Substitution in position 222 of haemagglutinin of pandemic influenza A (H1N1) viruses isolated from pigs in Poland

Andrzej Kowalczyk 1 , Kinga Urbaniak 1 , Iwona Markowska-Daniel 1 , and Zygmunt Pejsak 1
  • 1 Department of Swine Diseases, National Veterinary Research Institute, 24-100 Pulawy, Poland


The aim of the study was to monitor genetic diversity and antigenic changes in the genome of influenza A(H1N1)pdm09 viral isolates detected during the post-pandemic period in Poland. Clinical specimens obtained from three suspected cases of influenza were analysed by sequencing. Among the differences identified in amino acids sequences, nine substitutions were located within the antigenic HA1 sites and in five residues forming receptor-binding pocket. The HA(D222G) mutation was shown in the isolate Swine/Poland/134312/12 obtained from a mild case of the disease. It must be emphasized that, in general, clinically mild cases are caused by the viruses in which that specific mutation, i.e. haemagglutinin (D222G), does not occur.

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  • 1. Chen L.M., Rivailler P., Hossain J., Carney P., Balish A., Perry I., Davis C.T., Garten R., Shu B., Xu X., Klimov A., Paulson J.C., Cox N.J., Swenson S., Stevens J., Vincent A., Gramer M., Donis R.O.: Receptor specificity of subtype H1 influenza A viruses isolated from swine and humans in the United States. Virology 2011, 412, 401-410.

  • 2. Couceiro J.N., Paulson J.C., Baum L.G.: Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 1993, 29, 155-165.

  • 3. Gabriel G., Dauber B., Wolff T., Planz O., Klenk H.D., Stech J.: The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 2003, 102, 18590-18595.

  • 4. Gambaryan A.S., Boravleva E.Y., Matrosovich T.Y., Matrosovich M.N., Klenk H.D., Moiseeva E.V., Tuzikov A.B., Chinarev A.A., Pazynina G.V., Bovin N.V.: Polymer-bound 6' sialyl-N-acetyllactosamine protects mice infected by influenza virus. Antiviral Res 2005, 68, 116-123.

  • 5. Guldemir D., Kalaycioglu A.T., Altas A.B., Korukluoglu G., Durmaz R.: Monitoring genetic diversity of influenza A(H1N1)pdm09 virus circulating during the post-pandemic period in Turkey. Jpn J Infect Dis 2013, 66, 299-305.

  • 6. Hoffmann E., Stech J., Guan Y., Webster R.G., Perez D.R: Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146, 2275-2289.

  • 7. Ilyushina N.A., Khalenkov AM., Seiler J.P., Forrest H.L., Bovin N.V., Marjuki H., Barman S., Webster R.G., Webby R.J.: Adaptation of pandemic H1N1 influenza viruses in mice. Virology 2010, 84, 8607-8616.

  • 8. Kilander A., Rykkvin R., Dudman S.G., Hungnes O.: Observed association between the HA1 mutation D222G in the 2009 pandemic influenza A(H1N1) virus and severe clinical outcome, Norway 2009-2010. Euro Surveill 2010, 15, 19498.

  • 9. Kowalczyk A., Markowska-Daniel I., Rasmussen T.B.: Development of a primer-probe energy transfer based real-time PCR for the detection of Swine influenza virus. J Virol Methods 2013, 187, 228-233.

  • 10. Ledesma J., Pozo F., Reina G., Blasco M., Rodríguez G., Montes M., López-Miragaya I., Salvador C., Reina J., Ortíz de Lejarazu R., Egido P., López Barba J., Delgado C., Cuevas M.T., Casas I.: Genetic diversity of influenza A(H1N1)2009 virus circulating during the season 2010-2011 in Spain. J Clin Virol 2012, 53, 16-21.

  • 11. Maines T.R., Jayaraman A., Belser, J.A., Wadford D.A., Pappas C., Zeng H., Gustin K.M., Pearce M.B., Viswanathan K., Shriver Z.H., Raman R, Cox N.J., Sasisekharan R., Katz J.M., Tumpey T.M.: Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 2009, 325, 484-487.

  • 12. Mak D.B., Daly A.M., Armstrong P.K., Effler P.V.: Pandemic (H1N1) 2009 influenza vaccination coverage in Western Australia. Med J Aust 2010, 193, 401-404.

  • 13. Melidou A., Gioula G., Exindari M., Chatzidimitriou D., Diza E., Malisiovas N.: Molecular and phylogenetic analysis of the haemagglutinin gene of pandemic influenza H1N1 2009 viruses associated with severe and fatal infections. Vet Res 2010, 151, 192-199.

  • 14. Moussi A., Kacem M.A., Pozo F., Ledesma J., Cuevas M.T., Casas I., Slim A.: Genetic diversity of HA1 domain of heammaglutinin gene of influenza A(H1N1)pdm09 in Tunisia. J Virol 2013, 10, 150.

  • 15. Nelson M., Spiro D., Wentworth D., Beck E., Fan J., Ghedin E., Halpin R., Bera J., Hine E., Proudfoot K., Stockwell T., Lin X., Griesemer S., Kumar S., Bose M., Viboud C., Holmes E., Henrickson K.: The early diversification of influenza A/H1N1pdm. 2009, PLoS Curr 1:RRN1126.

  • 16. Schaefer R., Zanella R.C., Brentano L., Vincent A., Ritterbusch G.A., Silveira S., Luizinho Caron L., Mores G.: Isolation and characterization of a pandemic H1N1 influenza virus in pigs in Brazil. Pesq Vet Bras 2011, 31, 761-767.

  • 17. Stevens J., Chen L.M., Carney P.J., Garten R., Foust A., Le J., Pokorny B.A., Manojkumar R., Silverman J., Devis R., Rhea K., Xu X., Bucher D.J., Paulson J.C., Cox N.J., Klimov A., Donis R.O.: Receptor specificity of influenza A H3N2 viruses isolated in mammalian cells and embryonated chicken eggs. J Virol 2010, 84, 8287-8299.

  • 18. Takemae N., Ruttanapumma R., Parchariyanon S., Yoneyama S., Hayashi T., Hiramatsu H., Sriwilaijaroen N., Uchida Y., Kondo S., Yagi H., Kato K., Suzuki Y., Saito T.: Alterations in receptor-binding properties of swine influenza viruses of the H1 subtype after isolation in embryonated chicken eggs. J Gen Virol 2010, 91, 938-948.

  • 19. Tate M.D., Brooks A.G., Reading P.C.: Receptor specificity of the influenza virus hemagglutinin modulates sensitivity to soluble collections of the innate immune system and virulence in mice. Virology 2011, 413, 128-138.

  • 20. Vines A., Wells K., Matrosovich M., Castrucci M.R., Ito T., Kawaoka Y.: The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J Virol 1998, 72, 7626-7631.

  • 21. Yasugi M., Nakamura S., Daidoji T., Kawashita N., Ramadhany R., Yang C.S., Yasunaga T., Iida T., Horii T., Ikuta K., Takahashi K., Nakaya T.: Frequency of D222G and Q223R hemagglutinin mutants of pandemic (H1N1) 2009 influenza virus in Japan between 2009 and 2010. PLoS One 2012, 7, 30946.

  • 22. Zheng B., Chan K.H., Zhang A.J., Zhou J., Chan C.C., Poon V.K., Zhang K., Leung V.H., Jin D.Y., Woo P.C., Chan J.F., To K.K., Chen H, Yuen K.Y.: D225G mutation in hemagglutinin of pandemic influenza H1N1 (2009) virus enhances virulence in mice. Exp Biol Med 2010, 235, 981-988.

  • 23. Zhou B., Li Y., Halpin R., Hine E., Spiro D.J., Wentworth D.E.: PB2 residue 158 is a pathogenic determinant of pandemic H1N1 and H5 influenza a viruses in mice. J Virol 2011, 85, 357-365.


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