Influenza virus protein PB1-F2 interacts with CALCOCO2 (NDP52) to modulate innate immune response

Journal of General Virology

Volumn 98, Issue 6, 2017, Pages 1196-1208

  Leymarie, Olivier ^a   Meyer, Léa ^a   Tafforeau, Lionel ^b,e   Lotteau, Vincent ^c,d   Da Costa, Bruno ^a   Delmas, Bernard ^a   Chevalier, Christophe ^a   Goffic, Ronan Le ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b INSERM   (France)

^c CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^d UNIVERSITÉ DE LYON   (France)

^e UNIVERSITY OF MONS   (Belgium)

Author keywords

CALCOCO2; Influenza virus; Innate immune response; PB1 F2

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BETA INTERFERON; CALCIUM BINDING AND COILED COIL DOMAIN 2; FIBRONECTIN; FIBRONECTIN 1; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLUENZA VIRUS PROTEIN PB1 F2; INTERFERON; INTERFERON TYPE 1; PROTEASOME 26S SUBUNIT ATPASE 3; PROTEIN; SMALL INTERFERING RNA; TBK1 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VIRAL PROTEIN; NUCLEAR DOT PROTEIN 52, HUMAN; NUCLEAR PROTEIN; PB1-F2 PROTEIN, INFLUENZA A VIRUS; PROTEIN BINDING; VIRULENCE FACTOR;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA BINDING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNODETECTION; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INNATE IMMUNITY; INTERFERON PRODUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; VIRUS TITRATION; WESTERN BLOTTING; BIOLOGY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLUENZA A VIRUS; KINETICS; METABOLISM; PATHOGENICITY; PROTEIN ANALYSIS; TWO HYBRID SYSTEM;

COMPUTATIONAL BIOLOGY; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INFLUENZA A VIRUS; KINETICS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; SURFACE PLASMON RESONANCE; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL PROTEINS; VIRULENCE FACTORS;

EID: 85023597654     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000782     Document Type: Article

References (58)

1. Taubenberger JK, Morens DM. The pathology of influenza virus infections. Annu Rev Pathol 2008;3:499-522.
2. Hale BG, Randall RE, Ortín J, Jackson D. The multifunctional NS1 protein of influenza A viruses. J Gen Virol 2008;89:2359-2376.
3. Krumbholz A, Philipps A, Oehring H, Schwarzer K, Eitner A et al. Current knowledge on PB1-F2 of influenza A viruses. Med Microbiol Immunol 2011;200:69-75.
4. Jagger BW, Wise HM, Kash JC, Walters KA, Wills NM et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 2012;337:199-204.
5. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U et al. A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 2001;7:1306-1312.
6. Zamarin D, Ortigoza MB, Palese P. Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J Virol 2006;80:7976-7983.
7. Mazur I, Anhlan D, Mitzner D, Wixler L, Schubert U et al. The proapoptotic influenza A virus protein PB1-F2 regulates viral polymerase activity by interaction with the PB1 protein. Cell Microbiol 2008;10:1140-1152.
8. Iverson AR, Boyd KL, Mcauley JL, Plano LR, Hart ME et al. Influenza virus primes mice for pneumonia from Staphylococcus aureus. J Infect Dis 2011;203:880-888.
9. McAuley JL, Hornung F, Boyd KL, Smith AM, Mckeon R et al. Expression of the 1918 influenza A virus PB1-F2 enhances the pathogenesis of viral and secondary bacterial pneumonia. Cell Host Microbe 2007;2:240-249.
10. Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog 2007;3:1414-1421.
11. Le Goffic R, Leymarie O, Chevalier C, Rebours E, da Costa B et al. Transcriptomic analysis of host immune and cell death responses associated with the influenza A virus PB1-F2 protein. PLoS Pathog 2011;7:e1002202.
12. McAuley JL, Chipuk JE, Boyd KL, van de Velde N, Green DR et al. PB1-F2 proteins from H5N1 and 20th century pandemic influenza viruses cause immunopathology. PLoS Pathog 2010;6:e1001014.
13. Le Goffic R, Bouguyon E, Chevalier C, Vidic J, da Costa B et al. Influenza A virus protein PB1-F2 exacerbates IFN-β expression of human respiratory epithelial cells. J Immunol 2010;185:4812-4823.
14. Alymova IV, Green AM, van de Velde N, Mcauley JL, Boyd KL et al. Immunopathogenic and antibacterial effects of H3N2 influenza A virus PB1-F2 map to amino acid residues 62, 75, 79, and 82. J Virol 2011;85:12324-12333.
15. Chen CJ, Chen GW, Wang CH, Huang CH, Wang YC et al. Differential localization and function of PB1-F2 derived from different strains of influenza A virus. J Virol 2010;84:10051-10062.
16. McAuley JL, Zhang K, McCullers JA. The effects of influenza A virus PB1-F2 protein on polymerase activity are strain specific and do not impact pathogenesis. J Virol 2010;84:558-564.
17. Conenello GM, Tisoncik JR, Rosenzweig E, Varga ZT, Palese P et al. A single N66S mutation in the PB1-F2 protein of influenza A virus increases virulence by inhibiting the early interferon response in vivo. J Virol 2011;85:652-662.
18. Leymarie O, Jouvion G, Hervé PL, Chevalier C, Lorin V et al. Kinetic characterization of PB1-F2-mediated immunopathology during highly pathogenic avian H5N1 influenza virus infection. PLoS One 2013;8:e57894.
19. Schmolke M, Manicassamy B, Pena L, Sutton T, Hai R et al. Differential contribution of PB1-F2 to the virulence of highly pathogenic H5N1 influenza A virus in mammalian and avian species. PLoS Pathog 2011;7:e1002186.
20. Varga ZT, Ramos I, Hai R, Schmolke M, García-Sastre A et al. The influenza virus protein PB1-F2 inhibits the induction of type I interferon at the level of the MAVS adaptor protein. PLoS Pathog 2011;7:e1002067.
21. Zamarin D, García-Sastre A, Xiao X, Wang R, Palese P. Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog 2005;1:e4.
22. Varga ZT, Grant A, Manicassamy B, Palese P. Influenza virus protein PB1-F2 inhibits the induction of type I interferon by binding to MAVS and decreasing mitochondrial membrane potential. J Virol 2012;86:8359-8366.
23. McAuley JL, Tate MD, Mackenzie-Kludas CJ, Pinar A, Zeng W et al. Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog 2013;9:e1003392.
24. Jaworska J, Coulombe F, Downey J, Tzelepis F, Shalaby K et al. NLRX1 prevents mitochondrial induced apoptosis and enhances macrophage antiviral immunity by interacting with influenza virus PB1-F2 protein. Proc Natl Acad Sci USA 2014;111:E2110-E2119.
25. Reis AL, Mccauley JW. The influenza virus protein PB1-F2 interacts with IKKb and modulates NF-κB signalling. PLoS One 2013;8:e63852.
26. Boyle KB, Randow F. The role of ‘eat-me’ signals and autophagy cargo receptors in innate immunity. Curr Opin Microbiol 2013;16:339-348.
27. Gibbs JS, Malide D, Hornung F, Bennink JR, Yewdell JW. The influenza A virus PB1-F2 protein targets the inner mitochondrial membrane via a predicted basic amphipathic helix that disrupts mitochondrial function. J Virol 2003;77:7214-7224.
28. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C et al. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009;37:D412-D416.
29. Jacobs JL, Coyne CB. Mechanisms of MAVS regulation at the mitochondrial membrane. J Mol Biol 2013;425:5009-5019.
30. Arthur JS, Ley SC. Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol 2013;13:679-692.
31. Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 2009;10:1215-1221.
32. Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E et al. Cutting edge: influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J Immunol 2007;178:3368-3372.
33. Marjuki H, Scholtissek C, Franks J, Negovetich NJ, Aldridge JR et al. Three amino acid changes in PB1-F2 of highly pathogenic H5N1 avian influenza virus affect pathogenicity in mallard ducks. Arch Virol 2010;155:925-934.
34. Dudek SE, Wixler L, Nordhoff C, Nordmann A, Anhlan D et al. The influenza virus PB1-F2 protein has interferon antagonistic activity. Biol Chem 2011;392:1135-1144.
35. Yoshizumi T, Ichinohe T, Sasaki O, Otera H, Kawabata S et al. Influenza A virus protein PB1-F2 translocates into mitochondria via Tom40 channels and impairs innate immunity. Nat Commun 2014;5:4713.
36. Truax AD, Koues OI, Mentel MK, Greer SF. The 19S ATPase S6a (S6'/TBP1) regulates the transcription initiation of class II transactivator. J Mol Biol 2010;395:254-269.
37. Ito M, Iwasaki M, Takeda M, Nakamura T, Yanagi Y et al. Measles virus nonstructural C protein modulates viral RNA polymerase activity by interacting with host protein SHCBP1. J Virol 2013;87:9633-9642.
38. de Chassey B, Navratil V, Tafforeau L, Hiet MS, Aublin-Gex A et al. Hepatitis C virus infection protein network. Mol Syst Biol 2008;4:230.
39. Bouraï M, Lucas-Hourani M, Gad HH, Drosten C, Jacob Y et al. Mapping of chikungunya virus interactions with host proteins identified nsP2 as a highly connected viral component. J Virol 2012;86:3121-3134.
40. Judith D, Mostowy S, Bourai M, Gangneux N, Lelek M et al. Species- specific impact of the autophagy machinery on chikungunya virus infection. EMBO Rep 2013;14:534-544.
41. Li S, Wang L, Berman M, Kong YY, Dorf ME. Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 2011;35:426-440.
42. Sternsdorf T, Jensen K, Züchner D, Will H. Cellular localization, expression, and structure of the nuclear dot protein 52. J Cell Biol 1997;138:435-448.
43. Morriswood B, Ryzhakov G, Puri C, Arden SD, Roberts R et al. T6BP and NDP52 are myosin VI binding partners with potential roles in cytokine signalling and cell adhesion. J Cell Sci 2007;120:2574-2585.
44. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008;451:1069-1075.
45. Vidic J, Richard CA, Péchoux C, da Costa B, Bertho N et al. Amyloid assemblies of influenza A virus PB1-F2 protein damage membrane and induce cytotoxicity. J Biol Chem 2016;291:739-751.
46. Chevalier C, Le Goffic R, Jamme F, Leymarie O, Réfrégiers M et al. Synchrotron infrared and deep UV fluorescent microspectroscopy study of PB1-F2 β-aggregated structures in influenza A virus-infected cells. J Biol Chem 2016;291:9060-9072.
47. Chevalier C, Al Bazzal A, Vidic J, Février V, Bourdieu C et al. PB1-F2 influenza A virus protein adopts a β-sheet conformation and forms amyloid fibers in membrane environments. J Biol Chem 2010;285:13233-13243.
48. Miodek A, Vidic J, Sauriat-Dorizon H, Richard CA, Le Goffic R et al. Electrochemical detection of the oligomerization of PB1-F2 influenza A virus protein in infected cells. Anal Chem 2014;86:9098-9105.
49. Bucciantini M, Calloni G, Chiti F, Formigli L, Nosi D et al. Prefibrillar amyloid protein aggregates share common features of cytotoxicity. J Biol Chem 2004;279:31374-31382.
50. Hou F, Sun L, Zheng H, Skaug B, Jiang QX et al. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 2011;146:448-461.
51. Castanier C, Zemirli N, Portier A, Garcin D, Bidére N et al. MAVS ubiquitination by the E3 ligase TRIM25 and degradation by the proteasome is involved in type I interferon production after activation of the antiviral RIG-I-like receptors. BMC Biol 2012;10:44.
52. Xu H, He X, Zheng H, Huang LJ, Hou F et al. Structural basis for the prion-like MAVS filaments in antiviral innate immunity. Elife 2014;3:e01489.
53. Tafforeau L, Chantier T, Pradezynski F, Pellet J, Mangeot PE et al. Generation and comprehensive analysis of an influenza virus polymerase cellular interaction network. J Virol 2011;85:13010-13018.
54. Tafforeau L, Rabourdin-Combe C, Lotteau V. Virus-human cell interactomes. Methods Mol Biol 2012;812:103-120.
55. Pellet J, Meyniel L, Vidalain PO, de Chassey B, Tafforeau L et al. pISTil: a pipeline for yeast two-hybrid interaction sequence tags identification and analysis. BMC Res Notes 2009;2:220.
56. Guillot L, Le Goffic R, Bloch S, Escriou N, Akira S 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 2005;280:5571-5580.
57. Hervé PL, Raliou M, Bourdieu C, Dubuquoy C, Petit-Camurdan A et al. A novel subnucleocapsid nanoplatform for mucosal vaccination against influenza virus that targets the ectodomain of matrix protein 2. J Virol 2014;88:325-338.
58. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 2015;43:D447-D452.