H5N1 influenza A virus PB1-F2 relieves HAX-1- mediated restriction of avian virus polymerase PA in human lung cells

Journal of Virology

Volumn 92, Issue 11, 2018, Pages

  Mazel Sanchez, B ^a   Boal Carvalho, I ^a   Silva, F ^a   Dijkman, R ^b,c   Schmolke, M ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

H5N1; HAX 1; Influenza A virus; PA; PB1 F2; Polymerases; Zoonosis

Indexed keywords

HCLS1 ASSOCIATED PROTEIN X1; PROTEIN PB1 F2; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS POLYMERASE PA; HAX1 PROTEIN, HUMAN; PB1-F2 PROTEIN, INFLUENZA A VIRUS; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; INFLUENZA A VIRUS (H3N2); INFLUENZA A VIRUS (H5N1); LUNG ALVEOLUS CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN RESTRICTION; VIRUS REPLICATION; VIRUS TRANSMISSION; A-549 CELL LINE; ANIMAL; AVIAN INFLUENZA; BIRD; CRISPR CAS SYSTEM; DOG; GENE KNOCKOUT; GENETICS; HEK293 CELL LINE; HELA CELL LINE; INFLUENZA; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H7N9); LUNG; MDCK CELL LINE; METABOLISM; PATHOGENICITY; TRANSMISSION; TUMOR CELL LINE; VIROLOGY; ZOONOSIS;

A549 CELLS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BIRDS; CELL LINE, TUMOR; CRISPR-CAS SYSTEMS; DOGS; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HELA CELLS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; LUNG; MADIN DARBY CANINE KIDNEY CELLS; PROTEIN BINDING; VIRAL PROTEINS; VIRUS REPLICATION; ZOONOSES;

EID: 85046890548     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00425-18     Document Type: Article

References (50)

1. World Health Organization. 2018. Cumulative number of confirmed human cases of avian influenza A (H5N1) reported to WHO. World Health Organization, Geneva, Switzerland
2. Yee KS, Carpenter TE, Cardona CJ. 2009. Epidemiology of H5N1 avian influenza. Comp Immunol Microbiol Infect Dis 32:325-340. https://doi.org/10.1016/j.cimid.2008.01.005
3. Olsen SJ, Ungchusak K, Sovann L, Uyeki TM, Dowell SF, Cox NJ, Aldis W, Chunsuttiwat S. 2005. Family clustering of avian influenza A (H5N1). Emerg Infect Dis 11:1799-1801. https://doi.org/10.3201/eid1111.050646
4. Conenello GM, Tisoncik JR, Rosenzweig E, Varga ZT, Palese P, Katze MG. 2011. 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 85:652-662. https://doi.org/10.1128/JVI.01987-10
5. McAuley JL, Chipuk JE, Boyd KL, Van De Velde N, Green DR, McCullers JA. 2010. PB1-F2 proteins from H5N1 and 20 century pandemic influenza viruses cause immunopathology. PLoS Pathog 6(7):e1001014. https://doi.org/10.1371/journal.ppat.1001014
6. Vidy A, Maisonnasse P, Da Costa B, Delmas B, Chevalier C, Le Goffic R. 2016. The influenza virus protein PB1-F2 increases viral pathogenesis through neutrophil recruitment and NK cells inhibition. PLoS One 11(10): e0165361. https://doi.org/10.1371/journal.pone.0165361
7. Zamarin D, Ortigoza MB, Palese P. 2006. Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J Virol 80:7976-7983. https://doi.org/10.1128/JVI.00415-06
8. Schmolke M, Manicassamy B, Pena L, Sutton T, Hai R, Varga ZT, Hale BG, Steel J, Perez DR, Garcia-Sastre A. 2011. Differential contribution of PB1-F2 to the virulence of highly pathogenic H5N1 influenza A virus in mammalian and avian species. PLoS Pathog 7(8):e1002186. https://doi.org/10.1371/journal.ppat.1002186
9. Zell R, Krumbholz A, Eitner A, Krieg R, Halbhuber KJ, Wutzler P. 2007. Prevalence of PB1-F2 of influenza A viruses. J Gen Virol 88(Part 2): 536-546. https://doi.org/10.1099/vir.0.82378-0
10. Alymova IV, Green AM, van de Velde N, McAuley JL, Boyd KL, Ghoneim HE, McCullers JA. 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. https://doi.org/10.1128/JVI.05872-11
11. Varga ZT, Ramos I, Hai R, Schmolke M, Garcia-Sastre A, Fernandez-Sesma A, Palese P. 2011. The influenza virus protein PB1-F2 inhibits the induction of type I interferon at the level of the MAVS adaptor protein. PLoS Pathog 7(6):e1002067. https://doi.org/10.1371/journal.ppat.1002067
12. Le Goffic R, Bouguyon E, Chevalier C, Vidic J, Da Costa B, Leymarie O, Bourdieu C, Decamps L, Dhorne-Pollet S, Delmas B. 2010. Influenza A virus protein PB1-F2 exacerbates IFN-beta expression of human respiratory epithelial cells. J Immunol 185:4812-4823. https://doi.org/10.4049/jimmunol.0903952
13. Hai R, Schmolke M, Varga ZT, Manicassamy B, Wang TT, Belser JA, Pearce MB, Garcia-Sastre A, Tumpey TM, Palese P. 2010. PB1-F2 expression by the 2009 pandemic H1N1 influenza virus has minimal impact on virulence in animal models. J Virol 84:4442-4450. https://doi.org/10.1128/JVI.02717-09
14. McAuley J, Deng YM, Gilbertson B, Mackenzie-Kludas C, Barr I, Brown L. 2017. Rapid evolution of the PB1-F2 virulence protein expressed by human seasonal H3N2 influenza viruses reduces inflammatory responses to infection. Virol J 14:162. https://doi.org/10.1186/s12985-017-0827-0
15. Hsu WB, Shih JL, Shih JR, Du JL, Teng SC, Huang LM, Wang WB. 2013. Cellular protein HAX1 interacts with the influenza A virus PA polymerase subunit and impedes its nuclear translocation. J Virol 87:110-123. https://doi.org/10.1128/JVI.00939-12
16. Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E. 2005. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191-2198. https://doi.org/10.1128/JVI.79.4.2191-2198.2005
17. Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM, Nguyen V, Pham VTS, Vo CD, Le TQ, Ngo TT, Dao BK, Le PP, Nguyen TT, Hoang TL, Cao VT, Le TG, Nguyen DT, Le HN, Nguyen KT, Le HS, Le VT, Christiane D, Tran TT, Menno de J, Schultsz C, Cheng P, Lim W, Horby P, Farrar J, World Health Organization International Avian Influenza Investigative Team. 2004. Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med 350:1179-1188. https://doi.org/10.1056/NEJMoa040419
18. Steel J, Lowen AC, Pena L, Angel M, Solorzano A, Albrecht R, Perez DR, Garcia-Sastre A, Palese P. 2009. Live attenuated influenza viruses containing NS1 truncations as vaccine candidates against H5N1 highly pathogenic avian influenza. J Virol 83:1742-1753. https://doi.org/10.1128/JVI.01920-08
19. Tauber S, Ligertwood Y, Quigg-Nicol M, Dutia BM, Elliott RM. 2012. Behaviour of influenza A viruses differentially expressing segment 2 gene products in vitro and in vivo. J Gen Virol 93(Part 4):840-849. https://doi.org/10.1099/vir.0.039966-0
20. Schmidt U, Richter K, Berger AB, Lichter P. 2006. In vivo BiFC analysis of Y14 and NXF1 mRNA export complexes: preferential localization within and around SC35 domains. J Cell Biol 172:373-381. https://doi.org/10.1083/jcb.200503061
21. Vafiadaki E, Arvanitis DA, Pagakis SN, Papalouka V, Sanoudou D, Kontrogianni-Konstantopoulos A, Kranias EG. 2009. The anti-apoptotic protein HAX-1 interacts with SERCA2 and regulates its protein levels to promote cell survival. Mol Biol Cell 20:306-318. https://doi.org/10.1091/mbc.E08-06-0587
22. Wurzer WJ, Planz O, Ehrhardt C, Giner M, Silberzahn T, Pleschka S, Ludwig S. 2003. Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J 22:2717-2728. https://doi.org/10.1093/emboj/cdg279
23. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW. 2009. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914-918
24. Akkina RK, Chambers TM, Londo DR, Nayak DP. 1987. Intracellular localization of the viral polymerase proteins in cells infected with influenza virus and cells expressing PB1 protein from cloned cDNA. J Virol 61: 2217-2224
25. Shaw ML, Palese P. 2013. Orthomyxoviridae: the viruses and their replication, p 1691-1740. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed. Lippincott Williams & Williams, Philadelphia, PA
26. Zhang H, Hale BG, Xu K, Sun B. 2013. Viral and host factors required for avian H5N1 influenza A virus replication in mammalian cells. Viruses 5:1431-1446. https://doi.org/10.3390/v5061431
27. Taft AS, Ozawa M, Fitch A, Depasse JV, Halfmann PJ, Hill-Batorski L, Hatta M, Friedrich TC, Lopes TJ, Maher EA, Ghedin E, Macken CA, Neumann G, Kawaoka Y. 2015. Identification of mammalian-adapting mutations in the polymerase complex of an avian H5N1 influenza virus. Nat Commun 6:7491. https://doi.org/10.1038/ncomms8491
28. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J. 2005. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102:18590-18595. https://doi.org/10.1073/pnas.0507415102
29. Mänz B, Schwemmle M, Brunotte L. 2013. Adaptation of avian influenza A virus polymerase in mammals to overcome the host species barrier. J Virol 87:7200-7209. https://doi.org/10.1128/JVI.00980-13
30. Bussey KA, Desmet EA, Mattiacio JL, Hamilton A, Bradel-Tretheway B, Bussey HE, Kim B, Dewhurst S, Takimoto T. 2011. PA residues in the 2009 H1N1 pandemic influenza virus enhance avian influenza virus polymerase activity in mammalian cells. J Virol 85:7020-7028. https://doi.org/10.1128/JVI.00522-11
31. Mehle A, Doudna JA. 2009. Adaptive strategies of the influenza virus polymerase for replication in humans. Proc Natl Acad Sci U S A 106: 21312-21316. https://doi.org/10.1073/pnas.0911915106
32. Mehle A, Dugan VG, Taubenberger JK, Doudna JA. 2012. Reassortment and mutation of the avian influenza virus polymerase PA subunit overcome species barriers. J Virol 86:1750-1757. https://doi.org/10.1128/JVI.06203-11
33. Dittmann J, Stertz S, Grimm D, Steel J, Garcia-Sastre A, Haller O, Kochs G. 2008. Influenza A virus strains differ in sensitivity to the antiviral action of Mx-GTPase. J Virol 82:3624-3631. https://doi.org/10.1128/JVI.01753-07
34. Suzuki Y, Demoliere C, Kitamura D, Takeshita H, Deuschle U, Watanabe T. 1997. HAX-1, a novel intracellular protein, localized on mitochondria, directly associates with HS1, a substrate of Src family tyrosine kinases. J Immunol 158:2736-2744
35. Simmen T. 2011. Hax-1: a regulator of calcium signaling and apoptosis progression with multiple roles in human disease. Expert Opin Ther Targets 15:741-751. https://doi.org/10.1517/14728222.2011.561787
36. Yap SV, Koontz JM, Kontrogianni-Konstantopoulos A. 2011. HAX-1: a family of apoptotic regulators in health and disease. J Cell Physiol 226:2752-2761. https://doi.org/10.1002/jcp.22638
37. Yedavalli VS, Shih HM, Chiang YP, Lu CY, Chang LY, Chen MY, Chuang CY, Dayton AI, Jeang KT, Huang LM. 2005. Human immunodeficiency virus type 1 Vpr interacts with antiapoptotic mitochondrial protein HAX-1. J Virol 79:13735-13746. https://doi.org/10.1128/JVI.79.21.13735-13746.2005
38. Sharp TV, Wang HW, Koumi A, Hollyman D, Endo Y, Ye H, Du MQ, Boshoff C. 2002. K15 protein of Kaposi's sarcoma-associated herpesvirus is latently expressed and binds to HAX-1, a protein with antiapoptotic function. J Virol 76:802-816. https://doi.org/10.1128/JVI.76.2.802-816.2002
39. Kawaguchi Y, Nakajima K, Igarashi M, Morita T, Tanaka M, Suzuki M, Yokoyama A, Matsuda G, Kato K, Kanamori M, Hirai K. 2000. Interaction of Epstein-Barr virus nuclear antigen leader protein (EBNA-LP) with HS1-associated protein X-1: implication of cytoplasmic function of EBNA-LP. J Virol 74:10104-10111. https://doi.org/10.1128/JVI.74.21.10104-10111.2000
40. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122-1125. https://doi.org/10.1038/nature08182
41. Mazur I, Anhlan D, Mitzner D, Wixler L, Schubert U, Ludwig S. 2008. The proapoptotic influenza A virus protein PB1-F2 regulates viral polymerase activity by interaction with the PB1 protein. Cell Microbiol 10: 1140-1152. https://doi.org/10.1111/j.1462-5822.2008.01116.x
42. McAuley JL, Zhang K, McCullers JA. 2010. The effects of influenza A virus PB1-F2 protein on polymerase activity are strain specific and do not impact pathogenesis. J Virol 84:558-564. https://doi.org/10.1128/JVI.01785-09
43. Jaworska J, Coulombe F, Downey J, Tzelepis F, Shalaby K, Tattoli I, Berube J, Rousseau S, Martin JG, Girardin SE, McCullers JA, Divangahi M. 2014. NLRX1 prevents mitochondrial induced apoptosis and enhances macrophage antiviral immunity by interacting with influenza virus PB1-F2 protein. Proc Natl Acad Sci U S A 111:E2110-E2119. https://doi.org/10.1073/pnas.1322118111
44. Kosík I, Holly J, Russ G. 2013. PB1-F2 expedition from the whole protein through the domain to aa residue function. Acta Virol 57:138-148. https://doi.org/10.4149/av_2013_02_138
45. Quinlivan M, Zamarin D, Garcia-Sastre A, Cullinane A, Chambers T, Palese P. 2005. Attenuation of equine influenza viruses through truncations of the NS1 protein. J Virol 79:8431-8439. https://doi.org/10.1128/JVI.79.13.8431-8439.2005
46. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108: 193-199
47. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281-2308. https://doi.org/10.1038/nprot.2013.143
48. Goedhart J, von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, Hink MA, van Weeren L, Gadella TW, Jr, Royant A. 2012. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun 3:751. https://doi.org/10.1038/ncomms1738
49. Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA, Li T, Miteva YV, Hauri S, Sardiu ME, Low TY, Halim VA, Bagshaw RD, Hubner NC, Al-Hakim A, Bouchard A, Faubert D, Fermin D, Dunham WH, Goudreault M, Lin ZY, Badillo BG, Pawson T, Durocher D, Coulombe B, Aebersold R, Superti-Furga G, Colinge J, Heck AJ, Choi H, Gstaiger M, Mohammed S, Cristea IM, Bennett KL, Washburn MP, Raught B, Ewing RM, Gingras AC, Nesvizhskii AI. 2013. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10:730-736. https://doi.org/10.1038/nmeth.2557
50. Pleschka S, Jaskunas R, Engelhardt OG, Zurcher T, Palese P, Garcia-Sastre A. 1996. A plasmid-based reverse genetics system for influenza A virus. J Virol 70:4188-4192