PB2-588I Enhances 2009 H1N1 pandemic influenza virus virulence by increasing viral replication and exacerbating PB2 inhibition of beta interferon expression

Journal of Virology

Volumn 88, Issue 4, 2014, Pages 2260-2267

  Zhao, Zongzheng ^a   Yi, Chenyang ^a   Zhao, Lianzhong ^a   Wang, Shengyu ^a   Zhou, Lishan ^a   Hu, Yong ^a   Zou, Wei ^a   Chen, Huanchun ^a   Jin, Meilin ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CELL LINE; DOGS; HUMANS; IMMUNOPRECIPITATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERFERON-BETA; LUCIFERASES; MICE; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; RNA REPLICASE; SPECIES SPECIFICITY; SWINE; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 84893485475     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03024-13     Document Type: Article

References (43)

1. Berhane Y, Ojkic D, Neufeld J, Leith M, Hisanaga T, Kehler H, Ferencz A, Wojcinski H, Cottam-Birt C, Suderman M, Handel K, Alexandersen S, Pasick J. 2010. Molecular characterization of pandemic H1N1 influenza viruses isolated from turkeys and pathogenicity of a human pH1N1 isolate in turkeys. Avian Dis. 54:1275-1285. http://dx.doi.org/10.1637/9422-061410-Reg.1.
2. Dundon WG, De Benedictis P, Viale E, Capua I. 2010. Serologic evidence of pandemic (H1N1) 2009 infection in dogs, Italy. Emerg. Infect. Dis. 16:2019-2021. http://dx.doi.org/10.3201/eid1612.100514.
3. Pasma T, Joseph T. 2010. Pandemic (H1N1) 2009 infection in swine herds, Manitoba, Canada. Emerg. Infect. Dis. 16:706-708. http://dx.doi.org/10.3201/eid1604.091636.
4. Sponseller BA, Strait E, Jergens A, Trujillo J, Harmon K, Koster L, Jenkins-Moore M, Killian M, Swenson S, Bender H, Waller K, Miles K, Pearce T, Yoon KJ, Nara P. 2010. Influenza A pandemic (H1N1) 2009 virus infection in domestic cat. Emerg. Infect. Dis. 16:534-537. http://dx.doi.org/10.3201/eid1603.091737.
5. Gibbs AJ, Armstrong JS, Downie JC. 2009. From where did the 2009 "swine-origin" influenza A virus (H1N1) emerge? Virol. J. 6:207. http://dx.doi.org/10.1186/1743-422X-6-207.
6. Li Y, Zou W, Jia G, Ke J, Zhu J, Lin X, Zhou H, Jin M. 2013. The 2009 pandemic (H1N1) viruses isolated from pigs show enhanced pathogenicity in mice. Vet. Res. 44:41. http://dx.doi.org/10.1186/1297-9716-44-41.
7. 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. http://dx.doi.org/10.1073/pnas.0911915106.
8. Song MS, Pascua PN, Lee JH, Baek YH, Park KJ, Kwon HI, Park SJ, Kim CJ, Kim H, Webby RJ, Webster RG, Choi YK. 2011. Virulence and genetic compatibility of polymerase reassortant viruses derived from the pandemic (H1N1) 2009 influenza virus and circulating influenza A viruses. J. Virol. 85:6275-6286. http://dx.doi.org/10.1128/JVI.02125-10.
9. Zhou B, Li Y, Halpin R, Hine E, Spiro DJ, Wentworth DE. 2011. PB2 residue 158 is a pathogenic determinant of pandemic H1N1 and H5 influenza a viruses in mice. J. Virol. 85:357-365. http://dx.doi.org/10.1128/JVI.01694-10.
10. Chutinimitkul S, Herfst S, Steel J, Lowen AC, Ye J, van Riel D, Schrauwen EJ, Bestebroer TM, Koel B, Burke DF, Sutherland-Cash KH, Whittleston CS, Russell CA, Wales DJ, Smith DJ, Jonges M, Meijer A, Koopmans M, Rimmelzwaan GF, Kuiken T, Osterhaus AD, García-Sastre A, Perez DR, Fouchier RA. 2010. Virulence-associated substitution D222G in the hemagglutinin of 2009 pandemic influenza A(H1N1) virus affects receptor binding. J. Virol. 84:11802-11813. http://dx.doi.org/10.1128/JVI.01136-10.
11. Liu Y, Childs RA, Matrosovich T, Wharton S, Palma AS, Chai W, Daniels R, Gregory V, Uhlendorff J, Kiso M, Klenk HD, Hay A, Feizi T, Matrosovich M. 2010. Altered receptor specificity and cell tropism of D222G hemagglutinin mutants isolated from fatal cases of pandemic A(H1N1) 2009 influenza virus. J. Virol. 84:12069-12074. http://dx.doi.org/10.1128/JVI.01639-10.
12. Li J, Ishaq M, Prudence M, Xi X, Hu T, Liu Q, Guo D. 2009. Single mutation at the amino acid position 627 of PB2 that leads to increased virulence of an H5N1 avian influenza virus during adaptation in mice can be compensated by multiple mutations at other sites of PB2. Virus Res. 144:123-129. http://dx.doi.org/10.1016/j.virusres.2009.04.008.
13. Steel J, Lowen AC, Mubareka S, Palese P. 2009. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 5:e1000252. http://dx.doi.org/10.1371/journal.ppat.1000252.
14. Jagger BW, Memoli MJ, Sheng ZM, Qi L, Hrabal RJ, Allen GL, Dugan VG, Wang R, Digard P, Kash JC, Taubenberger JK. 2010. The PB2-E627K mutation attenuates viruses containing the 2009 H1N1 influenza pandemic polymerase. mBio 1(1):e00067-10. http://dx.doi.org/10.1128/mBio.00067-10.
15. Zhu H, Wang J, Wang P, Song W, Zheng Z, Chen R, Guo K, Zhang T, Peiris JS, Chen H, Guan Y. 2010. Substitution of lysine at 627 position in PB2 protein does not change virulence of the 2009 pandemic H1N1 virus in mice. Virology 401:1-5. http://dx.doi.org/10.1016/j.virol.2010.02.024.
16. Herfst S, Chutinimitkul S, Ye J, de Wit E, Munster VJ, Schrauwen EJ, Bestebroer TM, Jonges M, Meijer A, Koopmans M, Rimmelzwaan GF, Osterhaus AD, Perez DR, Fouchier RA. 2010. Introduction of virulence markers in PB2 of pandemic swine-origin influenza virus does not result in enhanced virulence or transmission. J. Virol. 84:3752-3758. http://dx.doi.org/10.1128/JVI.02634-09.
17. Graef KM, Vreede FT, Lau YF, McCall AW, Carr SM, Subbarao K, Fodor E. 2010. The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J. Virol. 84:8433-8445. http://dx.doi.org/10.1128/JVI.00879-10.
18. Varga ZT, Grant A, Manicassamy B, Palese P. 2012. Influenza virus protein PB1-F2 inhibits the induction of type I interferon by binding to MAVS and decreasing mitochondrial membrane potential. J. Virol. 86:8359-8366. http://dx.doi.org/10.1128/JVI.01122-12.
19. Seth RB, Sun L, Ea CK, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 122:669-682. http://dx.doi.org/10.1016/j.cell.2005.08.012.
20. García-Sastre A, Biron CA. 2006. Type 1 interferons and the virus-host relationship: a lesson in détente. Science 312:879-882. http://dx.doi.org/10.1126/science.1125676.
21. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. U.S.A. 97:6108-6113. http://dx.doi.org/10.1073/pnas.100133697.
22. Zhou H, Wang C, Yang Y, Guo X, Kang C, Chen H, Jin M. 2011. Pandemic (H1N1) 2009 virus in swine herds, People's Republic of China. Emerg. Infect. Dis. 17:1757-1759. http://dx.doi.org/10.3201/eid1709.101916.
23. Zhao G, Fan Q, Zhong L, Li Y, Liu W, Liu X, Gao S, Peng D. 2012. Isolation and phylogenetic analysis of pandemic H1N1/09 influenza virus from swine in Jiangsu province of China. Res. Vet. Sci. 93:125-132. http://dx.doi.org/10.1016/j.rvsc.2011.06.009.
24. Chen Y, Zhang J, Qiao C, Yang H, Zhang Y, Xin X, Chen H. 2013. Co-circulation of pandemic 2009 H1N1, classical swine H1N1 and avianlike swine H1N1 influenza viruses in pigs in China. Infect. Genet. Evol. 13:331-338. http://dx.doi.org/10.1016/j.meegid.2012.09.021.
25. Pan C, Cheung B, Tan S, Li C, Li L, Liu S, Jiang S. 2010. Genomic signature and mutation trend analysis of pandemic (H1N1) 2009 influenza A virus. PLoS One 5:e9549. http://dx.doi.org/10.1371/journal.pone.0009549.
26. Zhu W, Zhu Y, Qin K, Yu Z, Gao R, Yu H, Zhou J, Shu Y. 2012. Mutations in polymerase genes enhanced the virulence of 2009 pandemic H1N1 influenza virus in mice. PLoS One 7:e33383. http://dx.doi.org/10.1371/journal.pone.0033383.
27. Iwai A, Shiozaki T, Kawai T, Akira S, Kawaoka Y, Takada A, Kida H, Miyazaki T. 2010. Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J. Biol. Chem. 285:32064-32074. http://dx.doi.org/10.1074/jbc.M110.112458.
28. Liniger M, Moulin HR, Sakoda Y, Ruggli N, Summerfield A. 2012. Highly pathogenic avian influenza virus H5N1 controls type I IFN induction in chicken macrophage HD-11 cells: a polygenic trait that involves NS1 and the polymerase complex. Virol. J. 9:7. http://dx.doi.org/10.1186/1743-422X-9-7.
29. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737. http://dx.doi.org/10.1038/ni1087.
30. Kang DC, Gopalkrishnan RV, Wu Q, Jankowsky E, Pyle AM, Fisher PB. 2002. mda-5: An interferon-inducible putative RNA helicase with doublestranded RNA-dependent ATPase activity and melanoma growthsuppressive properties. Proc. Natl. Acad. Sci. U.S.A. 99:637-642. http://dx.doi.org/10.1073/pnas.022637199.
31. Alff PJ, Gavrilovskaya IN, Gorbunova E, Endriss K, Chong Y, Geimonen E, Sen N, Reich NC, Mackow ER. 2006. The pathogenic NY-1 hantavirus G1 cytoplasmic tail inhibits RIG-I-and TBK-1-directed interferon responses. J. Virol. 80:9676-9686. http://dx.doi.org/10.1128/JVI.00508-06.
32. Foeglein Á, Loucaides EM, Mura M, Wise HM, Barclay WS, Digard P. 2011. Influence of PB2 host-range determinants on the intranuclear mobility of the influenza A virus polymerase. J. Gen. Virol. 92:1650-1661. http://dx.doi.org/10.1099/vir.0.031492-0.
33. Hai R, Schmolke M, Varga ZT, Manicassamy B, Wang TT, Belser JA, Pearce MB, García-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. http://dx.doi.org/10.1128/JVI.02717-09.
34. Chen GW, Chang SC, Mok CK, Lo YL, Kung YN, Huang JH, Shih YH, Wang JY, Chiang C, Chen CJ, Shih SR. 2006. Genomic signatures of human versus avian influenzaAviruses. Emerg. Infect. Dis. 12:1353-1360. http://dx.doi.org/10.3201/eid1209.060276.
35. Liu Q, Lu L, Sun Z, Chen GW, Wen Y, Jiang S. 2013. Genomic signature and protein sequence analysis of a novel influenza A (H7N9) virus that causes an outbreak in humans in China. Microbes Infect. 15:432-439. http://dx.doi.org/10.1016/j.micinf.2013.04.004.
36. Meunier I, von Messling V. 2011. NS1-mediated delay of type I interferon induction contributes to influenza A virulence in ferrets. J. Gen. Virol. 92:1635-1644. http://dx.doi.org/10.1099/vir.0.032193-0.
37. Matthaei M, Budt M, Wolff T. 2013. Highly pathogenic H5N1 influenza A virus strains provoke heterogeneous IFN-α/β responses that distinctively affect viral propagation in human cells. PLoS One 8:e56659. http://dx.doi.org/10.1371/journal.pone.0056659.
38. Forbes NE, Ping J, Dankar SK, Jia JJ, Selman M, Keleta L, Zhou Y, Brown EG. 2012. Multifunctional adaptive NS1 mutations are selected upon human influenza virus evolution in the mouse. PLoS One 7:e31839. http://dx.doi.org/10.1371/journal.pone.0031839.
39. Leymarie O, Jouvion G, Hervé PL, Chevalier C, Lorin V, Lecardonnel J, Da Costa B, Delmas B, Escriou N, Le Goffic R. 2013. Kinetic characterization of PB1-F2-mediated immunopathology during highly pathogenic avian H5N1 influenza virus infection. PLoS One 8:e57894. http://dx.doi.org/10.1371/journal.pone.0057894.
40. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N, Goodbourn S, Randall RE. 2004. The V proteins of paramyxoviruses bind the IFNinducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. U.S.A. 101:17264-17269. http://dx.doi.org/10.1073/pnas.0407639101.
41. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. 2005. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19:727-740. http://dx.doi.org/10.1016/j.molcel.2005.08.014.
42. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. 2005. IPS-1, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988. http://dx.doi.org/10.1038/ni1243.
43. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172. http://dx.doi.org/10.1038/nature04193.