Molecular Characterizations of Surface Proteins Hemagglutinin and Neuraminidase from Recent H5Nx Avian Influenza Viruses

Yang, Hua; Carney, Paul J.; Mishin, Vasiliy P.; Guo, Zhu; Chang, Jessie C.; Wentworth, David E.; Gubareva, Larisa V.; Stevens, James; Schultz-Cherry, S.

doi:10.1128/JVI.00180-16

Molecular Characterizations of Surface Proteins Hemagglutinin and Neuraminidase from Recent H5Nx Avian Influenza Viruses

Journal Article · Fri May 27 00:00:00 EDT 2016 · Journal of Virology

DOI:https://doi.org/10.1128/JVI.00180-16· OSTI ID:1257478

Yang, Hua ^[1]; Carney, Paul J. ^[1]; Mishin, Vasiliy P. ^[1]; Guo, Zhu ^[1]; Chang, Jessie C. ^[1]; Wentworth, David E. ^[1]; Gubareva, Larisa V. ^[1]; Stevens, James ^[1]; Schultz-Cherry, S. ^[2]

Centers for Disease Control and Prevention, Atlanta, GA (United States)
St. Jude Children's Research Hospital, Knoxville, TN (United States)

During 2014, a subclade 2.3.4.4 highly pathogenic avian influenza (HPAI) A(H5N8) virus caused poultry outbreaks around the world. In late 2014/early 2015, the virus was detected in wild birds in Canada and the United States, and these viruses also gave rise to reassortant progeny, composed of viral RNA segments (vRNAs) from both Eurasian and North American lineages. In particular, viruses were found with N1, N2, and N8 neuraminidase vRNAs, and these are collectively referred to as H5Nx viruses. In the United States, more than 48 million domestic birds have been affected. Here we present a detailed structural and biochemical analysis of the surface antigens of H5N1, H5N2, and H5N8 viruses in addition to those of a recent human H5N6 virus. Our results with recombinant hemagglutinin reveal that these viruses have a strict avian receptor binding preference, while recombinantly expressed neuraminidases are sensitive to FDA-approved and investigational antivirals. Although H5Nx viruses currently pose a low risk to humans, it is important to maintain surveillance of these circulating viruses and to continually assess future changes that may increase their pandemic potential. The H5Nx viruses emerging in North America, Europe, and Asia pose a great public health concern. Here we report a molecular and structural study of the major surface proteins of several H5Nx influenza viruses. Furthermore, our results improve the understanding of these new viruses and provide important information on their receptor preferences and susceptibilities to antivirals, which are central to pandemic risk assessment.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Inst. of General Medical Sciences; HHS; Center for Disease Control and Prevention (CDC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1257478

Journal Information:: Journal of Virology, Journal Name: Journal of Virology Journal Issue: 12 Vol. 90; ISSN 0022-538X

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (76)

The 2.2 A resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. Burmeister, W. P.; Ruigrok, R. W.; Cusack, S. The EMBO Journal, Vol. 11, Issue 1 https://doi.org/10.1002/j.1460-2075.1992.tb05026.x	journal	January 1992
Three-dimensional structure of neuraminidase of subtype N9 from an avian influenza virus Baker, A. T.; Varghese, J. N.; Laver, W. G. Proteins: Structure, Function, and Genetics, Vol. 2, Issue 2 https://doi.org/10.1002/prot.340020205	journal	January 1987
The neuraminidase of influenza virus Air, Gillian M.; Laver, W. Graeme Proteins: Structure, Function, and Genetics, Vol. 6, Issue 4 https://doi.org/10.1002/prot.340060402	journal	January 1989
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
Avian Influenza A Viruses Differ from Human Viruses by Recognition of Sialyloligosaccharides and Gangliosides and by a Higher Conservation of the HA Receptor-Binding Site Matrosovich, M. N.; Gambaryan, A. S.; Teneberg, S. Virology, Vol. 233, Issue 1 https://doi.org/10.1006/viro.1997.8580	journal	June 1997
Optimization Techniques for Automation and High Throughput Chayen, Naomi E. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-209-0_9	book	January 2007
Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-d-N-acetylneuraminate) substrate Potier, M.; Mameli, L.; Bélisle, M. Analytical Biochemistry, Vol. 94, Issue 2 https://doi.org/10.1016/0003-2697(79)90362-2	journal	April 1979
Host cell proteases controlling virus pathogenicity Klenk, Hans-Dieter; Garten, Wolfgang Trends in Microbiology, Vol. 2, Issue 2 https://doi.org/10.1016/0966-842X(94)90123-6	journal	February 1994
X-ray structure of the hemagglutinin of a potential H3 avian progenitor of the 1968 Hong Kong pandemic influenza virus☆ Ha, Ya; Stevens, David J.; Skehel, John J. Virology, Vol. 309, Issue 2 https://doi.org/10.1016/S0042-6822(03)00068-0	journal	May 2003
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Structure of the Hemagglutinin Precursor Cleavage Site, a Determinant of Influenza Pathogenicity and the Origin of the Labile Conformation Chen, Jue; Lee, Kon Ho; Steinhauer, David A. Cell, Vol. 95, Issue 3 https://doi.org/10.1016/S0092-8674(00)81771-7	journal	October 1998
Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus Yuen, Ky; Chan, Pks; Peiris, M. The Lancet, Vol. 351, Issue 9101 https://doi.org/10.1016/S0140-6736(98)01182-9	journal	February 1998
Human infection with a novel, highly pathogenic avian influenza A (H5N6) virus: Virological and clinical findings Pan, Ming; Gao, Rongbao; Lv, Qiang Journal of Infection, Vol. 72, Issue 1 https://doi.org/10.1016/j.jinf.2015.06.009	journal	January 2016
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
The antigenic architecture of the hemagglutinin of influenza H5N1 viruses Velkov, Tony; Ong, Chi; Baker, Mark A. Molecular Immunology, Vol. 56, Issue 4 https://doi.org/10.1016/j.molimm.2013.07.010	journal	December 2013
H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes Russell, R. J.; Gamblin, S. J.; Haire, L. F. Virology, Vol. 325, Issue 2 https://doi.org/10.1016/j.virol.2004.04.040	journal	August 2004
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
Structure of Influenza Virus Neuraminidase B/Lee/40 Complexed with Sialic Acid and a Dehydro Analog at 1.8-.ANG. Resolution: Implications for the Catalytic Mechanism Janakiraman, Musiri N.; White, Clinton L.; Laver, W. Graeme Biochemistry, Vol. 33, Issue 27 https://doi.org/10.1021/bi00193a002	journal	July 1994
Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution Wilson, I. A.; Skehel, J. J.; Wiley, D. C. Nature, Vol. 289, Issue 5796 https://doi.org/10.1038/289366a0	journal	January 1981
Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation Wiley, D. C.; Wilson, I. A.; Skehel, J. J. Nature, Vol. 289, Issue 5796 https://doi.org/10.1038/289373a0	journal	January 1981
Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution Varghese, J. N.; Laver, W. G.; Colman, P. M. Nature, Vol. 303, Issue 5912 https://doi.org/10.1038/303035a0	journal	May 1983
Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity Rogers, G. N.; Paulson, J. C.; Daniels, R. S. Nature, Vol. 304, Issue 5921 https://doi.org/10.1038/304076a0	journal	July 1983
The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design Russell, Rupert J.; Haire, Lesley F.; Stevens, David J. Nature, Vol. 443, Issue 7107 https://doi.org/10.1038/nature05114	journal	August 2006
Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors Yamada, Shinya; Suzuki, Yasuo; Suzuki, Takashi Nature, Vol. 444, Issue 7117 https://doi.org/10.1038/nature05264	journal	November 2006
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
Neuraminidase Inhibitors for Influenza Moscona, Anne New England Journal of Medicine, Vol. 353, Issue 13 https://doi.org/10.1056/NEJMra050740	journal	September 2005
The VASP tetramerization domain is a right-handed coiled coil based on a 15-residue repeat Kuhnel, K.; Jarchau, T.; Wolf, E. Proceedings of the National Academy of Sciences, Vol. 101, Issue 49 https://doi.org/10.1073/pnas.0403069101	journal	November 2004
Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia Hulse-Post, D. J.; Sturm-Ramirez, K. M.; Humberd, J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 30 https://doi.org/10.1073/pnas.0504662102	journal	July 2005
Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion Russell, R. J.; Kerry, P. S.; Stevens, D. J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 46 https://doi.org/10.1073/pnas.0807142105	journal	November 2008
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
Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site Zhu, Xueyong; Yang, Hua; Guo, Zhu Proceedings of the National Academy of Sciences, Vol. 109, Issue 46 https://doi.org/10.1073/pnas.1212579109	journal	September 2012
X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs Ha, Y.; Stevens, D. J.; Skehel, J. J. Proceedings of the National Academy of Sciences, Vol. 98, Issue 20 https://doi.org/10.1073/pnas.201401198	journal	September 2001
The Amino Acid at the X Position of an Asn-X-Ser Sequon Is an Important Determinant of N-Linked Core-glycosylation Efficiency Shakin-Eshleman, Susan H.; Spitalnik, Steven L.; Kasturi, Lakshmi Journal of Biological Chemistry, Vol. 271, Issue 11 https://doi.org/10.1074/jbc.271.11.6363	journal	March 1996
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Davis, I. W.; Leaver-Fay, A.; Chen, V. B. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm216	journal	May 2007
The predicted antigenicity of the haemagglutinin of the 1918 Spanish influenza pandemic suggests an avian origin Brownlee, G. G.; Fodor, E. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 356, Issue 1416 https://doi.org/10.1098/rstb.2001.1001	journal	December 2001
Calcium is needed for the thermostability of influenza B virus neuraminidase Burmeister, W. P.; Cusack, S.; Ruigrok, R. W. H. Journal of General Virology, Vol. 75, Issue 2 https://doi.org/10.1099/0022-1317-75-2-381	journal	February 1994
Use of TLS parameters to model anisotropic displacements in macromolecular refinement Winn, M. D.; Isupov, M. N.; Murshudov, G. N. Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 1 https://doi.org/10.1107/S0907444900014736	journal	January 2001
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
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
Structure of a calcium-deficient form of influenza virus neuraminidase: implications for substrate binding Smith, Brian J.; Huyton, Trevor; Joosten, Robbie P. Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9 https://doi.org/10.1107/S0907444906020063	journal	August 2006
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
The CCP4 suite programs for protein crystallography No authors listed Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014 Smith, Gavin J. D.; Donis, Ruben O. Influenza and Other Respiratory Viruses, Vol. 9, Issue 5 https://doi.org/10.1111/irv.12324	journal	August 2015
Evidence for a sialosyl cation transition-state complex in the reaction of sialidase from influenza virus Chong, Andrew K. J.; Pegg, Michael S.; Taylor, Neil R. European Journal of Biochemistry, Vol. 207, Issue 1 https://doi.org/10.1111/j.1432-1033.1992.tb17055.x	journal	July 1992
Influenza neuraminidase: Influenza neuraminidase Air, Gillian M. Influenza and Other Respiratory Viruses, Vol. 6, Issue 4 https://doi.org/10.1111/j.1750-2659.2011.00304.x	journal	November 2011
The Structure and Receptor Binding Properties of the 1918 Influenza Hemagglutinin Gamblin, S. J. Science, Vol. 303, Issue 5665 https://doi.org/10.1126/science.1093155	journal	March 2004
Structure of the Uncleaved Human H1 Hemagglutinin from the Extinct 1918 Influenza Virus Stevens, J. Science, Vol. 303, Issue 5665 https://doi.org/10.1126/science.1093373	journal	March 2004
Structure and Receptor Specificity of the Hemagglutinin from an H5N1 Influenza Virus Stevens, J.; Blixt, O.; Tumpey, T. M. Science, Vol. 312, Issue 5772 https://doi.org/10.1126/science.1124513	journal	March 2006
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
The Potential for Respiratory Droplet-Transmissible A/H5N1 Influenza Virus to Evolve in a Mammalian Host Russell, C. A.; Fonville, J. M.; Brown, A. E. X. Science, Vol. 336, Issue 6088 https://doi.org/10.1126/science.1222526	journal	June 2012
Glycosylation at 158N of the Hemagglutinin Protein and Receptor Binding Specificity Synergistically Affect the Antigenicity and Immunogenicity of a Live Attenuated H5N1 A/Vietnam/1203/2004 Vaccine Virus in Ferrets Wang, W.; Lu, B.; Zhou, H. Journal of Virology, Vol. 84, Issue 13 https://doi.org/10.1128/JVI.00221-10	journal	April 2010
Structure and Receptor Binding Specificity of Hemagglutinin H13 from Avian Influenza A Virus H13N6 Lu, X.; Qi, J.; Shi, Y. Journal of Virology, Vol. 87, Issue 16 https://doi.org/10.1128/JVI.00235-13	journal	June 2013
Structure and Receptor Complexes of the Hemagglutinin from a Highly Pathogenic H7N7 Influenza Virus Yang, Hua; Carney, Paul J.; Donis, Ruben O. Journal of Virology, Vol. 86, Issue 16 https://doi.org/10.1128/JVI.00281-12	journal	June 2012
Influenza A Virus N5 Neuraminidase Has an Extended 150-Cavity Wang, M.; Qi, J.; Liu, Y. Journal of Virology, Vol. 85, Issue 16 https://doi.org/10.1128/JVI.00638-11	journal	June 2011
Structure of Influenza Virus N7: the Last Piece of the Neuraminidase "Jigsaw" Puzzle Sun, X.; Li, Q.; Wu, Y. Journal of Virology, Vol. 88, Issue 16 https://doi.org/10.1128/JVI.00805-14	journal	June 2014
Structural Characterization of the 1918 Influenza Virus H1N1 Neuraminidase Xu, X.; Zhu, X.; Dwek, R. A. Journal of Virology, Vol. 82, Issue 21 https://doi.org/10.1128/JVI.00959-08	journal	August 2008
Functional and Structural Analysis of Influenza Virus Neuraminidase N3 Offers Further Insight into the Mechanisms of Oseltamivir Resistance Li, Q.; Qi, J.; Wu, Y. Journal of Virology, Vol. 87, Issue 18 https://doi.org/10.1128/JVI.01129-13	journal	July 2013
Insights into Avian Influenza Virus Pathogenicity: the Hemagglutinin Precursor HA0 of Subtype H16 Has an Alpha-Helix Structure in Its Cleavage Site with Inefficient HA1/HA2 Cleavage Lu, X.; Shi, Y.; Gao, F. Journal of Virology, Vol. 86, Issue 23 https://doi.org/10.1128/JVI.01606-12	journal	September 2012
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
Structural and Functional Analysis of Surface Proteins from an A(H3N8) Influenza Virus Isolated from New England Harbor Seals Yang, Hua; Nguyen, Ha T.; Carney, Paul J. Journal of Virology, Vol. 89, Issue 5 https://doi.org/10.1128/JVI.02723-14	journal	December 2014
Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. Liu, C.; Eichelberger, M. C.; Compans, R. W. Journal of virology, Vol. 69, Issue 2 https://doi.org/10.1128/JVI.69.2.1099-1106.1995	journal	January 1995
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
Evolution and ecology of influenza A viruses. Webster, R. G.; Bean, W. J.; Gorman, O. T. Microbiological Reviews, Vol. 56, Issue 1 https://doi.org/10.1128/MMBR.56.1.152-179.1992	journal	January 1992
Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. Liu, C.; Eichelberger, M. C.; Compans, R. W. Journal of virology, Vol. 69, Issue 2 https://doi.org/10.1128/jvi.69.2.1099-1106.1995	journal	January 1995
Evolution and ecology of influenza A viruses Webster, R. G.; Bean, W. J.; Gorman, O. T. Microbiological Reviews, Vol. 56, Issue 1 https://doi.org/10.1128/mr.56.1.152-179.1992	journal	March 1992
Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin Yang, Hua; Carney, Paul; Stevens, James PLoS Currents, Vol. 2 https://doi.org/10.1371/currents.RRN1152	journal	March 2010
Structural and Antigenic Variation among Diverse Clade 2 H5N1 Viruses Shore, David A.; Yang, Hua; Balish, Amanda L. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0075209	journal	September 2013
Evolutionary Dynamics and Emergence of Panzootic H5N1 Influenza Viruses Vijaykrishna, Dhanasekaran; Bahl, Justin; Riley, Steven PLoS Pathogens, Vol. 4, Issue 9 https://doi.org/10.1371/journal.ppat.1000161	journal	September 2008
Structures of Receptor Complexes of a North American H7N2 Influenza Hemagglutinin with a Loop Deletion in the Receptor Binding Site Yang, Hua; Chen, Li-Mei; Carney, Paul J. PLoS Pathogens, Vol. 6, Issue 9 https://doi.org/10.1371/journal.ppat.1001081	journal	September 2010
Structural and Functional Analysis of Laninamivir and its Octanoate Prodrug Reveals Group Specific Mechanisms for Influenza NA Inhibition Vavricka, Christopher J.; Li, Qing; Wu, Yan PLoS Pathogens, Vol. 7, Issue 10 https://doi.org/10.1371/journal.ppat.1002249	journal	October 2011
New World Bats Harbor Diverse Influenza A Viruses Tong, Suxiang; Zhu, Xueyong; Li, Yan PLoS Pathogens, Vol. 9, Issue 10 https://doi.org/10.1371/journal.ppat.1003657	journal	October 2013
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids B., Chen, Vincent; C., Richardson, David; S., Richardson, Jane The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/m2an-p252	text	January 2007
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
Influenza Neuraminidase Goodsell, D. S. RCSB Protein Data Bank https://doi.org/10.2210/rcsb_pdb/mom_2009_5	journal	May 2009
Host Range Restriction and Pathogenicity in the Context of Influenza Pandemic Neumann, Gabriele; Kawaoka, Yoshihiro Emerging Infectious Diseases, Vol. 12, Issue 6 https://doi.org/10.3201/eid1206.051336	journal	June 2006
Novel Eurasian Highly Pathogenic Avian Influenza A H5 Viruses in Wild Birds, Washington, USA, 2014 Ip, Hon S.; Torchetti, Mia Kim; Crespo, Rocio Emerging Infectious Diseases, Vol. 21, Issue 5 https://doi.org/10.3201/eid2105.142020	journal	May 2015

Cited By (13)

Metabolic machinery encrypted in the Raman spectrum of influenza A virus‐inoculated mammalian cells Pezzotti, Giuseppe; Zhu, Wenliang; Adachi, Tetsuya Journal of Cellular Physiology, Vol. 235, Issue 6 https://doi.org/10.1002/jcp.29392	journal	November 2019
Full sequence analysis of hemagglutinin and neuraminidase genes and proteins of highly pathogenic avian influenza H5N1 virus detected in Iran, 2015 Yegani, Sima; Shoushtari, Abdel-Hamid; Eshratabadi, Fatemeh Tropical Animal Health and Production, Vol. 51, Issue 3 https://doi.org/10.1007/s11250-018-1731-3	journal	October 2018
Comparison of the pathogenic potential of highly pathogenic avian influenza (HPAI) H5N6, and H5N8 viruses isolated in South Korea during the 2016–2017 winter season Kwon, Hyeok-il; Kim, Eun-Ha; Kim, Young-il Emerging Microbes & Infections, Vol. 7, Issue 1 https://doi.org/10.1038/s41426-018-0029-x	journal	December 2018
Heterologous prime-boost with A(H5N1) pandemic influenza vaccines induces broader cross-clade antibody responses than homologous prime-boost Levine, Min Z.; Holiday, Crystal; Jefferson, Stacie npj Vaccines, Vol. 4, Issue 1 https://doi.org/10.1038/s41541-019-0114-8	journal	May 2019
Selective detections of single-viruses using solid-state nanopores Arima, Akihide; Tsutsui, Makusu; Harlisa, Ilva Hanun Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34665-4	journal	November 2018
Identification of antigenic epitopes in the haemagglutinin protein of H7 avian influenza virus Yao, Lu; Chen, Yuqing; Wang, Xingbo Avian Pathology, Vol. 49, Issue 1 https://doi.org/10.1080/03079457.2019.1666971	journal	October 2019
Altered virulence of Highly Pathogenic Avian Influenza (HPAI) H5N8 reassortant viruses in mammalian models Park, Su-Jin; Kim, Eun-Ha; Kwon, Hyeok-Il Virulence, Vol. 9, Issue 1 https://doi.org/10.1080/21505594.2017.1366408	journal	September 2017
Structure of an Influenza A virus N9 neuraminidase with a tetrabrachion-domain stalk Streltsov, Victor A.; Schmidt, Peter M.; McKimm-Breschkin, Jennifer L. Acta Crystallographica Section F Structural Biology Communications, Vol. 75, Issue 2 https://doi.org/10.1107/s2053230x18017892	journal	January 2019
Respiratory disease due to mixed viral infections in poultry flocks in Egypt between 2017 and 2018: Upsurge of highly pathogenic avian influenza virus subtype H5N8 since 2018 Hassan, Kareem E.; El‐Kady, Magdy F.; EL‐Sawah, Azza A. A. Transboundary and Emerging Diseases https://doi.org/10.1111/tbed.13281	journal	July 2019
A Naturally Occurring Deletion in the Effector Domain of H5N1 Swine Influenza Virus Nonstructural Protein 1 Regulates Viral Fitness and Host Innate Immunity Wang, Junyong; Zeng, Yan; Xu, Shuai Journal of Virology, Vol. 92, Issue 11 https://doi.org/10.1128/jvi.00149-18	journal	March 2018
Human Clade 2.3.4.4 A/H5N6 Influenza Virus Lacks Mammalian Adaptation Markers and Does Not Transmit via the Airborne Route between Ferrets Herfst, Sander; Mok, Chris K. P.; van den Brand, Judith M. A. mSphere, Vol. 3, Issue 1 https://doi.org/10.1128/msphere.00405-17	journal	January 2018
A study of the relationship between human infection with avian influenza a (H5N6) and environmental avian influenza viruses in Fujian, China Chen, Ping; Xie, Jian-Feng; Lin, Qi BMC Infectious Diseases, Vol. 19, Issue 1 https://doi.org/10.1186/s12879-019-4145-6	journal	September 2019
The Emergence and Decennary Distribution of Clade 2.3.4.4 HPAI H5Nx Antigua, Khristine Joy C.; Choi, Won-Suk; Baek, Yun Hee Microorganisms, Vol. 7, Issue 6 https://doi.org/10.3390/microorganisms7060156	journal	May 2019

Similar Records

Absence of clinical disease and contact transmission of HPAI H5NX clade 2.3.4.4 from North America in experimentally infected pigs

Journal Article · Sat Sep 02 00:00:00 EDT 2017 · Influenza and Other Respiratory Viruses · OSTI ID:1378274

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Molecular Characterizations of Surface Proteins Hemagglutinin and Neuraminidase from Recent H5Nx Avian Influenza Viruses

Citation Formats

References (76)

Cited By (13)

Similar Records

Related Subjects