PB1-F2 peptide derived from avian influenza A virus H7N9 induces inflammation via activation of the NLRP3 inflammasome

Journal of Biological Chemistry

Volumn 292, Issue 3, 2017, Pages 826-836

  Pinar, Anita ^a,b   Dowling, Jennifer K ^a,b   Bitto, Natalie J ^a,b   Robertson, Avril A B ^c   Latz, Eicke ^d,e,f   Stewart, Cameron R ^g   Drummond, Grant R ^b   Cooper, Matthew A ^c   McAuley, Julie L ^h   Tate, Michelle D ^a,b   Mansell, Ashley ^a,b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY HOSPITAL BONN   (Germany)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^g CSIRO   (Australia)

^h UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; CHEMICAL ACTIVATION; PEPTIDES; VIRUSES;

AVIAN INFLUENZA A; CLINICAL INFECTION; CONTRIBUTORY FACTORS; CYTOKINE PRODUCTION; INFLUENZA A VIRUS; LUNG INFLAMMATION; PATHOPHYSIOLOGY; VIRULENCE FACTORS;

PATHOLOGY;

CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; PB1 F2 PEPTIDE; PEPTIDES AND PROTEINS; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; FUSED HETEROCYCLIC RINGS; MCC-950; NLRP3 PROTEIN, MOUSE; PEPTIDE; SULFONE; VIRAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H7N9); INFLUENZA A VIRUS (A/PUERTO RICO/8/1934(H1N1)); INFLUENZA A VIRUS (H7N9); MACROPHAGE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PERIPHERAL BLOOD MONONUCLEAR CELL; VIRUS PNEUMONIA; ANIMAL; ANTAGONISTS AND INHIBITORS; IMMUNOLOGY; INFLAMMATION; INFLUENZA A VIRUS (H1N1); MITOCHONDRION; ORTHOMYXOVIRUS INFECTION; TRANSFORMED CELL LINE;

ANIMALS; CELL LINE, TRANSFORMED; HETEROCYCLIC COMPOUNDS, 4 OR MORE RINGS; INFLAMMATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; MICE; MITOCHONDRIA; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; ORTHOMYXOVIRIDAE INFECTIONS; PEPTIDES; REACTIVE OXYGEN SPECIES; SULFONES; VIRAL PROTEINS;

EID: 85010038988     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.756379     Document Type: Article

References (30)

1. Gao, R., Cao, B., Hu, Y., Feng, Z., Wang, D., Hu, W., Chen, J., Jie, Z., Qiu, H., Xu, K., Xu, X., Lu, H., Zhu, W., Gao, Z., Xiang, N., et al. (2013) Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 368, 1888-1897
2. Normile, D. (2015) Virology: bird flu virus's promiscuity raises red flags. Science 347, 1188
3. Lam, T. T., Zhou, B., Wang, J., Chai, Y., Shen, Y., Chen, X., Ma, C., Hong, W., Chen, Y., Zhang, Y., Duan, L., Chen, P., Jiang, J., Zhang, Y., Li, L., et al. (2015) Dissemination, divergence and establishment of H7N9 influenza viruses in China. Nature 522, 102-105
4. Iwasaki, A., and Pillai, P. S. (2014) Innate immunity to influenza virus infection. Nat. Rev. Immunol. 14, 315-328
5. Ichinohe, T., Pang, I. K., and Iwasaki, A. (2010) Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 11, 404-410
6. 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., and 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
7. Ichinohe, T., Lee, H. K., Ogura, Y., Flavell, R., and Iwasaki, A. (2009) Inflammasome recognition of influenza virus is essential for adaptive immune responses. J. Exp. Med. 206, 79-87
8. Allen, I. C., Scull, M. A., Moore, C. B., Holl, E. K., McElvania-TeKippe, E., Taxman, D. J., Guthrie, E. H., Pickles, R. J., and Ting, J. P. (2009) The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30, 556-565
9. Schmitz, N., Kurrer, M., Bachmann, M. F., and Kopf, M. (2005) Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J. Virol. 79, 6441-6448
10. Szretter, K. J., Gangappa, S., Lu, X., Smith, C., Shieh, W. J., Zaki, S. R., Sambhara, S., Tumpey, T. M., and Katz, J. M. (2007) Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81, 2736-2744
11. 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., and Mansell, A. (2016) Reassessing the role of the NLRP3 inflammasome during pathogenic influenza A virus infection via temporal inhibition. Sci. Rep. 6, 27912
12. Krumbholz, A., Philipps, A., Oehring, H., Schwarzer, K., Eitner, A., Wutzler, P., and Zell, R. (2011) Current knowledge on PB1-F2 of influenza A viruses. Med. Microbiol. Immunol. 200, 69-75
13. McAuley, J. L., Tate, M. D., MacKenzie-Kludas, C. J., Pinar, A., Zeng, W., Stutz, A., Latz, E., Brown, L. E., and Mansell, A. (2013) Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog. 9, e1003392
14. McAuley, J. L., Chipuk, J. E., Boyd, K. L., Van De Velde, N., Green, D. R., and McCullers, J. A. (2010) PB1-F2 proteins from H5N1 and 20 century pandemic influenza viruses cause immunopathology. PLoS Pathog. 6, e1001014
15. McAuley, J. L., Hornung, F., Boyd, K. L., Smith, A. M., McKeon, R., Bennink, J., Yewdell, J. W., and McCullers, J. A. (2007) Expression of the 1918 influenza A virus PB1-F2 enhances the pathogenesis of viral and secondary bacterial pneumonia. Cell Host Microbe 2, 240-249
16. Alymova, I. V., Green, A. M., van de Velde, N., McAuley, J. L., Boyd, K. L., Ghoneim, H. E., and McCullers, J. A. (2011) Immunopathogenic and antibacterial effects of H3N2 influenza A virus PB1-F2 map to amino acid residues 62, 75, 79, and 82. J. Virol. 85, 12324-12333
17. Hornung, V., Bauernfeind, F., Halle, A., Samstad, E. O., Kono, H., Rock, K. L., Fitzgerald, K. A., and Latz, E. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856
18. Franklin, B. S., Bossaller, L., De Nardo, D., Ratter, J. M., Stutz, A., Engels, G., Brenker, C., Nordhoff, M., Mirandola, S. R., Al-Amoudi, A., Mangan, M. S., Zimmer, S., Monks, B. G., Fricke, M., Schmidt, R. E., et al. (2014) The adaptor ASC has extracellular and "prionoid" activities that propagate inflammation. Nat. Immunol. 15, 727-737
19. Chen, C. J., Chen, G. W., Wang, C. H., Huang, C. H., Wang, Y. C., and Shih, S. R. (2010) Differential localization and function of PB1-F2 derived from different strains of influenza A virus. J. Virol. 84, 10051-10062
20. Chen, W., Calvo, P. A., Malide, D., Gibbs, J., Schubert, U., Bacik, I., Basta, S., O'Neill, R., Schickli, J., Palese, P., Henklein, P., Bennink, J. R., and Yewdell, J. W. (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 7, 1306-1312
21. Robinson, K. M., Janes, M. S., Pehar, M., Monette, J. S., Ross, M. F., Hagen, T. M., Murphy, M. P., and Beckman, J. S. (2006) Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U.S.A. 103, 15038-15043
22. Grailer, J. J., Canning, B. A., Kalbitz, M., Haggadone, M. D., Dhond, R. M., Andjelkovic, A. V., Zetoune, F. S., and Ward, P. A. (2014) Critical role for the NLRP3 inflammasome during acute lung injury. J. Immunol. 192, 5974-5983
23. 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., et al. (2015) A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat. Med. 21, 248-255
24. Kash, J. C., and Taubenberger, J. K. (2015) The Role of viral, host, and secondary bacterial factors in influenza pathogenesis. Am. J. Pathol. 185, 1528-1536
25. Dawood, F. S., Iuliano, A. D., Reed, C., Meltzer, M. I., Shay, D. K., Cheng, P. Y., Bandaranayake, D., Breiman, R. F., Brooks, W. A., Buchy, P., Feikin, D. R., Fowler, K. B., Gordon, A., Hien, N. T., Horby, P., et al. (2012) Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect. Dis. 12, 687-695
26. Yoshizumi, T., Ichinohe, T., Sasaki, O., Otera, H., Kawabata, S., Mihara, K., and Koshiba, T. (2014) Influenza A virus protein PB1-F2 translocates into mitochondria via Tom40 channels and impairs innate immunity. Nat. Commun. 5, 4713
27. Baroja-Mazo, A., Martín-Sánchez, F., Gomez, A. I., Martínez, C. M., Amores-Iniesta, J., Compan, V., Barberà-Cremades, M., Yagüe, J., Ruiz-Ortiz, E., Antón, J., Buján, S., Couillin, I., Brough, D., Arostegui, J. I., and Pelegrín, P. (2014) The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat. Immunol. 15, 738-748
28. Yu, L., Wang, Z., Chen, Y., Ding, W., Jia, H., Chan, J. F., To, K. K., Chen, H., Yang, Y., Liang, W., Zheng, S., Yao, H., Yang, S., Cao, H., Dai, X., et al. (2013) Clinical, virological, and histopathological manifestations of fatal human infections by avian influenza A(H7N9) virus. Clin. Infect. Dis. 57, 1449-1457
29. Coleman, J. R. (2007) The PB1-F2 protein of influenza A virus: increasing pathogenicity by disrupting alveolar macrophages. Virol. J. 4, 9
30. Tate, M. D., Pickett, D. L., van Rooijen, N., Brooks, A. G., and Reading, P. C. (2010) Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol. 84, 7569-7580