{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,23]],"date-time":"2026-04-23T06:32:06Z","timestamp":1776925926858,"version":"3.51.2"},"reference-count":69,"publisher":"Springer Science and Business Media LLC","issue":"5","license":[{"start":{"date-parts":[[2024,4,16]],"date-time":"2024-04-16T00:00:00Z","timestamp":1713225600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,4,16]],"date-time":"2024-04-16T00:00:00Z","timestamp":1713225600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"University of Sadat City"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Arch Virol"],"published-print":{"date-parts":[[2024,5]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>H9N2 avian influenza viruses (AIVs) affect both poultry and humans on a global level, and they are especially prevalent in Egypt. In this study, we sequenced the entire genome of AIV H9N2 isolated from chickens in Egypt in 2021, using next-generation sequencing (NGS) technology. Phylogenetic analysis of the resulting sequences showed that the studied strain was generally monophyletic and grouped within the G1 sublineage of the Eurasian lineage. Four segments (polymerase basic 2 [PB2], polymerase basic 1 [PB1], polymerase acidic [PA], and non-structural [NS]) were related to Egyptian genotype II, while the nucleoprotein (NP), neuraminidase (NA), matrix (M), and haemagglutinin (HA) segments were related to Egyptian genotype I. Molecular analysis revealed that HA protein contained amino acid residues (191H and 234L) that suggested a predilection for attaching to human-like receptors. The antigenic sites of HA had two nonsynonymous mutations: V194I at antigenic site A and M40K at antigenic site B. Furthermore, the R403W and S372A mutations, which have been observed in H3N2 and H2N2 strains that caused human pandemics, were found in the NA protein of the detected strain. The internal proteins contained virulence markers: 504V in the PB2 protein, 622G, 436Y, 207K, and 677T in the PB1 protein, 127V, 550L, and 672L in PA protein, and 64F and 69P in the M protein. These results show that the detected strain had undergone intrasubtype reassortment. Furthermore, it contains changes in the viral proteins that make it more likely to be virulent, raising a question about the tendency of AIV H9N2 to become highly pathogenic in the future for both poultry and humans.<\/jats:p>","DOI":"10.1007\/s00705-024-06018-2","type":"journal-article","created":{"date-parts":[[2024,4,16]],"date-time":"2024-04-16T07:01:56Z","timestamp":1713250916000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Molecular characterization of the whole genome of H9N2 avian influenza virus isolated from Egyptian poultry farms"],"prefix":"10.1007","volume":"169","author":[{"given":"Nahed M.","family":"Bedair","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Moustafa A.","family":"Sakr","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ahmed","family":"Mourad","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nourhan","family":"Eissa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ahmed","family":"Mostafa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Omaima","family":"Khamiss","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,4,16]]},"reference":[{"issue":"1","key":"6018_CR1","doi-asserted-by":"publisher","first-page":"66","DOI":"10.2307\/1588557","volume":"14","author":"PJ Homme","year":"1970","unstructured":"Homme PJ, Easterday BC (1970) Avian influenza virus infections. I. Characteristics of influenza A-turkey-Wisconsin-1966 virus. Avian Dis 14(1):66\u201374 PMID: 4314007","journal-title":"Avian Dis"},{"issue":"4","key":"6018_CR2","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1080\/03079450050118485","volume":"29","author":"J Banks","year":"2000","unstructured":"Banks J, Speidel EC, Harris PA, Alexander DJ (2000) Phylogenetic analysis of influenza A viruses of H9 haemagglutinin subtype. Avian Pathol 29(4):353\u2013359. https:\/\/doi.org\/10.1080\/03079450050118485","journal-title":"Avian Pathol"},{"issue":"1","key":"6018_CR3","doi-asserted-by":"publisher","first-page":"26","DOI":"10.7774\/cevr.2013.2.1.26","volume":"2","author":"DH Lee","year":"2013","unstructured":"Lee DH, Song CS (2013) H9N2 avian influenza virus in Korea: evolution and vaccination. Clin Exp Vaccine Res 2(1):26\u201333. https:\/\/doi.org\/10.7774\/cevr.2013.2.1.26","journal-title":"Clin Exp Vaccine Res"},{"issue":"1","key":"6018_CR4","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1016\/j.rvsc.2011.07.033","volume":"93","author":"S Shahsavandi","year":"2012","unstructured":"Shahsavandi S, Salmanian AH, Ghorashi SA, Masoudi S, Ebrahimi MM (2012) Evolutionary characterization of hemagglutinin gene of H9N2 influenza viruses isolated from Asia. Res Vet Sci 93(1):234\u2013239. https:\/\/doi.org\/10.1016\/j.rvsc.2011.07.033","journal-title":"Res Vet Sci"},{"issue":"10","key":"6018_CR5","doi-asserted-by":"publisher","first-page":"1931","DOI":"10.1007\/s00705-012-1385-9","volume":"157","author":"A Arafa","year":"2012","unstructured":"Arafa A, Suarez D, Kholosy SG, Hassan MK, Nasef S, Selim A, Dauphin G, Kim M, Yilma J, Swayne D, Aly MM (2012) Evolution of highly pathogenic avian influenza H5N1 viruses in Egypt indicating progressive adaptation. Arch Virol 157(10):1931\u20131947. https:\/\/doi.org\/10.1007\/s00705-012-1385-9","journal-title":"Arch Virol"},{"issue":"6","key":"6018_CR6","doi-asserted-by":"publisher","first-page":"1167","DOI":"10.1007\/s00705-012-1269-z","volume":"157","author":"EF El-Zoghby","year":"2012","unstructured":"El-Zoghby EF, Arafa AS, Hassan MK, Aly MM, Selim A, Kilany WH, Selim U, Nasef S, Aggor MG, Abdelwhab EM, Hafez HM (2012) Isolation of H9N2 avian influenza virus from bobwhite quail (Colinus virginianus) in Egypt. Arch Virol 157(6):1167\u20131172. https:\/\/doi.org\/10.1007\/s00705-012-1269-z","journal-title":"Arch Virol"},{"issue":"11","key":"6018_CR7","doi-asserted-by":"publisher","first-page":"2861","DOI":"10.1007\/s00705-014-2118-z","volume":"159","author":"A Kandeil","year":"2014","unstructured":"Kandeil A, El-Shesheny R, Maatouq AM, Moatasim Y, Shehata MM, Bagato O, Rubrum A, Shanmuganatham K, Webby RJ, Ali MA, Kayali G (2014) Genetic and antigenic evolution of H9N2 avian influenza viruses circulating in Egypt between 2011 and 2013. Arch Virol 159(11):2861\u20132876. https:\/\/doi.org\/10.1007\/s00705-014-2118-z","journal-title":"Arch Virol"},{"issue":"4","key":"6018_CR8","doi-asserted-by":"publisher","first-page":"548","DOI":"10.1099\/jgv.0.000657","volume":"98","author":"A Kandeil","year":"2017","unstructured":"Kandeil A, El-Shesheny R, Maatouq A, Moatasim Y, Cai Z, McKenzie P, Webby R, Kayali G, Ali MA (2017) Novel reassortant H9N2 viruses in pigeons and evidence for antigenic diversity of H9N2 viruses isolated from quails in Egypt. J Gen Virol 98(4):548\u2013562. https:\/\/doi.org\/10.1099\/jgv.0.000657","journal-title":"J Gen Virol"},{"issue":"7","key":"6018_CR9","doi-asserted-by":"publisher","first-page":"1484","DOI":"10.3390\/v14071484","volume":"14","author":"M El Sayes","year":"2022","unstructured":"El Sayes M, Kandeil A, Moatasim Y, El Taweel A, Rubrum A, Kutkat O, Kamel MN, Badra R, Barakat AB, McKenzie PP, El-Shesheny R, Webby RJ, Kayali G, Ali MA (2022) Insights into Genetic Characteristics and Virological Features of Endemic Avian Influenza A (H9N2) Viruses in Egypt from 2017\u20132021. Viruses 14(7):1484. https:\/\/doi.org\/10.3390\/v14071484","journal-title":"Viruses"},{"issue":"9","key":"6018_CR10","doi-asserted-by":"publisher","first-page":"497","DOI":"10.3390\/v10090497","volume":"10","author":"A Mostafa","year":"2018","unstructured":"Mostafa A, Abdelwhab EM, Mettenleiter TC, Pleschka S (2018) Zoonotic Potential of Influenza A Viruses: A Comprehensive Overview. Viruses 10(9):497. https:\/\/doi.org\/10.3390\/v10090497","journal-title":"Viruses"},{"issue":"3 Suppl","key":"6018_CR11","doi-asserted-by":"publisher","first-page":"828","DOI":"10.1637\/0005-2086-47.s3.828","volume":"47","author":"H Nili","year":"2003","unstructured":"Nili H, Asasi K (2003) Avian influenza (H9N2) outbreak in Iran. Avian Dis 47(3 Suppl):828\u2013831. https:\/\/doi.org\/10.1637\/0005-2086-47.s3.828","journal-title":"Avian Dis"},{"issue":"6","key":"6018_CR12","doi-asserted-by":"publisher","first-page":"e00929","DOI":"10.1128\/genomeA.00929-14","volume":"2","author":"Y Zhang","year":"2014","unstructured":"Zhang Y, Guo X, Qi J, Liu L, Wang J, Xu S, Wang J, Yin Y (2014) Complete Genome Sequence of an H9N2 Influenza Virus Lethal to Chickens. Genome Announc 2(6):e00929\u2013e00914. https:\/\/doi.org\/10.1128\/genomeA.00929-14","journal-title":"Genome Announc"},{"issue":"11","key":"6018_CR13","doi-asserted-by":"publisher","first-page":"5760","DOI":"10.1128\/JCM.43.11.5760-5767.2005","volume":"43","author":"KM Butt","year":"2005","unstructured":"Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, Lim W, Webster RG, Yuen KY, Peiris JS, Guan Y (2005) Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol 43(11):5760\u20135767. https:\/\/doi.org\/10.1128\/JCM.43.11.5760-5767.2005","journal-title":"J Clin Microbiol"},{"issue":"4","key":"6018_CR14","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1093\/infdis\/jiv109","volume":"212","author":"SU Khan","year":"2015","unstructured":"Khan SU, Anderson BD, Heil GL, Liang S, Gray GC (2015) A systematic review and meta-analysis of the seroprevalence of influenza A (H9N2) infection among humans. J Infect Dis 212(4):562\u2013569. https:\/\/doi.org\/10.1093\/infdis\/jiv109","journal-title":"J Infect Dis"},{"issue":"7","key":"6018_CR15","doi-asserted-by":"publisher","first-page":"620","DOI":"10.3390\/v11070620","volume":"11","author":"THP Peacock","year":"2019","unstructured":"Peacock THP, James J, Sealy JE, Iqbal M (2019) A Global Perspective on H9N2 Avian Influenza Virus. Viruses 11(7):620. https:\/\/doi.org\/10.3390\/v11070620","journal-title":"Viruses"},{"key":"6018_CR16","unstructured":"WHO (World Health Organization) (2022) Avian Influenza Weekly Update Number 836; WHO: Geneva, Switzerland"},{"issue":"5","key":"6018_CR17","doi-asserted-by":"publisher","first-page":"e02199","DOI":"10.1128\/JVI.02199-16","volume":"91","author":"L Yang","year":"2017","unstructured":"Yang L, Zhu W, Li X, Bo H, Zhang Y, Zou S, Gao R, Dong J, Zhao X, Chen W, Dong L, Zou X, Xing Y, Wang D, Shu Y (2017) Genesis and Dissemination of Highly Pathogenic H5N6 Avian Influenza Viruses. J Virol 91(5):e02199\u2013e02116. https:\/\/doi.org\/10.1128\/JVI.02199-16","journal-title":"J Virol"},{"issue":"7470","key":"6018_CR18","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1038\/nature12515","volume":"502","author":"TT Lam","year":"2013","unstructured":"Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y (2013) The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502(7470):241\u2013244. https:\/\/doi.org\/10.1038\/nature12515","journal-title":"Nature"},{"key":"6018_CR19","doi-asserted-by":"publisher","first-page":"1418","DOI":"10.1038\/ncomms2433","volume":"4","author":"YH Zhang","year":"2013","unstructured":"Zhang YH, Zhao Y, Li N, Peng YC, Giannoulatou E, Jin RH, Yan HP, Wu H, Liu JH, Liu N, Wang DY, Shu YL, Ho LP, Kellam P, McMichael A, Dong T (2013) Interferon-induced transmembrane protein-3 genetic variant rs12252-C is associated with severe influenza in Chinese individuals. Nat Commun 4:1418. https:\/\/doi.org\/10.1038\/ncomms2433","journal-title":"Nat Commun"},{"issue":"10","key":"6018_CR20","doi-asserted-by":"publisher","first-page":"1363","DOI":"10.1016\/j.chom.2022.09.003","volume":"30","author":"T Liu","year":"2022","unstructured":"Liu T, Wang Y, Tan TJC, Wu NC, Brooke CB (2022) The evolutionary potential of influenza A virus hemagglutinin is highly constrained by epistatic interactions with neuraminidase. Cell Host Microbe 30(10):1363\u20131369e4. https:\/\/doi.org\/10.1016\/j.chom.2022.09.003","journal-title":"Cell Host Microbe"},{"issue":"1","key":"6018_CR21","doi-asserted-by":"publisher","first-page":"e1004037","DOI":"10.1371\/journal.pgen.1004037","volume":"10","author":"AD Neverov","year":"2014","unstructured":"Neverov AD, Lezhnina KV, Kondrashov AS, Bazykin GA (2014) Intrasubtype reassortments cause adaptive amino acid replacements in H3N2 influenza genes. PLoS Genet 10(1):e1004037. https:\/\/doi.org\/10.1371\/journal.pgen.1004037","journal-title":"PLoS Genet"},{"issue":"2","key":"6018_CR22","doi-asserted-by":"publisher","first-page":"e17212","DOI":"10.1371\/journal.pone.0017212","volume":"6","author":"G Dong","year":"2011","unstructured":"Dong G, Luo J, Zhang H, Wang C, Duan M, Deliberto TJ, Nolte DL, Ji G, He H (2011) Phylogenetic diversity and genotypical complexity of H9N2 influenza A viruses revealed by genomic sequence analysis. PLoS ONE 6(2):e17212. https:\/\/doi.org\/10.1371\/journal.pone.0017212","journal-title":"PLoS ONE"},{"issue":"4","key":"6018_CR23","doi-asserted-by":"publisher","first-page":"82","DOI":"10.3390\/vetsci5040082","volume":"5","author":"EA Pusch","year":"2018","unstructured":"Pusch EA, Suarez DL (2018) The Multifaceted Zoonotic Risk of H9N2 Avian Influenza. Vet Sci 5(4):82. https:\/\/doi.org\/10.3390\/vetsci5040082","journal-title":"Vet Sci"},{"issue":"3 Suppl","key":"6018_CR24","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1637\/0005-2086-47.s3.1079","volume":"47","author":"E Spackman","year":"2003","unstructured":"Spackman E, Senne DA, Bulaga LL, Myers TJ, Perdue ML, Garber LP, Lohman K, Daum LT, Suarez DL (2003) Development of real-time RT-PCR for the detection of avian influenza virus. Avian Dis 47(3 Suppl):1079\u20131082. https:\/\/doi.org\/10.1637\/0005-2086-47.s3.1079","journal-title":"Avian Dis"},{"issue":"1\u20132","key":"6018_CR25","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/s0166-0934(01)00301-9","volume":"97","author":"MS Lee","year":"2001","unstructured":"Lee MS, Chang PC, Shien JH, Cheng MC, Shieh HK (2001) Identification and subtyping of avian influenza viruses by reverse transcription-PCR. J Virol Methods 97(1\u20132):13\u201322. https:\/\/doi.org\/10.1016\/s0166-0934(01)00301-9","journal-title":"J Virol Methods"},{"issue":"7","key":"6018_CR26","doi-asserted-by":"publisher","first-page":"2301","DOI":"10.1128\/JCM.02366-08","volume":"47","author":"K Tsukamoto","year":"2009","unstructured":"Tsukamoto K, Ashizawa T, Nakanishi K, Kaji N, Suzuki K, Shishido M, Okamatsu M, Mase M (2009) Use of reverse transcriptase PCR to subtype N1 to N9 neuraminidase genes of avian influenza viruses. J Clin Microbiol 47(7):2301\u20132303. https:\/\/doi.org\/10.1128\/JCM.02366-08","journal-title":"J Clin Microbiol"},{"issue":"7","key":"6018_CR27","doi-asserted-by":"publisher","first-page":"3022","DOI":"10.1093\/molbev\/msab120","volume":"38","author":"K Tamura","year":"2021","unstructured":"Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38(7):3022\u20133027. https:\/\/doi.org\/10.1093\/molbev\/msab120","journal-title":"Mol Biol Evol"},{"key":"6018_CR28","unstructured":"Gupta R, Jung E, Brunak S (2004) Prediction of N-glycosylation sites in human proteins"},{"issue":"2","key":"6018_CR29","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1093\/bioinformatics\/bti770","volume":"22","author":"K Arnold","year":"2006","unstructured":"Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22(2):195\u2013201. https:\/\/doi.org\/10.1093\/bioinformatics\/bti770","journal-title":"Bioinformatics"},{"issue":"4","key":"6018_CR30","doi-asserted-by":"publisher","first-page":"542","DOI":"10.3201\/eid2004.131295","volume":"20","author":"G Kayali","year":"2014","unstructured":"Kayali G, Kandeil A, El-Shesheny R, Kayed AS, Gomaa MM, Maatouq AM, Shehata MM, Moatasim Y, Bagato O, Cai Z, Rubrum A, Kutkat MA, McKenzie PP, Webster RG, Webby RJ, Ali MA (2014) Active surveillance for avian influenza virus, Egypt, 2010\u20132012. Emerg Infect Dis 20(4):542\u2013551. https:\/\/doi.org\/10.3201\/eid2004.131295","journal-title":"Emerg Infect Dis"},{"issue":"16","key":"6018_CR31","doi-asserted-by":"publisher","first-page":"3320","DOI":"10.1017\/S0950268817002576","volume":"145","author":"A Nagy","year":"2017","unstructured":"Nagy A, Mettenleiter TC, Abdelwhab EM (2017) A brief summary of the epidemiology and genetic relatedness of avian influenza H9N2 virus in birds and mammals in the Middle East and North Africa. Epidemiol Infect 145(16):3320\u20133333. https:\/\/doi.org\/10.1017\/S0950268817002576","journal-title":"Epidemiol Infect"},{"issue":"1","key":"6018_CR32","doi-asserted-by":"publisher","first-page":"129","DOI":"10.3201\/eid2601.190570","volume":"26","author":"KE Hassan","year":"2020","unstructured":"Hassan KE, King J, El-Kady M, Afifi M, Abozeid HH, Pohlmann A, Beer M, Harder T (2020) Novel Reassortant Highly Pathogenic Avian Influenza A(H5N2) Virus in Broiler Chickens, Egypt. Emerg Infect Dis 26(1):129\u2013133. https:\/\/doi.org\/10.3201\/eid2601.190570","journal-title":"Emerg Infect Dis"},{"issue":"10","key":"6018_CR33","doi-asserted-by":"publisher","first-page":"7579","DOI":"10.1128\/JVI.71.10.7579-7585.1997","volume":"71","author":"RJ Callan","year":"1997","unstructured":"Callan RJ, Hartmann FA, West SE, Hinshaw VS (1997) Cleavage of influenza A virus H1 hemagglutinin by swine respiratory bacterial proteases. J Virol 71(10):7579\u20137585. https:\/\/doi.org\/10.1128\/JVI.71.10.7579-7585.1997","journal-title":"J Virol"},{"issue":"4","key":"6018_CR34","doi-asserted-by":"publisher","first-page":"1617","DOI":"10.1128\/jvi.76.4.1617-1625.2002","volume":"76","author":"OP Zhirnov","year":"2002","unstructured":"Zhirnov OP, Konakova TE, Wolff T, Klenk HD (2002) NS1 protein of influenza A virus down-regulates apoptosis. J Virol 76(4):1617\u20131625. https:\/\/doi.org\/10.1128\/jvi.76.4.1617-1625.2002","journal-title":"J Virol"},{"issue":"5","key":"6018_CR35","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1002\/rmv.657","volume":"20","author":"S Bertram","year":"2010","unstructured":"Bertram S, Glowacka I, Steffen I, K\u00fchl A, P\u00f6hlmann S (2010) Novel insights into proteolytic cleavage of influenza virus hemagglutinin. Rev Med Virol 20(5):298\u2013310. https:\/\/doi.org\/10.1002\/rmv.657","journal-title":"Rev Med Virol"},{"issue":"18","key":"6018_CR36","doi-asserted-by":"publisher","first-page":"7565","DOI":"10.1073\/pnas.0900877106","volume":"106","author":"EM Sorrell","year":"2009","unstructured":"Sorrell EM, Wan H, Araya Y, Song H, Perez DR (2009) Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Natl Acad Sci U S A 106(18):7565\u20137570. https:\/\/doi.org\/10.1073\/pnas.0900877106","journal-title":"Proc Natl Acad Sci U S A"},{"key":"6018_CR37","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1159\/000151617","volume":"27","author":"MN Matrosovich","year":"2008","unstructured":"Matrosovich MN, Gambaryan AS, Klenk HD (2008) Receptor specificity of influenza viruses and its alteration during interspecies transmission. Avian influenza 27:134\u2013155 Karger Publishers. https:\/\/doi.org\/10.1159\/000151617","journal-title":"Avian influenza"},{"issue":"10","key":"6018_CR38","doi-asserted-by":"publisher","first-page":"5181","DOI":"10.1128\/JVI.02827-06","volume":"81","author":"H Wan","year":"2007","unstructured":"Wan H, Perez DR (2007) Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. J Virol 81(10):5181\u20135191. https:\/\/doi.org\/10.1128\/JVI.02827-06","journal-title":"J Virol"},{"issue":"5","key":"6018_CR39","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1142\/s0219720008003813","volume":"6","author":"XF Wan","year":"2008","unstructured":"Wan XF, Ozden M, Lin G (2008) Ubiquitous reassortments in influenza A viruses. J Bioinform Comput Biol 6(5):981\u2013999. https:\/\/doi.org\/10.1142\/s0219720008003813","journal-title":"J Bioinform Comput Biol"},{"issue":"Pt 12","key":"6018_CR40","doi-asserted-by":"publisher","first-page":"3067","DOI":"10.1099\/0022-1317-83-12-3067","volume":"83","author":"E Tsuchiya","year":"2002","unstructured":"Tsuchiya E, Sugawara K, Hongo S, Matsuzaki Y, Muraki Y, Nakamura K (2002) Role of overlapping glycosylation sequons in antigenic properties, intracellular transport and biological activities of influenza A\/H2N2 virus haemagglutinin. J Gen Virol 83(Pt 12):3067\u20133074. https:\/\/doi.org\/10.1099\/0022-1317-83-12-3067","journal-title":"J Gen Virol"},{"issue":"23","key":"6018_CR41","doi-asserted-by":"publisher","first-page":"12911","DOI":"10.1128\/JVI.01522-07","volume":"81","author":"NV Kaverin","year":"2007","unstructured":"Kaverin NV, Rudneva IA, Govorkova EA, Timofeeva TA, Shilov AA, Kochergin-Nikitsky KS, Krylov PS, Webster RG (2007) Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. J Virol 81(23):12911\u201312917. https:\/\/doi.org\/10.1128\/JVI.01522-07","journal-title":"J Virol"},{"issue":"6","key":"6018_CR42","doi-asserted-by":"publisher","first-page":"e5788","DOI":"10.1371\/journal.pone.0005788","volume":"4","author":"M Iqbal","year":"2009","unstructured":"Iqbal M, Yaqub T, Reddy K, McCauley JW (2009) Novel genotypes of H9N2 influenza A viruses isolated from poultry in Pakistan containing NS genes similar to highly pathogenic H7N3 and H5N1 viruses. PLoS ONE 4(6):e5788. https:\/\/doi.org\/10.1371\/journal.pone.0005788","journal-title":"PLoS ONE"},{"issue":"2","key":"6018_CR43","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1006\/viro.2000.0799","volume":"281","author":"MN Matrosovich","year":"2001","unstructured":"Matrosovich MN, Krauss S, Webster RG (2001) H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281(2):156\u2013162. https:\/\/doi.org\/10.1006\/viro.2000.0799","journal-title":"Virology"},{"issue":"12","key":"6018_CR44","doi-asserted-by":"publisher","first-page":"2526","DOI":"10.3382\/ps.2009-00262","volume":"88","author":"S Rashid","year":"2009","unstructured":"Rashid S, Naeem K, Ahmed Z, Saddique N, Abbas MA, Malik SA (2009) Multiplex polymerase chain reaction for the detection and differentiation of avian influenza viruses and other poultry respiratory pathogens. Poult Sci 88(12):2526\u20132531. https:\/\/doi.org\/10.3382\/ps.2009-00262","journal-title":"Poult Sci"},{"issue":"9","key":"6018_CR45","doi-asserted-by":"publisher","first-page":"1353","DOI":"10.3201\/eid1209.060276","volume":"12","author":"GW Chen","year":"2006","unstructured":"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 influenza A viruses. Emerg Infect Dis 12(9):1353\u20131360. https:\/\/doi.org\/10.3201\/eid1209.060276","journal-title":"Emerg Infect Dis"},{"key":"6018_CR46","doi-asserted-by":"publisher","first-page":"5021","DOI":"10.1038\/ncomms6021","volume":"5","author":"S Fan","year":"2014","unstructured":"Fan S, Hatta M, Kim JH, Halfmann P, Imai M, Macken CA, Le MQ, Nguyen T, Neumann G, Kawaoka Y (2014) Novel residues in avian influenza virus PB2 protein affect virulence in mammalian hosts. Nat Commun 5:5021. https:\/\/doi.org\/10.1038\/ncomms6021","journal-title":"Nat Commun"},{"key":"6018_CR47","doi-asserted-by":"publisher","first-page":"7491","DOI":"10.1038\/ncomms8491","volume":"6","author":"AS Taft","year":"2015","unstructured":"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","journal-title":"Nat Commun"},{"issue":"13","key":"6018_CR48","doi-asserted-by":"publisher","first-page":"6673","DOI":"10.1128\/JVI.00212-09","volume":"83","author":"T Rolling","year":"2009","unstructured":"Rolling T, Koerner I, Zimmermann P, Holz K, Haller O, Staeheli P, Kochs G (2009) Adaptive mutations resulting in enhanced polymerase activity contribute to high virulence of influenza A virus in mice. J Virol 83(13):6673\u20136680. https:\/\/doi.org\/10.1128\/JVI.00212-09","journal-title":"J Virol"},{"issue":"16","key":"6018_CR49","doi-asserted-by":"publisher","first-page":"8515","DOI":"10.1128\/JVI.00435-07","volume":"81","author":"DJ Hulse-Post","year":"2007","unstructured":"Hulse-Post DJ, Franks J, Boyd K, Salomon R, Hoffmann E, Yen HL, Webby RJ, Walker D, Nguyen TD, Webster RG (2007) Molecular changes in the polymerase genes (PA and PB1) associated with high pathogenicity of H5N1 influenza virus in mallard ducks. J Virol 81(16):8515\u20138524. https:\/\/doi.org\/10.1128\/JVI.00435-07","journal-title":"J Virol"},{"issue":"51","key":"6018_CR50","doi-asserted-by":"publisher","first-page":"18590","DOI":"10.1073\/pnas.0507415102","volume":"102","author":"G Gabriel","year":"2005","unstructured":"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(51):18590\u201318595. https:\/\/doi.org\/10.1073\/pnas.0507415102.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5536","key":"6018_CR51","doi-asserted-by":"publisher","first-page":"1840","DOI":"10.1126\/science.1062882","volume":"293","author":"M Hatta","year":"2001","unstructured":"Hatta M, Gao P, Halfmann P, Kawaoka Y (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293(5536):1840\u20131842. https:\/\/doi.org\/10.1126\/science.1062882","journal-title":"Science"},{"key":"6018_CR52","doi-asserted-by":"publisher","first-page":"10510","DOI":"10.1038\/srep10510","volume":"5","author":"J Song","year":"2015","unstructured":"Song J, Xu J, Shi J, Li Y, Chen H (2015) Synergistic Effect of S224P and N383D Substitutions in the PA of H5N1 Avian Influenza Virus Contributes to Mammalian Adaptation. Sci Rep 5:10510. https:\/\/doi.org\/10.1038\/srep10510","journal-title":"Sci Rep"},{"issue":"1","key":"6018_CR53","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1111\/irv.12412","volume":"11","author":"U Joseph","year":"2017","unstructured":"Joseph U, Su YC, Vijaykrishna D, Smith GJ (2017) The ecology and adaptive evolution of influenza A interspecies transmission. Influenza Other Respir Viruses 11(1):74\u201384. https:\/\/doi.org\/10.1111\/irv.12412","journal-title":"Influenza Other Respir Viruses"},{"key":"6018_CR54","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1186\/1743-422X-6-67","volume":"6","author":"Y Furuse","year":"2009","unstructured":"Furuse Y, Suzuki A, Kamigaki T, Oshitani H (2009) Evolution of the M gene of the influenza A virus in different host species: large-scale sequence analysis. Virol J 6:67. https:\/\/doi.org\/10.1186\/1743-422X-6-67","journal-title":"Virol J"},{"issue":"5","key":"6018_CR55","doi-asserted-by":"publisher","first-page":"323","DOI":"10.2217\/fvl-2017-0151","volume":"13","author":"Y Jie","year":"2018","unstructured":"Jie Y, Zheng H, Xiaolei L, Xinhua O, Dong Y, Yingchun S, Lingzhi L, Rengui Y (2018) Full-length genome analysis of an avian influenza A virus (H9N2) from a human infection in Changsha City. Future Virol 13(5):323\u2013330. https:\/\/doi.org\/10.2217\/fvl-2017-0151","journal-title":"Future Virol"},{"issue":"1","key":"6018_CR56","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1002\/jmv.2118","volume":"66","author":"M Shaw","year":"2002","unstructured":"Shaw M, Cooper L, Xu X, Thompson W, Krauss S, Guan Y, Zhou N, Klimov A, Cox N, Webster R, Lim W, Shortridge K, Subbarao K (2002) Molecular changes associated with the transmission of avian influenza a H5N1 and H9N2 viruses to humans. J Med Virol 66(1):107\u2013114. https:\/\/doi.org\/10.1002\/jmv.2118","journal-title":"J Med Virol"},{"issue":"13","key":"6018_CR57","doi-asserted-by":"publisher","first-page":"6733","DOI":"10.1128\/JVI.02427-09","volume":"84","author":"SM Soubies","year":"2010","unstructured":"Soubies SM, Volmer C, Croville G, Loupias J, Peralta B, Costes P, Lacroux C, Gu\u00e9rin JL, Volmer R (2010) Species-specific contribution of the four C-terminal amino acids of influenza A virus NS1 protein to virulence. J Virol 84(13):6733\u20136747. https:\/\/doi.org\/10.1128\/JVI.02427-09","journal-title":"J Virol"},{"issue":"1","key":"6018_CR58","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.virol.2006.01.005","volume":"349","author":"S Li","year":"2006","unstructured":"Li S, Min JY, Krug RM, Sen GC (2006) Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349(1):13\u201321. https:\/\/doi.org\/10.1016\/j.virol.2006.01.005","journal-title":"Virology"},{"issue":"3","key":"6018_CR59","doi-asserted-by":"publisher","first-page":"1146","DOI":"10.1128\/JVI.01698-07","volume":"82","author":"P Jiao","year":"2008","unstructured":"Jiao P, Tian G, Li Y, Deng G, Jiang Y, Liu C, Liu W, Bu Z, Kawaoka Y, Chen H (2008) A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 82(3):1146\u20131154. https:\/\/doi.org\/10.1128\/JVI.01698-07","journal-title":"J Virol"},{"issue":"5349","key":"6018_CR60","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1126\/science.279.5349.393","volume":"279","author":"K Subbarao","year":"1998","unstructured":"Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, Perdue M, Swayne D, Bender C, Huang J, Hemphill M, Cox N (1998) Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279(5349):393\u2013396","journal-title":"Science"},{"issue":"7","key":"6018_CR61","doi-asserted-by":"publisher","first-page":"e40752","DOI":"10.1371\/journal.pone.0040752","volume":"7","author":"J Wang","year":"2012","unstructured":"Wang J, Sun Y, Xu Q, Tan Y, Pu J, Yang H, Brown EG, Liu J (2012) Mouse-adapted H9N2 influenza A virus PB2 protein M147L and E627K mutations are critical for high virulence. PLoS ONE 7(7):e40752","journal-title":"PLoS ONE"},{"issue":"1","key":"6018_CR62","doi-asserted-by":"publisher","first-page":"e01180","DOI":"10.1128\/JVI.01180-19","volume":"94","author":"H Kong","year":"2019","unstructured":"Kong H, Ma S, Wang J, Gu C, Wang Z, Shi J, Deng G, Guan Y, Chen H (2019) Identification of key amino acids in the PB2 and M1 proteins of H7N9 influenza virus that affect its transmission in guinea pigs. J Virol 94(1):e01180\u2013e01119","journal-title":"J Virol"},{"issue":"3\u20134","key":"6018_CR63","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.vetmic.2007.04.021","volume":"124","author":"MS Lee","year":"2007","unstructured":"Lee MS, Deng MC, Lin YJ, Chang CY, Shieh HK, Shiau JZ, Huang CC (2007) Characterization of an H5N1 avian influenza virus from Taiwan. Vet Microbiol 124(3\u20134):193\u2013201","journal-title":"Vet Microbiol"},{"issue":"10","key":"6018_CR64","doi-asserted-by":"publisher","first-page":"e141","DOI":"10.1371\/journal.ppat.0030141","volume":"3","author":"GM Conenello","year":"2007","unstructured":"Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P (2007) A single mutation in the PB1-F2 of H5N1 (HK\/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog 3(10):e141","journal-title":"PLoS Pathog"},{"issue":"5","key":"6018_CR65","doi-asserted-by":"publisher","first-page":"2706","DOI":"10.1128\/JVI.05546-11","volume":"86","author":"AL Suguitan Jr","year":"2012","unstructured":"Suguitan AL Jr, Matsuoka Y, Lau YF, Santos CP, Vogel L, Cheng LI, Orandle M, Subbarao K (2012) The multibasic cleavage site of the hemagglutinin of highly pathogenic A\/Vietnam\/1203\/2004 (H5N1) avian influenza virus acts as a virulence factor in a host-specific manner in mammals. J Virol 86(5):2706\u20132714","journal-title":"J Virol"},{"key":"6018_CR66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1743-422X-8-13","volume":"8","author":"SK Dankar","year":"2011","unstructured":"Dankar SK, Wang S, Ping J, Forbes NE, Keleta L, Li Y, Brown EG (2011) Influenza A virus NS1 gene mutations F103L and M106I increase replication and virulence. Virol J 8:1\u201313","journal-title":"Virol J"},{"key":"6018_CR67","doi-asserted-by":"publisher","first-page":"1770","DOI":"10.1007\/PL00000657","volume":"57","author":"K Subbarao","year":"2000","unstructured":"Subbarao K, Katz J (2000) Avian influenza viruses infecting humans. CMLS 57:1770\u20131784","journal-title":"CMLS"},{"issue":"19","key":"6018_CR68","doi-asserted-by":"publisher","first-page":"9901","DOI":"10.1128\/JVI.00608-09","volume":"83","author":"SJ Lycett","year":"2009","unstructured":"Lycett SJ, Ward MJ, Lewis FI, Poon AFY, Kosakovsky Pond SL, Brown AL (2009) Detection of mammalian virulence determinants in highly pathogenic avian influenza H5N1 viruses: multivariate analysis of published data. J Virol 83(19):9901\u20139910","journal-title":"J Virol"},{"issue":"2","key":"6018_CR69","doi-asserted-by":"publisher","first-page":"e01530","DOI":"10.1128\/JVI.01530-19","volume":"94","author":"S Ma","year":"2020","unstructured":"Ma S, Zhang B, Shi J, Yin X, Wang G, Cui P, Liu L, Deng G, Jiang Y, Li C, Chen H (2020) Amino acid mutations A286V and T437M in the nucleoprotein attenuate H7N9 viruses in mice. J Virol 94(2):e01530\u2013e01519","journal-title":"J Virol"}],"container-title":["Archives of Virology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00705-024-06018-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00705-024-06018-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00705-024-06018-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,23]],"date-time":"2024-05-23T13:05:06Z","timestamp":1716469506000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00705-024-06018-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,16]]},"references-count":69,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2024,5]]}},"alternative-id":["6018"],"URL":"https:\/\/doi.org\/10.1007\/s00705-024-06018-2","relation":{},"ISSN":["0304-8608","1432-8798"],"issn-type":[{"value":"0304-8608","type":"print"},{"value":"1432-8798","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,16]]},"assertion":[{"value":"14 December 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 February 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 April 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"99"}}