Three mutations switch H7N9 influenza to human-type receptor specificity

de Vries, Robert P.; Peng, Wenjie; Grant, Oliver C.; Thompson, Andrew J.; Zhu, Xueyong; Bouwman, Kim M.; de la Pena, Alba T. Torrents; van Breemen, Marielle J.; Ambepitiya Wickramasinghe, Iresha N.; de Haan, Cornelis A. M.; Yu, Wenli; McBride, Ryan; Sanders, Rogier W.; Woods, Robert J.; Verheije, Monique H.; Wilson, Ian A.; Paulson, James C.; Fernandez-Sesma, Ana

doi:10.1371/journal.ppat.1006390

Title: Three mutations switch H7N9 influenza to human-type receptor specificity

Journal Article · Thu Jun 15 00:00:00 EDT 2017 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1006390· OSTI ID:1400283

de Vries, Robert P. ^[1];

^[2]; Grant, Oliver C. ^[3]; Thompson, Andrew J. ^[2]; Zhu, Xueyong ^[2]; Bouwman, Kim M. ^[4]; de la Pena, Alba T. Torrents ^[5]; van Breemen, Marielle J. ^[5]; Ambepitiya Wickramasinghe, Iresha N. ^[4];

^[4]; Yu, Wenli ^[2];

^[2]; Sanders, Rogier W. ^[6]; Woods, Robert J. ^[3];

^[4]; Wilson, Ian A. ^[2];

^[2]; Fernandez-Sesma, Ana ^[7]

The Scripps Research Inst., La Jolla, CA (United States); Utrecht Univ. (The Netherlands)
The Scripps Research Inst., La Jolla, CA (United States)
Univ. of Georgia, Athens, GA (United States)
Utrecht Univ. (The Netherlands)
Univ. of Amsterdam (The Netherlands)
Univ. of Amsterdam (The Netherlands); Weil Medical College of Cornell Univ., New York, NY (United States)
Icahn School of Medicine at Mount Sinai, New York City, NY (United States)

The avian H7N9 influenza outbreak in 2013 resulted from an unprecedented incidence of influenza transmission to humans from infected poultry. The majority of human H7N9 isolates contained a hemagglutinin (HA) mutation (Q226L) that has previously been associated with a switch in receptor specificity from avian-type (NeuAcα2-3Gal) to human-type (NeuAcα2-6Gal), as documented for the avian progenitors of the 1957 (H2N2) and 1968 (H3N2) human influenza pandemic viruses. While this raised concern that the H7N9 virus was adapting to humans, the mutation was not sufficient to switch the receptor specificity of H7N9, and has not resulted in sustained transmission in humans. To determine if the H7 HA was capable of acquiring human-type receptor specificity, we conducted mutation analyses. Remarkably, three amino acid mutations conferred a switch in specificity for human-type receptors that resembled the specificity of the 2009 human H1 pandemic virus, and promoted binding to human trachea epithelial cells.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health; National Center for Research Resources; National Cancer Inst.

Grant/Contract Number:: AC02-06CH11357; P41GM103393; P41RR001209; R56 AI11765; GM100058; GM103390; U01-CA207824; AI099274; AI114730; GM62116; Y1-CO-1020; Y1-GM-1104

OSTI ID:: 1400283

Journal Information:: PLoS Pathogens, Vol. 13, Issue 6; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 67 works

Citation information provided by
Web of Science

References (60)

Immunization by Avian H5 Influenza Hemagglutinin Mutants with Altered Receptor Binding Specificity Yang, Z. -Y.; Wei, C. -J.; Kong, W. -P. Science, Vol. 317, Issue 5839 https://doi.org/10.1126/science.1135165	journal	August 2007
Importance of ligand conformational energies in carbohydrate docking: Sorting the wheat from the chaff Nivedha, Anita K.; Makeneni, Spandana; Foley, Bethany Lachele Journal of Computational Chemistry, Vol. 35, Issue 7 https://doi.org/10.1002/jcc.23517	journal	December 2013
Glycomic Analysis of Human Respiratory Tract Tissues and Correlation with Influenza Virus Infection Walther, Trevenan; Karamanska, Rositsa; Chan, Renee W. Y. PLoS Pathogens, Vol. 9, Issue 3 https://doi.org/10.1371/journal.ppat.1003223	journal	March 2013
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Limited airborne transmission of H7N9 influenza A virus between ferrets Richard, Mathilde; Schrauwen, Eefje J. A.; de Graaf, Miranda Nature, Vol. 501, Issue 7468 https://doi.org/10.1038/nature12476	journal	August 2013
Structural Analysis of the Hemagglutinin from the Recent 2013 H7N9 Influenza Virus Yang, H.; Carney, P. J.; Chang, J. C. Journal of Virology, Vol. 87, Issue 22 https://doi.org/10.1128/jvi.01854-13	journal	September 2013
Preferential Recognition of Avian-Like Receptors in Human Influenza A H7N9 Viruses Xu, R.; de Vries, R. P.; Zhu, X. Science, Vol. 342, Issue 6163 https://doi.org/10.1126/science.1243761	journal	December 2013
Limited airborne transmission of H7N9 influenza A virus between ferrets. Richard, Mathilde; Schrauwen, Eefje JA; De Graaf, Miranda Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.53832	text	January 2013
Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957 Liu, J.; Stevens, D. J.; Haire, L. F. Proceedings of the National Academy of Sciences, Vol. 106, Issue 40 https://doi.org/10.1073/pnas.0906849106	journal	September 2009
Gain-of-Function Experiments on H7N9 Fouchier, R. A. M.; Kawaoka, Y.; Cardona, C. Science, Vol. 341, Issue 6146 https://doi.org/10.1126/science.1243325	journal	August 2013
Combining 3D structure with glycan array data provides insight into the origin of glycan specificity Grant, Oliver C.; Tessier, Matthew B.; Meche, Lawrence Glycobiology, Vol. 26, Issue 7 https://doi.org/10.1093/glycob/cww020	journal	February 2016
Avian influenza A H7N9 in Zhejiang, China Koopmans, Marion; de Jong, Menno D. The Lancet, Vol. 381, Issue 9881 https://doi.org/10.1016/s0140-6736(13)60936-8	journal	June 2013
Receptor binding by an H7N9 influenza virus from humans Xiong, Xiaoli; Martin, Stephen R.; Haire, Lesley F. Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12372	journal	June 2013
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Structural Determinants for Naturally Evolving H5N1 Hemagglutinin to Switch Its Receptor Specificity Tharakaraman, Kannan; Raman, Rahul; Viswanathan, Karthik Cell, Vol. 153, Issue 7 https://doi.org/10.1016/j.cell.2013.05.035	journal	June 2013
Computational Screening of the Human TF-Glycome Provides a Structural Definition for the Specificity of Anti-Tumor Antibody JAA-F11 Tessier, Matthew B.; Grant, Oliver C.; Heimburg-Molinaro, Jamie PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054874	journal	January 2013
H7N9 influenza viruses interact preferentially with α2,3-linked sialic acids and bind weakly to α2,6-linked sialic acids Ramos, Irene; Krammer, Florian; Hai, Rong Journal of General Virology, Vol. 94, Issue 11 https://doi.org/10.1099/vir.0.056184-0	journal	November 2013
Receptor binding properties of human and animal H1 influenza virus isolates Rogers, Gary N.; D'Souza, Bruce L. Virology, Vol. 173, Issue 1 https://doi.org/10.1016/0042-6822(89)90249-3	journal	November 1989
Presentation, presentation, presentation! Molecular-level insight into linker effects on glycan array screening data Grant, O. C.; Smith, H. M.; Firsova, D. Glycobiology, Vol. 24, Issue 1 https://doi.org/10.1093/glycob/cwt083	journal	September 2013
Influenza hemagglutinin is spring-loaded by a metastable native conformation Carr, C. M.; Chaudhry, C.; Kim, P. S. Proceedings of the National Academy of Sciences, Vol. 94, Issue 26 https://doi.org/10.1073/pnas.94.26.14306	journal	December 1997
Role of receptor binding specificity in influenza A virus transmission and pathogenesis Graaf, Miranda; Fouchier, Ron A. M. The EMBO Journal, Vol. 33, Issue 14 https://doi.org/10.15252/embj.201489251	journal	July 2014
Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets Imai, Masaki; Watanabe, Tokiko; Hatta, Masato Nature, Vol. 486, Issue 7403 https://doi.org/10.1038/nature10831	journal	May 2012
Identification, Characterization, and Natural Selection of Mutations Driving Airborne Transmission of A/H5N1 Virus Linster, Martin; van Boheemen, Sander; de Graaf, Miranda Cell, Vol. 157, Issue 2 https://doi.org/10.1016/j.cell.2014.02.040	journal	April 2014
Airborne Transmission of Influenza A/H5N1 Virus Between Ferrets Herfst, S.; Schrauwen, E. J. A.; Linster, M. Science, Vol. 336, Issue 6088 https://doi.org/10.1126/science.1213362	journal	June 2012
Glycomic Characterization of Respiratory Tract Tissues of Ferrets: IMPLICATIONS FOR ITS USE IN INFLUENZA VIRUS INFECTION STUDIES Jia, Nan; Barclay, Wendy S.; Roberts, Kim Journal of Biological Chemistry, Vol. 289, Issue 41 https://doi.org/10.1074/jbc.m114.588541	journal	August 2014
Evolution of the Hemagglutinin Protein of the New Pandemic H1N1 Influenza Virus: Maintaining Optimal Receptor Binding by Compensatory Substitutions de Vries, R. P.; de Vries, E.; Martinez-Romero, C. Journal of Virology, Vol. 87, Issue 24 https://doi.org/10.1128/jvi.01955-13	journal	October 2013
Erratum to “In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity” [Virology 422 (2011) 105–113] Chen, Li-Mei; Blixt, Ola; Stevens, James Virology, Vol. 424, Issue 2 https://doi.org/10.1016/j.virol.2011.12.014	journal	March 2012
The soft palate is an important site of adaptation for transmissible influenza viruses Lakdawala, Seema S.; Jayaraman, Akila; Halpin, Rebecca A. Nature, Vol. 526, Issue 7571 https://doi.org/10.1038/nature15379	journal	September 2015
Structures and Receptor Binding of Hemagglutinins from Human-Infecting H7N9 Influenza Viruses Shi, Y.; Zhang, W.; Wang, F. Science, Vol. 342, Issue 6155 https://doi.org/10.1126/science.1242917	journal	September 2013
In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity Chen, Li-Mei; Blixt, Ola; Stevens, James Virology, Vol. 422, Issue 1 https://doi.org/10.1016/j.virol.2011.10.006	journal	January 2012
The 150-Loop Restricts the Host Specificity of Human H10N8 Influenza Virus Tzarum, Netanel; de Vries, Robert P.; Peng, Wenjie Cell Reports, Vol. 19, Issue 2 https://doi.org/10.1016/j.celrep.2017.03.054	journal	April 2017
Probable person to person transmission of novel avian influenza A (H7N9) virus in Eastern China, 2013: epidemiological investigation Qi, X.; Qian, Y. -H.; Bao, C. -J. BMJ, Vol. 347, Issue aug06 2 https://doi.org/10.1136/bmj.f4752	journal	August 2013
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Receptor Specificity in Human, Avian, and Equine H2 and H3 Influenza Virus Isolates Connor, Robert J.; Kawaoka, Yoshihiro; Webster, Robert G. Virology, Vol. 205, Issue 1 https://doi.org/10.1006/viro.1994.1615	journal	November 1994
H10N8 and H6N1 Maintain Avian Receptor Binding Richard, Mathilde; Fouchier, Ron A. M. Cell Host & Microbe, Vol. 17, Issue 3 https://doi.org/10.1016/j.chom.2015.02.020	journal	March 2015
A Human-Infecting H10N8 Influenza Virus Retains a Strong Preference for Avian-type Receptors Zhang, Heng; de Vries, Robert P.; Tzarum, Netanel Cell Host & Microbe, Vol. 17, Issue 3 https://doi.org/10.1016/j.chom.2015.02.006	journal	March 2015
Epidemiology of Human Infections with Avian Influenza A(H7N9) Virus in China Li, Qun; Zhou, Lei; Zhou, Minghao New England Journal of Medicine, Vol. 370, Issue 6 https://doi.org/10.1056/NEJMoa1304617	journal	February 2014
The influenza A virus hemagglutinin glycosylation state affects receptor-binding specificity de Vries, Robert P.; de Vries, Erik; Bosch, Berend Jan Virology, Vol. 403, Issue 1 https://doi.org/10.1016/j.virol.2010.03.047	journal	July 2010
A Two-Amino Acid Change in the Hemagglutinin of the 1918 Influenza Virus Abolishes Transmission Tumpey, T. M.; Maines, T. R.; Van Hoeven, N. Science, Vol. 315, Issue 5812 https://doi.org/10.1126/science.1136212	journal	February 2007
In Vitro Assessment of Attachment Pattern and Replication Efficiency of H5N1 Influenza A Viruses with Altered Receptor Specificity Chutinimitkul, Salin; van Riel, Debby; Munster, Vincent J. Journal of Virology, Vol. 84, Issue 13 https://doi.org/10.1128/jvi.02737-09	journal	April 2010
Role of Substitutions in the Hemagglutinin in the Emergence of the 1968 Pandemic Influenza Virus Van Poucke, Sjouke; Doedt, Jennifer; Baumann, Jan Journal of Virology, Vol. 89, Issue 23 https://doi.org/10.1128/jvi.01292-15	journal	September 2015
Adaptation of novel H7N9 influenza A virus to human receptors Dortmans, J. C. F. M.; Dekkers, J.; Wickramasinghe, I. N. Ambepitiya Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep03058	journal	October 2013
Recent H3N2 Viruses Have Evolved Specificity for Extended, Branched Human-type Receptors, Conferring Potential for Increased Avidity Peng, Wenjie; de Vries, Robert P.; Grant, Oliver C. Cell Host & Microbe, Vol. 21, Issue 1 https://doi.org/10.1016/j.chom.2016.11.004	journal	January 2017
Rotamer Libraries in the 21st Century Dunbrack, Roland L. Current Opinion in Structural Biology, Vol. 12, Issue 4 https://doi.org/10.1016/s0959-440x(02)00344-5	journal	August 2002
Amino Acid Substitutions That Affect Receptor Binding and Stability of the Hemagglutinin of Influenza A/H7N9 Virus Schrauwen, Eefje J. A.; Richard, Mathilde; Burke, David F. Journal of Virology, Vol. 90, Issue 7 https://doi.org/10.1128/jvi.03052-15	journal	January 2016
Role of receptor binding specificity in influenza A virus transmission and pathogenesis de Graaf, M.; Fouchier, R. A. M. The EMBO Journal, Vol. 33, Issue 8 https://doi.org/10.1002/embj.201387442	journal	March 2014
Likelihood-enhanced fast translation functions McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Storoni, Laurent C. Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 4 https://doi.org/10.1107/S0907444905001617	journal	March 2005
Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin Chandrasekaran, Aarthi; Srinivasan, Aravind; Raman, Rahul Nature Biotechnology, Vol. 26, Issue 1 https://doi.org/10.1038/nbt1375	journal	January 2008
Gain-of-Function Experiments on H7N9 Fouchier, R. A. M.; Kawaoka, Y.; Cardona, C. Science, Vol. 341, Issue 6146 https://doi.org/10.1126/science.341.6146.612	journal	August 2013
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
COVID‐19 and the gain of function debates Warmbrod, Kelsey Lane; Montague, Michael G.; Gronvall, Gigi Kwik EMBO reports, Vol. 22, Issue 10 https://doi.org/10.15252/embr.202153739	journal	September 2021
H5N1 receptor specificity as a factor in pandemic risk Paulson, James C.; de Vries, Robert P. Virus Research, Vol. 178, Issue 1 https://doi.org/10.1016/j.virusres.2013.02.015	journal	December 2013
Early Alterations of the Receptor-Binding Properties of H1, H2, and H3 Avian Influenza Virus Hemagglutinins after Their Introduction into Mammals Matrosovich, M.; Tuzikov, A.; Bovin, N. Journal of Virology, Vol. 74, Issue 18 https://doi.org/10.1128/jvi.74.18.8502-8512.2000	journal	September 2000
Epidemic of avian influenza A (H7N9) virus in China Poovorawan, Yong Pathogens and Global Health, Vol. 108, Issue 4 https://doi.org/10.1179/2047772414z.000000000206	journal	June 2014
Glycan Microarray Analysis of the Hemagglutinins from Modern and Pandemic Influenza Viruses Reveals Different Receptor Specificities Stevens, James; Blixt, Ola; Glaser, Laurel Journal of Molecular Biology, Vol. 355, Issue 5 https://doi.org/10.1016/j.jmb.2005.11.002	journal	February 2006
Receptor binding by a ferret-transmissible H5 avian influenza virus Xiong, Xiaoli; Coombs, Peter J.; Martin, Stephen R. Nature, Vol. 497, Issue 7449 https://doi.org/10.1038/nature12144	journal	April 2013
Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome Chen, Yu; Liang, Weifeng; Yang, Shigui The Lancet, Vol. 381, Issue 9881 https://doi.org/10.1016/S0140-6736(13)60903-4	journal	June 2013
Host-mediated selection of influenza virus receptor variants. Sialic acid-alpha 2,6Gal-specific clones of A/duck/Ukraine/1/63 revert to sialic acid-alpha 2,3Gal-specific wild type in ovo. Rogers, G. N.; Daniels, R. S.; Skehel, J. J. Journal of Biological Chemistry, Vol. 260, Issue 12 https://doi.org/10.1016/S0021-9258(17)39617-5	journal	June 1985

Cited By (16)

Flexibility In Vitro of Amino Acid 226 in the Receptor-Binding Site of an H9 Subtype Influenza A Virus and Its Effect In Vivo on Virus Replication, Tropism, and Transmission Obadan, Adebimpe O.; Santos, Jefferson; Ferreri, Lucas Journal of Virology, Vol. 93, Issue 6 https://doi.org/10.1128/jvi.02011-18	journal	December 2018
The Drivers of Pathology in Zoonotic Avian Influenza: The Interplay Between Host and Pathogen Horman, William S. J.; Nguyen, Thi H. O.; Kedzierska, Katherine Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.01812	journal	August 2018
Convergent Evolution of Human-Isolated H7N9 Avian Influenza A Viruses Xiang, Dan; Shen, Xuejuan; Pu, Zhiqing The Journal of Infectious Diseases, Vol. 217, Issue 11 https://doi.org/10.1093/infdis/jiy082	journal	February 2018
Clinician-initiated research on treating the host response to pandemic influenza Fedson, David S. Human Vaccines & Immunotherapeutics, Vol. 14, Issue 3 https://doi.org/10.1080/21645515.2017.1378292	journal	July 2017
Glycosciences.DB: an annotated data collection linking glycomics and proteomics data (2018 update) Böhm, Michael; Bohne-Lang, Andreas; Frank, Martin Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky994	journal	October 2018
Potent anti-influenza H7 human monoclonal antibody induces separation of hemagglutinin receptor-binding head domains Turner, Hannah L.; Pallesen, Jesper; Lang, Shanshan PLOS Biology, Vol. 17, Issue 2 https://doi.org/10.1371/journal.pbio.3000139	journal	February 2019
Evolution of Influenza A Virus by Mutation and Re-Assortment Shao, Wenhan; Li, Xinxin; Goraya, Mohsan International Journal of Molecular Sciences, Vol. 18, Issue 8 https://doi.org/10.3390/ijms18081650	journal	August 2017
Low-Fidelity Assembly of Influenza A Virus Promotes Escape from Host Cells Vahey, Michael D.; Fletcher, Daniel A. Cell, Vol. 176, Issue 1-2 https://doi.org/10.1016/j.cell.2018.10.056	journal	January 2019
H7N9 Influenza Virus Containing a Polybasic HA Cleavage Site Requires Minimal Host Adaptation to Obtain a Highly Pathogenic Disease Phenotype in Mice Chan, Mable; Leung, Anders; Hisanaga, Tamiko Viruses, Vol. 12, Issue 1 https://doi.org/10.3390/v12010065	journal	January 2020
Genesis and Spread of Newly Emerged Highly Pathogenic H7N9 Avian Viruses in Mainland China Yang, Lei; Zhu, Wenfei; Li, Xiyan Journal of Virology, Vol. 91, Issue 23 https://doi.org/10.1128/jvi.01277-17	journal	September 2017
A comprehensive comparison of the fifth-wave highly pathogenic and low-pathogenic H7N9 avian influenza viruses reveals potential threat posed by both types of viruses in mammals He, Lihong; Liu, Dong; Hu, Jiao Transboundary and Emerging Diseases, Vol. 65, Issue 6 https://doi.org/10.1111/tbed.12954	journal	July 2018
Global patterns of avian influenza A (H7): virus evolution and zoonotic threats Naguib, Mahmoud M.; Verhagen, Josanne H.; Mostafa, Ahmed FEMS Microbiology Reviews https://doi.org/10.1093/femsre/fuz019	journal	August 2019
Evolutionary consequences of delaying intervention for monkeypox Johnson, Philip L. F.; Bergstrom, Carl T.; Regoes, Roland R. The Lancet, Vol. 400, Issue 10359 https://doi.org/10.1016/s0140-6736(22)01789-5	journal	October 2022
Identification of two residues within the NS1 of H7N9 influenza A virus that critically affect the protein stability and function Wang, Song; Zhang, Lanlan; Zhang, Rong Veterinary Research, Vol. 49, Issue 1 https://doi.org/10.1186/s13567-018-0594-y	journal	October 2018
Inventory of molecular markers affecting biological characteristics of avian influenza A viruses Suttie, Annika; Deng, Yi-Mo; Greenhill, Andrew R. Virus Genes, Vol. 55, Issue 6 https://doi.org/10.1007/s11262-019-01700-z	journal	August 2019
Low-Fidelity Assembly of Influenza A Virus Promotes Escape from Host Cells Vahey, Michael D.; Fletcher, Daniel A. Cell, Vol. 176, Issue 3 https://doi.org/10.1016/j.cell.2019.01.009	journal	January 2019

Similar Records

A Human-Infecting H10N8 Influenza Virus Retains a Strong Preference for Avian-type Receptors

Journal Article · Sun Mar 01 00:00:00 EST 2015 · Cell Host & Microbe · OSTI ID:1400283

Zhang, Heng; de Vries, Robert P.; Tzarum, Netanel; +5 more

Structural and Molecular Characterization of the Hemagglutinin from the Fifth-Epidemic-Wave A(H7N9) Influenza Viruses

Journal Article · Wed May 30 00:00:00 EDT 2018 · Journal of Virology · OSTI ID:1400283

Yang, Hua; Carney, Paul J.; Chang, Jessie C.; +3 more

A single mutation in Taiwanese H6N1 influenza hemagglutinin switches binding to human-type receptors

Journal Article · Mon Jul 10 00:00:00 EDT 2017 · EMBO Molecular Medicine · OSTI ID:1400283

de Vries, Robert P.; Tzarum, Netanel; Peng, Wenjie; +12 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
receptor binding assays
H7N9
microbial mutation
trachea
chickens
H1N1
H5N1
Influenza A virus

Title: Three mutations switch H7N9 influenza to human-type receptor specificity

Citation Formats

References (60)

Cited By (16)

Similar Records

Related Subjects