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Article: Hemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets

TitleHemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets
Authors
KeywordsInfluenza A
Viral genes
Zoonosis
Issue Date2011
PublisherNational Academy of Sciences. The Journal's web site is located at http://www.pnas.org
Citation
Proceedings Of The National Academy Of Sciences Of The United States Of America, 2011, v. 108 n. 34, p. 14264-14269 How to Cite?
AbstractA novel reassortant derived from North American triple-reassortant (TRsw) and Eurasian swine (EAsw) influenza viruses acquired sustained human-to-human transmissibility and caused the 2009 influenza pandemic. To identify molecular determinants that allowed efficient transmission of the pandemic H1N1 virus among humans, we evaluated the direct-contact and respiratory-droplet transmissibility in ferrets of representative swine influenza viruses of different lineages obtained through a 13-y surveillance program in southern China. Whereas all viruses studied were transmitted by direct contact with varying efficiency, respiratory-droplet transmissibility (albeit inefficient) was observed only in the TRsw-like A/swine/Hong Kong/915/04 (sw915) (H1N2) virus. The sw915 virus had acquired the M gene derived from EAsw and differed from the gene constellation of the pandemic H1N1 virus by the neuraminidase (NA) gene alone. Glycan array analysis showed that pandemic H1N1 virus A/HK/415742/09 (HK415742) and sw915 possess similar receptor-binding specificity and affinity for α2,6-linked sialosides. Sw915 titers in differentiated normal human bronchial epithelial cells and in ferret nasal washes were lower than those of HK415742. Introducing the NA from pandemic HK415742 into sw915 did not increase viral replication efficiency but increased respiratory-droplet transmissibility, despite a substantial amino acid difference between the two viruses. The NA of the pandemic HK415742 virus possessed significantly higher enzyme activity than that of sw915 or other swine influenza viruses. Our results suggest that a unique gene constellation and hemagglutinin-neuraminidase balance play a critical role in acquisition of efficient and sustained human-to-human transmissibility.
Persistent Identifierhttp://hdl.handle.net/10722/142404
ISSN
2015 Impact Factor: 9.423
2015 SCImago Journal Rankings: 6.883
PubMed Central ID
ISI Accession Number ID
Funding AgencyGrant Number
Food and Health Bureau, Hong Kong
University Grants Committee, Hong KongAoE/M-12/06
University of Hong Kong
National Institute of Allergy and Infectious Diseases, National Institutes of HealthHHSN266200700005C
Funding Information:

We thank Dr. K. H. Chan for providing the pandemic H1N1 virus; Drs. G. J. D. Smith and D. Vijaykrishna for informative discussions; E. S. K. Ma, H. P. Chiu, and C. S. W. Leung, P. Seiler, K. Friedman, J. Franks, J. Turner, J. C. Crumpton, B. Marathe, A. Prevost, and D. Carey for technical assistance; and S. Naron for manuscript editing. This study was supported by the Research Fund for the Control of Infectious Diseases Commissioned Project from the Food and Health Bureau, Hong Kong; the Area of Excellence Scheme of the University Grants Committee (AoE/M-12/06), Hong Kong; Seed Funding for Basic Research, University of Hong Kong; and Contract HHSN266200700005C from the National Institute of Allergy and Infectious Diseases, National Institutes of Health.

References
Grants

 

DC FieldValueLanguage
dc.contributor.authorYen, HLen_HK
dc.contributor.authorLiang, CHen_HK
dc.contributor.authorWu, CYen_HK
dc.contributor.authorForrest, HLen_HK
dc.contributor.authorFerguson, Aen_HK
dc.contributor.authorChoy, KTen_HK
dc.contributor.authorJones, Jen_HK
dc.contributor.authorWong, DDYen_HK
dc.contributor.authorCheung, PPHen_HK
dc.contributor.authorHsu, CHen_HK
dc.contributor.authorLi, OTen_HK
dc.contributor.authorYuen, KMen_HK
dc.contributor.authorChan, RWYen_HK
dc.contributor.authorPoon, LLMen_HK
dc.contributor.authorChan, MCWen_HK
dc.contributor.authorNicholls, JMen_HK
dc.contributor.authorKrauss, Sen_HK
dc.contributor.authorWong, CHen_HK
dc.contributor.authorGuan, Yen_HK
dc.contributor.authorWebster, RGen_HK
dc.contributor.authorWebby, RJen_HK
dc.contributor.authorPeiris, Men_HK
dc.date.accessioned2011-10-28T02:45:21Z-
dc.date.available2011-10-28T02:45:21Z-
dc.date.issued2011en_HK
dc.identifier.citationProceedings Of The National Academy Of Sciences Of The United States Of America, 2011, v. 108 n. 34, p. 14264-14269en_HK
dc.identifier.issn0027-8424en_HK
dc.identifier.urihttp://hdl.handle.net/10722/142404-
dc.description.abstractA novel reassortant derived from North American triple-reassortant (TRsw) and Eurasian swine (EAsw) influenza viruses acquired sustained human-to-human transmissibility and caused the 2009 influenza pandemic. To identify molecular determinants that allowed efficient transmission of the pandemic H1N1 virus among humans, we evaluated the direct-contact and respiratory-droplet transmissibility in ferrets of representative swine influenza viruses of different lineages obtained through a 13-y surveillance program in southern China. Whereas all viruses studied were transmitted by direct contact with varying efficiency, respiratory-droplet transmissibility (albeit inefficient) was observed only in the TRsw-like A/swine/Hong Kong/915/04 (sw915) (H1N2) virus. The sw915 virus had acquired the M gene derived from EAsw and differed from the gene constellation of the pandemic H1N1 virus by the neuraminidase (NA) gene alone. Glycan array analysis showed that pandemic H1N1 virus A/HK/415742/09 (HK415742) and sw915 possess similar receptor-binding specificity and affinity for α2,6-linked sialosides. Sw915 titers in differentiated normal human bronchial epithelial cells and in ferret nasal washes were lower than those of HK415742. Introducing the NA from pandemic HK415742 into sw915 did not increase viral replication efficiency but increased respiratory-droplet transmissibility, despite a substantial amino acid difference between the two viruses. The NA of the pandemic HK415742 virus possessed significantly higher enzyme activity than that of sw915 or other swine influenza viruses. Our results suggest that a unique gene constellation and hemagglutinin-neuraminidase balance play a critical role in acquisition of efficient and sustained human-to-human transmissibility.en_HK
dc.languageengen_US
dc.publisherNational Academy of Sciences. The Journal's web site is located at http://www.pnas.orgen_HK
dc.relation.ispartofProceedings of the National Academy of Sciences of the United States of Americaen_HK
dc.subjectInfluenza Aen_HK
dc.subjectViral genesen_HK
dc.subjectZoonosisen_HK
dc.subject.meshFerrets - virologyen_HK
dc.subject.meshHemagglutinin Glycoproteins, Influenza Virus - metabolismen_HK
dc.subject.meshInfluenza A Virus, H1N1 Subtype - enzymology - genetics - physiologyen_HK
dc.subject.meshNeuraminidase - metabolismen_HK
dc.subject.meshOrthomyxoviridae Infections - epidemiology - transmission - virologyen_HK
dc.titleHemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferretsen_HK
dc.typeArticleen_HK
dc.identifier.emailYen, HL: hyen@hku.hken_HK
dc.identifier.emailChan, RWY: reneewy@hku.hken_HK
dc.identifier.emailPoon, LLM: llmpoon@hkucc.hku.hken_HK
dc.identifier.emailChan, MCW: mchan@hku.hken_HK
dc.identifier.emailNicholls, JM: jmnichol@hkucc.hku.hken_HK
dc.identifier.emailGuan, Y: yguan@hkucc.hku.hken_HK
dc.identifier.emailPeiris, M: malik@hkucc.hku.hken_HK
dc.identifier.authorityYen, HL=rp00304en_HK
dc.identifier.authorityChan, RWY=rp01596en_HK
dc.identifier.authorityPoon, LLM=rp00484en_HK
dc.identifier.authorityChan, MCW=rp00420en_HK
dc.identifier.authorityNicholls, JM=rp00364en_HK
dc.identifier.authorityGuan, Y=rp00397en_HK
dc.identifier.authorityPeiris, M=rp00410en_HK
dc.description.naturelink_to_OA_fulltext-
dc.identifier.doi10.1073/pnas.1111000108en_HK
dc.identifier.pmid21825167-
dc.identifier.pmcidPMC3161546-
dc.identifier.scopuseid_2-s2.0-80052186216en_HK
dc.identifier.hkuros196694en_US
dc.relation.referenceshttp://www.scopus.com/mlt/select.url?eid=2-s2.0-80052186216&selection=ref&src=s&origin=recordpageen_HK
dc.identifier.volume108en_HK
dc.identifier.issue34en_HK
dc.identifier.spage14264en_HK
dc.identifier.epage14269en_HK
dc.identifier.eissn1091-6490-
dc.identifier.isiWOS:000294163500078-
dc.publisher.placeUnited Statesen_HK
dc.relation.projectControl of Pandemic and Inter-pandemic Influenza-
dc.identifier.scopusauthoridYen, HL=7102476668en_HK
dc.identifier.scopusauthoridLiang, CH=35098914100en_HK
dc.identifier.scopusauthoridWu, CY=35265629600en_HK
dc.identifier.scopusauthoridForrest, HL=25637014700en_HK
dc.identifier.scopusauthoridFerguson, A=8152884900en_HK
dc.identifier.scopusauthoridChoy, KT=54388685500en_HK
dc.identifier.scopusauthoridJones, J=8619650600en_HK
dc.identifier.scopusauthoridWong, DDY=50662409700en_HK
dc.identifier.scopusauthoridCheung, PPH=35214597500en_HK
dc.identifier.scopusauthoridHsu, CH=36838906800en_HK
dc.identifier.scopusauthoridLi, OT=36860875900en_HK
dc.identifier.scopusauthoridYuen, KM=35301205900en_HK
dc.identifier.scopusauthoridChan, RWY=26661379100en_HK
dc.identifier.scopusauthoridPoon, LLM=7005441747en_HK
dc.identifier.scopusauthoridChan, MCW=26654715500en_HK
dc.identifier.scopusauthoridNicholls, JM=7201463077en_HK
dc.identifier.scopusauthoridKrauss, S=7102769210en_HK
dc.identifier.scopusauthoridWong, CH=35493196700en_HK
dc.identifier.scopusauthoridGuan, Y=7202924055en_HK
dc.identifier.scopusauthoridWebster, RG=36048363100en_HK
dc.identifier.scopusauthoridWebby, RJ=35448064800en_HK
dc.identifier.scopusauthoridPeiris, M=7005486823en_HK

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