McCullers, J. A. (2007) Induction of pro- and anti-inflammatory molecules in a mouse model of pneumococcal pneumonia after influenza. Comp. Med. 57, 82–89.
105. Robinson, K. M., Choi, S. M., McHugh, K. J., Mandalapu, S., Enelow, R. I., Kolls, J. K., Alcorn, J. F. (2013) Influenza A exacerbates Staphylococcus aureus pneumonia by attenuating IL-1β production in mice. J. Immunol. 191, 5153–5159.