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Original Articles

Mammalian-adaptive mutation NP-Q357K in Eurasian H1N1 Swine Influenza viruses determines the virulence phenotype in mice

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Pages 989-999 | Received 14 Apr 2019, Accepted 16 Jun 2019, Published online: 03 Jul 2019

References

  • Castrucci MR, Donatelli I, Sidoli L, et al. Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology. 1993;193:503–506. doi: 10.1006/viro.1993.1155
  • Ma W, Kahn RE, Richt JA. The pig as a mixing vessel for influenza viruses: human and veterinary implications. J Mol Genet Med. 2008;3:158–166.
  • Smith GJ, Bahl J, Vijaykrishna D, et al. Dating the emergence of pandemic influenza viruses. Proc Natl Acad Sci U S A. 2009;106:11709–11712. doi: 10.1073/pnas.0904991106
  • Brown IH. The epidemiology and evolution of influenza viruses in pigs. Vet Microbiol. 2000;74:29–46. doi: 10.1016/S0378-1135(00)00164-4
  • Vijaykrishna D, Smith GJ, Pybus OG, et al. Long-term evolution and transmission dynamics of swine influenza A virus. Nature. 2011;473:519–522. doi: 10.1038/nature10004
  • Yang H, Chen Y, Qiao C, et al. Prevalence, genetics, and transmissibility in ferrets of Eurasian avian-like H1N1 swine influenza viruses. Proc Natl Acad Sci U S A. 2015. doi:10.1073/pnas.1522643113
  • Liang H, Lam TT, Fan X, et al. Expansion of genotypic diversity and establishment of 2009 H1N1 pandemic-origin internal genes in pigs in China. J Virol. 2014;88:10864–10874. doi: 10.1128/JVI.01327-14
  • Vijaykrishna D, Poon LL, Zhu HC, et al. Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science. 2010;328:1529. doi: 10.1126/science.1189132
  • Zhu WF, Shu YL. [An overview of swine influenza virus infection in humans]. Bing Du Xue Bao. 2013;29:559–565.
  • Olsen CW, Brown IH, Easterday BC, et al. Swine influenza. In: Straw B, D’Allaire S, Zimmerman J, Taylor D, editor. Diseases of swine. Iowa, USA: Iowa State University Press; 2005. p. 469–482.
  • Qi X, Cui L, Jiao Y, et al. Antigenic and genetic characterization of a European avian-like H1N1 swine influenza virus from a boy in China in 2011. Arch Virol. 2012;158:39–53. doi: 10.1007/s00705-012-1423-7
  • Wang DY, Qi SX, Li XY, et al. Human infection with Eurasian avian-like influenza A(H1N1) virus, China. Emerg Infect Dis. 2013;19:1709–1711. doi: 10.3201/eid1910.130420
  • Zhu W, Zhang H, Xiang X, et al. Reassortant Eurasian avian-like influenza A(H1N1) virus from a severely Ill Child, Hunan Province, China, 2015. Emerg Infect Dis. 2016;22:1930–1936. doi: 10.3201/eid2211.160181
  • Zhang Y, Zhang Q, Kong H, et al. H5n1 hybrid viruses bearing 2009/H1N1 virus genes transmit in Guinea pigs by respiratory droplet. Science. 2013;340:1459–1463. doi: 10.1126/science.1229455
  • Zhou B, Li Y, Halpin R, et al. PB2 residue 158 is a pathogenic determinant of pandemic H1N1 and H5 influenza a viruses in mice. J Virol. 2011;85:357–365. doi: 10.1128/JVI.01694-10
  • Bussey KA, Bousse T, Desmet EA, et al. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J Virol. 2010;84:4395–4406. doi: 10.1128/JVI.02642-09
  • Chen H, Bright RA, Subbarao K, et al. Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res. 2007;128:159–163. doi: 10.1016/j.virusres.2007.04.017
  • Lee MS, Deng MC, Lin YJ, et al. Characterization of an H5N1 avian influenza virus from Taiwan. Vet Microbiol. 2007;124:193–201. doi: 10.1016/j.vetmic.2007.04.021
  • Katz JM, Lu X, Tumpey TM, et al. Molecular correlates of influenza A H5N1 virus pathogenesis in mice. J Virol. 2000;74:10807–10810. doi: 10.1128/JVI.74.22.10807-10810.2000
  • Conenello GM, Zamarin D, Perrone LA, et al. 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. doi: 10.1371/journal.ppat.0030141
  • Subbarao K, Shaw MW. Molecular aspects of avian influenza (H5N1) viruses isolated from humans. Rev Med Virol. 2000;10:337–348. doi: 10.1002/1099-1654(200009/10)10:5<337::AID-RMV292>3.0.CO;2-V
  • Hatta M, Gao P, Halfmann P, et al. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science. 2001;293:1840–1842. doi: 10.1126/science.1062882
  • Chen H, Bright RA, Subbarao K, et al. Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res. 2007;128:159–163. doi: 10.1016/j.virusres.2007.04.017
  • Labadie K DSAE, Rameix-Welti MA, van der Werf S, et al. Host-range determinants on the PB2 protein of influenza A viruses control the interaction between the viral polymerase and nucleoprotein in human cells. Virology. 2007;362:271–282. doi: 10.1016/j.virol.2006.12.027
  • Naffakh N, Massin P, Escriou N, et al. Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J Gen Virol. 2000;81:1283–1291. doi: 10.1099/0022-1317-81-5-1283
  • Munster VJ, de Wit E, van Riel D, et al. The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J Infect Dis. 2007;196:258–265. doi: 10.1086/518792
  • Subbarao EK, London W, Murphy BR. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol. 1993;67:1761–1764.
  • Hatta M, Gao P, Halfmann P, et al. Molecular Basis for high virulence of Hong Kong H5N1 influenza A viruses. Science. 2001;293:1840–1842. doi: 10.1126/science.1062882
  • Zhu W, Li L, Yan Z, et al. Dual E627 K and D701N mutations in the PB2 protein of A(H7N9) influenza virus increased its virulence in mammalian models. Sci Rep. 2015;5:14170. doi: 10.1038/srep14170
  • Gabriel G, Herwig A, Klenk HD. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLos Pathog. 2008;4:e11. doi: 10.1371/journal.ppat.0040011
  • Le QM, Sakai-Tagawa Y, Ozawa M, et al. Selection of H5N1 influenza virus PB2 during replication in humans. J Virol. 2009;83:5278–5281. doi: 10.1128/JVI.00063-09
  • Li J, Ishaq M, Prudence M, et al. 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. 2009;144:123–129. doi: 10.1016/j.virusres.2009.04.008
  • Steel J, Lowen AC, Mubareka S, et al. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627 K or 627E/701N. PLos Pathog. 2009;5:e1000252. doi: 10.1371/journal.ppat.1000252
  • Fornek JL, Gillim-Ross L, Santos C, et al. A single-amino-acid substitution in a polymerase protein of an H5N1 influenza virus is associated with systemic infection and impaired T-cell activation in mice. J Virol. 2009;83:11102–11115. doi: 10.1128/JVI.00994-09
  • Gabriel G, Dauber B, Wolff T, et al. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A. 2005;102:18590–18595. doi: 10.1073/pnas.0507415102
  • Gao Y, Zhang Y, Shinya K, et al. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLos Pathog. 2009;5:e1000709. doi: 10.1371/journal.ppat.1000709
  • Steel J, Lowen AC, Mubareka S, et al. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627 K or 627E/701N. PLoS Pathog. 2009;5:e1000252. doi: 10.1371/journal.ppat.1000252
  • Reed LJ, Skiadopoulos MH. A Simple method of estimating fifty percent endpoints. Am J Hyg. 1938;27:493–497.
  • Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010
  • Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054
  • Yamanaka K, Ishihama A, Nagata K. Reconstitution of influenza virus RNA-nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. J Biol Chem. 1990;265:11151–11155.
  • Ruigrok RW, Baudin F. Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. J Gen Virol. 1995;76(Pt 4):1009–1014. doi: 10.1099/0022-1317-76-4-1009
  • Chenavas S, Crepin T, Delmas B, et al. Influenza virus nucleoprotein: structure, RNA binding, oligomerization and antiviral drug target. Future Microbiol. 2013;8:1537–1545. doi: 10.2217/fmb.13.128
  • Ye Q, Guu TS, Mata DA, et al. Biochemical and structural evidence in support of a coherent model for the formation of the double-helical influenza A virus ribonucleoprotein. MBio. 2012;4:e00467–e00412. doi: 10.1128/mBio.00467-12
  • Gabriel G, Dauber B, Wolff T, et al. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A. 2005;102:18590–18595. doi: 10.1073/pnas.0507415102
  • Ye Q, Krug RM, Tao YJ. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature. 2006;444:1078–1082. doi: 10.1038/nature05379
  • Moeller A, Kirchdoerfer RN, Potter CS, et al. Organization of the influenza virus replication machinery. Science. 2012;338:1631–1634. doi: 10.1126/science.1227270
  • Biswas SK, Boutz PL, Nayak DP. Influenza virus nucleoprotein interacts with influenza virus polymerase proteins. J Virol. 1998;72:5493–5501.
  • Kim JH, Hatta M, Watanabe S, et al. Role of host-specific amino acids in the pathogenicity of avian H5N1 influenza viruses in mice. J Gen Virol. 2010;91:1284–1289. doi: 10.1099/vir.0.018143-0
  • Finkelstein DB, Mukatira S, Mehta PK, et al. Persistent host markers in pandemic and H5N1 influenza viruses. J Virol. 2007;81:10292–10299. doi: 10.1128/JVI.00921-07
  • Manz B, Dornfeld D, Gotz V, et al. Pandemic influenza A viruses escape from restriction by human MxA through adaptive mutations in the nucleoprotein. PLoS Pathog. 2013;9:e1003279. doi: 10.1371/journal.ppat.1003279
  • Karber G. 50% end point calculation. Archiv für Experimentelle Pathologie und Pharmakologie. 1931;162:480–483. doi: 10.1007/BF01863914