{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T21:46:59Z","timestamp":1792014419749,"version":"4.4.0"},"update-to":[{"DOI":"10.1371\/journal.ppat.1008816","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,9,9]],"date-time":"2020-09-09T00:00:00Z","timestamp":1599609600000}}],"reference-count":55,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2020,8,27]],"date-time":"2020-08-27T00:00:00Z","timestamp":1598486400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004543","name":"China Scholarship Council","doi-asserted-by":"publisher","award":["201603250057"],"award-info":[{"award-number":["201603250057"]}],"id":[{"id":"10.13039\/501100004543","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009578","name":"Mizutani Foundation for Glycoscience","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009578","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"DOI":"10.1371\/journal.ppat.1008816","type":"journal-article","created":{"date-parts":[[2020,8,27]],"date-time":"2020-08-27T17:53:39Z","timestamp":1598550819000},"page":"e1008816","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":36,"title":["Mutation of the second sialic acid-binding site of influenza A virus neuraminidase drives compensatory mutations in hemagglutinin"],"prefix":"10.1371","volume":"16","author":[{"given":"Wenjuan","family":"Du","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4864-0026","authenticated-orcid":true,"given":"Margreet A.","family":"Wolfert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3575-0680","authenticated-orcid":true,"given":"Ben","family":"Peeters","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5800-749X","authenticated-orcid":true,"given":"Frank J. M.","family":"van Kuppeveld","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3111-5954","authenticated-orcid":true,"given":"Geert-Jan","family":"Boons","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erik","family":"de Vries","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4459-9874","authenticated-orcid":true,"given":"Cornelis A. M.","family":"de Haan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2020,8,27]]},"reference":[{"issue":"18","key":"ppat.1008816.ref001","doi-asserted-by":"crossref","first-page":"8502","DOI":"10.1128\/JVI.74.18.8502-8512.2000","article-title":"Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals","volume":"74","author":"M Matrosovich","year":"2000","journal-title":"J Virol"},{"issue":"7468","key":"ppat.1008816.ref002","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/nature12392","article-title":"Characterization of H7N9 influenza A viruses isolated from humans","volume":"501","author":"T Watanabe","year":"2013","journal-title":"Nature"},{"issue":"2","key":"ppat.1008816.ref003","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1006\/viro.2000.0799","article-title":"H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity","volume":"281","author":"MN Matrosovich","year":"2001","journal-title":"Virology"},{"issue":"9","key":"ppat.1008816.ref004","article-title":"Mutation of the Second Sialic Acid-Binding Site, Resulting in Reduced Neuraminidase Activity, Preceded the Emergence of H7N9 Influenza A Virus.","volume":"91","author":"M Dai","year":"2017","journal-title":"J Virol"},{"issue":"20","key":"ppat.1008816.ref005","first-page":"e01243","article-title":"Substrate Binding by the Second Sialic Acid-Binding Site of Influenza A Virus N1 Neuraminidase Contributes to Enzymatic Activity","volume":"92","author":"W Du","year":"2018","journal-title":"Journal of virology"},{"issue":"4","key":"ppat.1008816.ref006","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1111\/j.1750-2659.2011.00304.x","article-title":"Influenza neuraminidase.","volume":"6","author":"GM Air","year":"2012","journal-title":"Influenza and other respiratory viruses."},{"key":"ppat.1008816.ref007","doi-asserted-by":"crossref","first-page":"39","DOI":"10.3389\/fmicb.2019.00039","article-title":"Influenza Virus Neuraminidase Structure and Functions.","volume":"10","author":"JL McAuley","year":"2019","journal-title":"Frontiers in microbiology"},{"issue":"1","key":"ppat.1008816.ref008","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/0042-6822(91)90003-T","article-title":"The N2 neuraminidase of human influenza virus has acquired a substrate specificity complementary to the hemagglutinin receptor specificity","volume":"180","author":"LG Baum","year":"1991","journal-title":"Virology"},{"issue":"17","key":"ppat.1008816.ref009","doi-asserted-by":"crossref","first-page":"9221","DOI":"10.1128\/JVI.00697-12","article-title":"Functional balance of the hemagglutinin and neuraminidase activities accompanies the emergence of the 2009 H1N1 influenza pandemic","volume":"86","author":"R Xu","year":"2012","journal-title":"J Virol"},{"issue":"7","key":"ppat.1008816.ref010","doi-asserted-by":"crossref","DOI":"10.3390\/ijms18071541","article-title":"The Interplay between the Host Receptor and Influenza Virus Hemagglutinin and Neuraminidase.","volume":"18","author":"L Byrd-Leotis","year":"2017","journal-title":"Int J Mol Sci"},{"key":"ppat.1008816.ref011","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1186\/1471-2148-13-222","article-title":"Evolutionary interactions between haemagglutinin and neuraminidase in avian influenza","volume":"13","author":"MJ Ward","year":"2013","journal-title":"BMC Evol Biol"},{"key":"ppat.1008816.ref012","article-title":"Influenza A Virus Hemagglutinin-Neuraminidase-Receptor Balance: Preserving Virus Motility","author":"E de Vries","year":"2019","journal-title":"Trends Microbiol"},{"issue":"8","key":"ppat.1008816.ref013","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1002\/embj.201387442","article-title":"Role of receptor binding specificity in influenza A virus transmission and pathogenesis","volume":"33","author":"M de Graaf","year":"2014","journal-title":"Embo j"},{"issue":"1","key":"ppat.1008816.ref014","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.chom.2016.11.004","article-title":"Recent H3N2 Viruses Have Evolved Specificity for Extended, Branched Human-type Receptors, Conferring Potential for Increased Avidity","volume":"21","author":"W Peng","year":"2017","journal-title":"Cell Host Microbe"},{"issue":"2","key":"ppat.1008816.ref015","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.coviro.2012.03.003","article-title":"The role of receptor binding specificity in interspecies transmission of influenza viruses","volume":"2","author":"M Imai","year":"2012","journal-title":"Curr Opin Virol"},{"issue":"6","key":"ppat.1008816.ref016","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1007\/s00705-009-0393-x","article-title":"Functional significance of the hemadsorption activity of influenza virus neuraminidase and its alteration in pandemic viruses","volume":"154","author":"J Uhlendorff","year":"2009","journal-title":"Arch Virol"},{"issue":"22","key":"ppat.1008816.ref017","doi-asserted-by":"crossref","first-page":"11808","DOI":"10.1073\/pnas.94.22.11808","article-title":"Structural evidence for a second sialic acid binding site in avian influenza virus neuraminidases","volume":"94","author":"JN Varghese","year":"1997","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"16","key":"ppat.1008816.ref018","doi-asserted-by":"crossref","first-page":"9197","DOI":"10.1128\/JVI.00805-14","article-title":"Structure of influenza virus N7: the last piece of the neuraminidase \"jigsaw\" puzzle.","volume":"88","author":"X Sun","year":"2014","journal-title":"J Virol"},{"issue":"9","key":"ppat.1008816.ref019","doi-asserted-by":"crossref","first-page":"2221","DOI":"10.1002\/anie.201108245","article-title":"A secondary sialic acid binding site on influenza virus neuraminidase: fact or fiction?","volume":"51","author":"JC Lai","year":"2012","journal-title":"Angew Chem Int Ed Engl"},{"issue":"6","key":"ppat.1008816.ref020","doi-asserted-by":"crossref","first-page":"e1007860","DOI":"10.1371\/journal.ppat.1007860","article-title":"The 2nd sialic acid-binding site of influenza A virus neuraminidase is an important determinant of the hemagglutinin-neuraminidase-receptor balance.","volume":"15","author":"W Du","year":"2019","journal-title":"PLOS Pathogens."},{"issue":"9","key":"ppat.1008816.ref021","doi-asserted-by":"crossref","first-page":"6706","DOI":"10.1128\/JVI.71.9.6706-6713.1997","article-title":"Neuraminidase hemadsorption activity, conserved in avian influenza A viruses, does not influence viral replication in ducks","volume":"71","author":"D Kobasa","year":"1997","journal-title":"J Virol"},{"issue":"11","key":"ppat.1008816.ref022","doi-asserted-by":"crossref","DOI":"10.1128\/JVI.02293-16","article-title":"Role of Neuraminidase in Influenza A(H7N9) Virus Receptor Binding.","volume":"91","author":"DJ Benton","year":"2017","journal-title":"J Virol"},{"issue":"7","key":"ppat.1008816.ref023","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1134\/S000629791507007X","article-title":"What adaptive changes in hemagglutinin and neuraminidase are necessary for emergence of pandemic influenza virus from its avian precursor?","volume":"80","author":"AS Gambaryan","year":"2015","journal-title":"Biochemistry (Mosc)."},{"issue":"8","key":"ppat.1008816.ref024","doi-asserted-by":"crossref","first-page":"e1007233","DOI":"10.1371\/journal.ppat.1007233","article-title":"Kinetic analysis of the influenza A virus HA\/NA balance reveals contribution of NA to virus-receptor binding and NA-dependent rolling on receptor-containing surfaces.","volume":"14","author":"H Guo","year":"2018","journal-title":"PLoS Pathog."},{"issue":"2","key":"ppat.1008816.ref025","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1016\/j.virol.2005.08.035","article-title":"Evolution of the receptor binding phenotype of influenza A (H5) viruses.","volume":"344","author":"A Gambaryan","year":"2006","journal-title":"Virology"},{"issue":"1","key":"ppat.1008816.ref026","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.virol.2011.10.006","article-title":"In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity.","volume":"422","author":"L-M Chen","year":"2012","journal-title":"Virology"},{"issue":"11","key":"ppat.1008816.ref027","doi-asserted-by":"crossref","first-page":"e7836","DOI":"10.1371\/journal.pone.0007836","article-title":"Mutations in H5N1 influenza virus hemagglutinin that confer binding to human tracheal airway epithelium.","volume":"4","author":"G Ayora-Talavera","year":"2009","journal-title":"PLoS One."},{"issue":"36","key":"ppat.1008816.ref028","doi-asserted-by":"crossref","first-page":"12915","DOI":"10.1073\/pnas.0506416102","article-title":"Role of specific hemagglutinin amino acids in the immunogenicity and protection of H5N1 influenza virus vaccines","volume":"102","author":"E Hoffmann","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"7117","key":"ppat.1008816.ref029","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1038\/nature05264","article-title":"Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors","volume":"444","author":"S Yamada","year":"2006","journal-title":"Nature"},{"key":"ppat.1008816.ref030","first-page":"456","article-title":"Enhanced human receptor binding by H5 haemagglutinins","author":"X Xiong","year":"2014","journal-title":"Virology"},{"key":"ppat.1008816.ref031","first-page":"479","article-title":"Transmission of influenza A viruses","author":"G Neumann","year":"2015","journal-title":"Virology"},{"issue":"23","key":"ppat.1008816.ref032","doi-asserted-by":"crossref","first-page":"4121","DOI":"10.1093\/bioinformatics\/bty407","article-title":"Nextstrain: real-time tracking of pathogen evolution","volume":"34","author":"J Hadfield","year":"2018","journal-title":"Bioinformatics"},{"issue":"2","key":"ppat.1008816.ref033","doi-asserted-by":"crossref","first-page":"e00081","DOI":"10.1128\/mBio.00081-15","article-title":"Characterization of H5N1 Influenza Virus Variants with Hemagglutinin Mutations Isolated from Patients.","volume":"6","author":"Y Watanabe","year":"2015","journal-title":"mBio"},{"issue":"1","key":"ppat.1008816.ref034","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/S0168-1702(01)00272-6","article-title":"Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture","volume":"79","author":"SJ Baigent","year":"2001","journal-title":"Virus Research"},{"issue":"2","key":"ppat.1008816.ref035","doi-asserted-by":"crossref","first-page":"1146","DOI":"10.1128\/JVI.73.2.1146-1155.1999","article-title":"The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties","volume":"73","author":"M Matrosovich","year":"1999","journal-title":"Journal of virology"},{"issue":"6088","key":"ppat.1008816.ref036","doi-asserted-by":"crossref","first-page":"1534","DOI":"10.1126\/science.1213362","article-title":"Airborne transmission of influenza A\/H5N1 virus between ferrets","volume":"336","author":"S Herfst","year":"2012","journal-title":"Science"},{"issue":"7449","key":"ppat.1008816.ref037","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1038\/nature12144","article-title":"Receptor binding by a ferret-transmissible H5 avian influenza virus","volume":"497","author":"X Xiong","year":"2013","journal-title":"Nature"},{"issue":"1328","key":"ppat.1008816.ref038","article-title":"Adaptive Evolution of Human-Isolated H5Nx Avian Influenza A Viruses.","volume":"10","author":"F Guo","year":"2019","journal-title":"Frontiers in Microbiology."},{"key":"ppat.1008816.ref039","doi-asserted-by":"crossref","first-page":"3058","DOI":"10.1038\/srep03058","article-title":"Adaptation of novel H7N9 influenza A virus to human receptors.","volume":"3","author":"JC Dortmans","year":"2013","journal-title":"Sci Rep."},{"issue":"1","key":"ppat.1008816.ref040","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1006\/viro.1994.1615","article-title":"Receptor Specificity in Human, Avian, and Equine H2 and H3 Influenza Virus Isolates.","volume":"205","author":"RJ Connor","year":"1994","journal-title":"Virology"},{"issue":"5921","key":"ppat.1008816.ref041","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1038\/304076a0","article-title":"Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity","volume":"304","author":"GN Rogers","year":"1983","journal-title":"Nature"},{"issue":"6163","key":"ppat.1008816.ref042","doi-asserted-by":"crossref","first-page":"1230","DOI":"10.1126\/science.1243761","article-title":"Preferential recognition of avian-like receptors in human influenza A H7N9 viruses","volume":"342","author":"R Xu","year":"2013","journal-title":"Science"},{"issue":"25\u201326","key":"ppat.1008816.ref043","doi-asserted-by":"crossref","first-page":"3165","DOI":"10.1016\/S0264-410X(02)00268-2","article-title":"Eight-plasmid system for rapid generation of influenza virus vaccines","volume":"20","author":"E Hoffmann","year":"2002","journal-title":"Vaccine"},{"key":"ppat.1008816.ref044","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.virol.2017.01.012","article-title":"Genetic versus antigenic differences among highly pathogenic H5N1 avian influenza A viruses: Consequences for vaccine strain selection","volume":"503","author":"B Peeters","year":"2017","journal-title":"Virology"},{"issue":"5","key":"ppat.1008816.ref045","doi-asserted-by":"crossref","first-page":"e10645","DOI":"10.1371\/journal.pone.0010645","article-title":"A single immunization with soluble recombinant trimeric hemagglutinin protects chickens against highly pathogenic avian influenza virus H5N1.","volume":"5","author":"LAHM Cornelissen","year":"2010","journal-title":"PloS one"},{"key":"ppat.1008816.ref046","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1186\/1472-6750-8-41","article-title":"In vivo site-specific biotinylation of proteins within the secretory pathway using a single vector system","volume":"8","author":"A Predonzani","year":"2008","journal-title":"BMC Biotechnol"},{"issue":"6044","key":"ppat.1008816.ref047","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1126\/science.1205669","article-title":"A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins","volume":"333","author":"D Corti","year":"2011","journal-title":"Science"},{"issue":"8","key":"ppat.1008816.ref048","doi-asserted-by":"crossref","first-page":"e71072","DOI":"10.1371\/journal.pone.0071072","article-title":"A protective and safe intranasal RSV vaccine based on a recombinant prefusion-like form of the F protein bound to bacterium-like particles","volume":"8","author":"A Rigter","year":"2013","journal-title":"PLoS One"},{"issue":"21","key":"ppat.1008816.ref049","doi-asserted-by":"crossref","first-page":"13419","DOI":"10.1073\/pnas.212519299","article-title":"Structure and function in rhodopsin: High-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible &lt;em&gt;N&lt;\/em&gt;-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line.","volume":"99","author":"PJ Reeves","year":"2002","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"ppat.1008816.ref050","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.virol.2010.03.047","article-title":"The influenza A virus hemagglutinin glycosylation state affects receptor-binding specificity","volume":"403","author":"RP de Vries","year":"2010","journal-title":"Virology"},{"issue":"20","key":"ppat.1008816.ref051","doi-asserted-by":"crossref","first-page":"9457","DOI":"10.1128\/JVI.01346-16","article-title":"Identification of Residues That Affect Oligomerization and\/or Enzymatic Activity of Influenza Virus H5N1 Neuraminidase Proteins","volume":"90","author":"M Dai","year":"2016","journal-title":"J Virol"},{"issue":"11","key":"ppat.1008816.ref052","doi-asserted-by":"crossref","first-page":"3284","DOI":"10.1016\/j.celrep.2019.05.048","article-title":"N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses.","volume":"27","author":"F Broszeit","year":"2019","journal-title":"Cell Reports"},{"issue":"2","key":"ppat.1008816.ref053","doi-asserted-by":"crossref","first-page":"220","DOI":"10.3201\/eid2302.161072","article-title":"Highly Pathogenic Influenza A(H5Nx) Viruses with Altered H5 Receptor-Binding Specificity.","volume":"23","author":"H Guo","year":"2017","journal-title":"Emerg Infect Dis"},{"issue":"31","key":"ppat.1008816.ref054","doi-asserted-by":"crossref","first-page":"10547","DOI":"10.1002\/anie.201903140","article-title":"Protecting-Group-Controlled Enzymatic Glycosylation of Oligo-N-Acetyllactosamine Derivatives","volume":"58","author":"IA Gagarinov","year":"2019","journal-title":"Angew Chem Int Ed Engl"},{"issue":"31","key":"ppat.1008816.ref055","doi-asserted-by":"crossref","first-page":"10547","DOI":"10.1002\/anie.201903140","article-title":"Protecting-Group-Controlled Enzymatic Glycosylation of Oligo-N-Acetyllactosamine Derivatives","volume":"58","author":"IA Gagarinov","year":"2019","journal-title":"Angewandte Chemie International Edition"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1008816","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,9,9]],"date-time":"2020-09-09T00:00:00Z","timestamp":1599609600000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1008816","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,9,9]],"date-time":"2020-09-09T17:37:12Z","timestamp":1599673032000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1008816"}},"subtitle":[],"editor":[{"given":"Daniel R.","family":"Perez","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2020,8,27]]},"references-count":55,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2020,8,27]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1008816","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.ppat.1008816","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,27]]}}}