Genetic analysis of the M gene of equine influenza virus strains isolated in Poland, in the context of the Asian-like group formation

1. Alves Beuttemmüller E., Woodward A., Rash A., Dos Santos Ferraz L.E., Fernandes Alfieri A., Alfieri A.A., Elton D.: Characterization of the epidemic strain of H3N8 equine influenza virus responsible for outbreaks in South America in 2012. Virol J 2016, 13, 45.10.1186/s12985-016-0503-9479959426993620Search in Google Scholar

2. Borchers K., Daly J., Stiens G., Kreling K., Kreling I., Ludwig H.: Characterisation of three equine influenza A H3N8 viruses from Germany (2000 and 2002): Evidence for frozen evolution. Vet Microbiol 2005, 107, 13–21.10.1016/j.vetmic.2005.01.01015795074Search in Google Scholar

3. Bountouri M., Fragkiadaki E., Ntafis V., Kanellos T., Xylouri E.: Phylogenetic and molecular characterization of equine H3N8 influenza viruses from Greece (2003 and 2007): Evidence for reassortment between evolutionary lineages. Virol J 2011, 8, 350.10.1186/1743-422X-8-350315812521756308Search in Google Scholar

4. Bryant N.A., Rash A.S., Russell C.A., Ross J., Cooke A., Bowman S., MacRae S., Lewis N.S., Paillot R., Zanoni R., Meier H., Griffiths L.A., Daly J.M., Tiwari A., Chambers T.M., Newton J.R., Elton D.M.: Antigenic and genetic variations in European and North American equine influenza virus strains (H3N8) isolated from 2006 to 2007. Vet Microbiol 2009, 138, 41–52.10.1016/j.vetmic.2009.03.00419346084Search in Google Scholar

5. Chen B.J., Leser G.P., Jackson D., Lamb R.A.: The influenza virus M2 protein cytoplasmic tail interacts with the M1 protein and influences virus assembly at the site of virus budding. J Virol 2008, 82, 10059–10070.10.1128/JVI.01184-08256624818701586Search in Google Scholar

6. Cullinane A., Newton J.R.: Equine influenza – a global perspective. Vet Microbiol 2013, 167, 205–214.10.1016/j.vetmic.2013.03.02923680107Search in Google Scholar

7. Daly J.M., Lai A.C.K., Binns M.M., Chambers T.M., Barrandeguy M., Mumford J.A.: Antigenic and genetic evolution of equine H3N8 influenza A viruses. J Gen Virol 1996, 77, 661–671.10.1099/0022-1317-77-4-6618627254Search in Google Scholar

8. Endo A., Pecoraro R., Sugita S., Nerome K.: Evolutionary pattern of the H3 haemagglutinin of equine influenza viruses: multiple evolutionary lineages and frozen replication. Arch Virol 1992, 123, 73–87.10.1007/BF013171391550498Search in Google Scholar

9. Fougerolle S., Legrand L., Lecouturier F., Sailleau C., Paillot R., Hans A., Pronost S.: Genetic evolution of equine influenza virus strains (H3N8) isolated in France from 1967 to 2015 and the implications of several potential pathogenic factors. Virology 2017, 505, 210–217.10.1016/j.virol.2017.02.00328292661Search in Google Scholar

10. Furuse Y., Suzuki A., Kamiqaki T., Oshitani H.: Evolution of the M gene of the influenza A virus in different host species: large-scale sequence analysis. Virol J, 2009, 6, 67.10.1186/1743-422X-6-67269478919476650Search in Google Scholar

11. Furuse Y., Suzuki A., Oshitani H.: Large-scale sequence analysis of M gene of influenza A viruses from different species: mechanisms for emergence and spread of amantadine resistance. Antimicrob Agents Chemother 2009, 53, 4457–4463.10.1128/AAC.00650-09276420219651904Search in Google Scholar

12. Gahan J., Garvey M., Gildea S., Gür E., Kagankaya A., Cullinane A.: Whole-genome sequencing and antigenic analysis of the first equine influenza virus identified in Turkey. Influenza Other Respir Viruses 2018, 12, 374–382.10.1111/irv.12485590780828940727Search in Google Scholar

13. Hall T.A.: User-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41, 95–98.Search in Google Scholar

14. 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 2001, 146, 2275–2289.10.1007/s00705017000211811679Search in Google Scholar

15. Ito T., Gorman O.T., Kawaoka Y., Bean W.J., Webster R.G.: Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. J Virol 1991, 65, 5491–5498.10.1128/jvi.65.10.5491-5498.19912490431895397Search in Google Scholar

16. Karamendin K., Kydyrmanov A., Kasymbekov Y. Khan E., Daulbayeva K., Asanova S., Zhumatov K., Seidalina A., Sayatov M., Fereidouni S.R.: Continuing evolution of equine influenza virus in Central Asia, 2007–2012. Arch Virol 2014, 159, 2321–2327.10.1007/s00705-014-2078-324748052Search in Google Scholar

17. Kumar S., Stecher G., Tamura K.: MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016, 33, 1870–1874.10.1093/molbev/msw054821082327004904Search in Google Scholar

18. Kwasnik M., Gora I.M., Rola J., Zmudzinski J.F., Rozek W.: NS-gene based phylogenetic analysis of equine influenza viruses isolated in Poland. Vet Microbiol 2016, 182, 95–101.10.1016/j.vetmic.2015.10.02826711034Search in Google Scholar

19. Laabassi F., Lecouturier F., Amelot G., Gaudaire D., Mamache B., Laugier C., Legrand L., Zientara S., Hans A.: Epidemiology and genetic characterization of H3N8 equine influenza virus responsible for clinical disease in Algeria in 2011. Transbound Emerg Dis 2015, 62, 623–631.10.1111/tbed.1220924472362Search in Google Scholar

20. Lai A.C., Chambers T.M., Holland R.E., Morley P.S., Haines D.M., Townsend H.G., Barrandeguy M.: Diverged evolution of recent equine-2 influenza (H3N8) viruses in the Western Hemisphere. Arch Virol 2001, 146, 1063–1074.10.1007/s00705017010611504416Search in Google Scholar

21. Lewis N.S., Daly J.M., Russell C.A., Horton D.L., Skepner E., Bryant N.A., Burke D.F., Rash A.S., Wood J.L., Chambers T.M., Fouchier R.A., Mumford J.A., Elton D.M., Smith D.J.: Antigenic and genetic evolution of equine influenza A (H3N8) virus from 1968 to 2007. J Virol 2011, 85, 12742–12749.10.1128/JVI.05319-11320941121937642Search in Google Scholar

22. Lindstrom S., Endo A., Sugita S., Pecoraro M., Hiromoto Y., Kamada M., Takahashi T., Nerome K.: Phylogenetic analyses of the matrix and non-structural genes of equine influenza viruses. Arch Virol 1998, 143, 1585–1598.10.1007/s0070500504009739336Search in Google Scholar

23. Liu H., Grantham M.L., Pekosz A.: Mutations in the influenza A virus M1 protein enhance virus budding to complement lethal mutations in the M2 cytoplasmic tail. J Virol 2018, 92, e00858–17.10.1128/JVI.00858-17573075929046451Search in Google Scholar

24. Madić J., Martinović S., Naglić T., Hajsig D., Cvetnić S.: Serological evidence for the presence of A/equine-1 influenza virus in unvaccinated horses in Croatia. Vet Rec 1996, 138, 68.10.1136/vr.138.3.688629334Search in Google Scholar

25. Murcia P.R., Wood.J.L.N., Holmes E.C.: Genome-scale evolution and phylodynamics of equine H3N8 influenza A virus. J Virol 2011, 85, 5312–5322.10.1128/JVI.02619-10309497921430049Search in Google Scholar

26. Noton S.L., Medcalf E., Fisher D., Mullin A.E., Elton D., Digard P.: Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J Gen Virol 2007, 88, 2280–2290.10.1099/vir.0.82809-0288497617622633Search in Google Scholar

27. Patrono L.V., Bonfante F., Zanardello C., Terregino C., Capua I., Murcia P.R.: Phylogenetically distinct equine influenza viruses show different tropism for the swine respiratory tract. J Gen Virol 2015, 96, 969–974.10.1099/vir.0.000049463106125593159Search in Google Scholar

28. Qi T., Guo W., Huang W., Dai L., Zhao L., Li H., Li X., Zhang X., Wang Y., Yan Y., He N., Xiang W.: Genetic evolution of equine influenza viruses isolated in China. Arch Virol 2010, 155, 1425–1432.10.1007/s00705-010-0724-y20559670Search in Google Scholar

29. Rash A., Morton R., Woodward A., Maes O., McCauley J., Bryant N., Elton D.: Evolution and divergence of H3N8 equine influenza viruses circulating in the United Kingdom from 2013 to 2015. Pathogens 2017, 6, 6.10.3390/pathogens6010006537189428208721Search in Google Scholar

30. Rossman J.S., Jing X., Leser G.P., Balannik V., Pinto L.H., Lamb R.A.: Influenza virus M2 ion channel protein is necessary for filamentous virion formation. J Virol 2010, 84, 5078–5088.10.1128/JVI.00119-10286383120219914Search in Google Scholar

31. Rossman J.S., Lamb R.A.: Influenza virus assembly and budding. Virology 2011, 411, 229–236.10.1016/j.virol.2010.12.003308665321237476Search in Google Scholar

32. Rozek W., Purzycka M., Polak M.P., Gradzki Z., Zmudzinski J.F.: Genetic typing of equine influenza virus isolated in Poland in 2005 and 2006. Virus Res 2009, 145, 121–126.10.1016/j.virusres.2009.06.01719580828Search in Google Scholar

33. Safo M.K., Musayev F.N., Mosier P.D., Zhou Q., Xie H., Desai U.R.: Crystal structures of influenza A virus matrix protein M1: variations on a theme. PLoS ONE 2014, 9, e109510.10.1371/journal.pone.0109510419011525295515Search in Google Scholar

34. Singh G.: Characterization of A/eq-1 virus isolated during the equine influenza epidemic in India. Acta Virol 1994, 38, 25–26.Search in Google Scholar

35. Thompson J.D., Higgins D.G., Gibson T.J.: CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22, 4673–4680.10.1093/nar/22.22.46733085177984417Search in Google Scholar

36. Virmani N., Bera B.C., Shanumugasundaram K., Singh B.K., Gulati B.R., Singh R.K., Vaid R.K.: Genetic analysis of the matrix and non-structural genes of equine influenza virus (H3N8) from epizootic of 2008–2009 in India. Vet Microbiol 2011, 152, 169–175.10.1016/j.vetmic.2011.04.01121620592Search in Google Scholar

37. Virmani N., Bera B.C., Singh B.K., Shanmugasundaram K., Gulati B.R., Barua S., Vaid R.K., Gupta A.K., Singh R.K.: Equine influenza outbreak in India (2008–09): virus isolation, sero-epidemiology, and phylogenetic analysis of HA gene. Vet Microbiol 2010, 143, 224–237.10.1016/j.vetmic.2009.12.00720053509Search in Google Scholar

38. Watson J., Daniels P., Kirkland P., Carroll A., Jeggo M.: The 2007 outbreak of equine influenza in Australia: lessons learned for international trade in horses. Rev Sci Tech Off Int Epiz 2011, 30, 87–93.10.20506/rst.30.1.202121809755Search in Google Scholar

39. Webster R. G.: Are equine 1 influenza viruses still present in horses? Equine Vet J 1993, 25, 537–538.10.1111/j.2042-3306.1993.tb03009.x8276003Search in Google Scholar

40. Wise H.M., Hutchinson E.C., Jagger B.W., Stuart A.D., Kang Z.H., Robb N., Schwartzman L.M., Kash J.C., Fodor E., Firth A.E., Gog J.R., Taubenberger J.K., Digard P: Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain. PLoS Pathog 2012, 8, e1002998.10.1371/journal.ppat.1002998348690023133386Search in Google Scholar

41. Zhang K., Wang Z., Fan G.Z., Wang J., Gao S., Li Y., Sun L., Yin C.C., Liu W.J.: Two polar residues within C-terminal domain of M1 are critical for the formation of influenza A virions: two polar residues control M1 oligomerization. Cell Microbiol 2015, 17, 1583–1593.10.1111/cmi.12457468245925939747Search in Google Scholar