A human-infecting H10N8 influenza virus retains a strong preference for avian-type receptors

Cell Host and Microbe

Volumn 17, Issue 3, 2015, Pages 377-384

  Zhang, Heng ^a,b   De Vries, Robert P ^a,c   Tzarum, Netanel ^a   Zhu, Xueyong ^a   Yu, Wenli ^a   McBride, Ryan ^a   Paulson, James C ^a   Wilson, Ian A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b INSTITUTE OF HIGH ENERGY PHYSICS   (China)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; VIRUS RECEPTOR; PROTEIN BINDING;

ARTICLE; AVIAN INFLUENZA VIRUS; BINDING SITE; CRYSTAL STRUCTURE; HUMAN; INFLUENZA A; INFLUENZA VIRUS A H10N8; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; CHEMICAL STRUCTURE; CHEMISTRY; INFLUENZA; INFLUENZA A VIRUS (H10N8); ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; VIROLOGY; VIRUS ATTACHMENT; X RAY CRYSTALLOGRAPHY;

AVES; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

CRYSTALLOGRAPHY, X-RAY; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H10N8 SUBTYPE; INFLUENZA, HUMAN; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, VIRUS; VIRUS ATTACHMENT;

EID: 84926225986     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.02.006     Document Type: Article

References (44)

1. G.G. Arzey, P.D. Kirkland, K.E. Arzey, M. Frost, P. Maywood, S. Conaty, A.C. Hurt, Y.M. Deng, P. Iannello, and I. Barr Influenza virus A (H10N7) in chickens and poultry abattoir workers, Australia Emerg. Infect. Dis. 18 2012 814 816
2. A. Chandrasekaran, A. Srinivasan, R. Raman, K. Viswanathan, S. Raguram, T.M. Tumpey, V. Sasisekharan, and R. Sasisekharan Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin Nat. Biotechnol. 26 2008 107 113
3. L.M. Chen, O. Blixt, J. Stevens, A.S. Lipatov, C.T. Davis, B.E. Collins, N.J. Cox, J.C. Paulson, and R.O. Donis In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity Virology 422 2012 105 113
4. H. Chen, H. Yuan, R. Gao, J. Zhang, D. Wang, Y. Xiong, G. Fan, F. Yang, X. Li, and J. Zhou Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study Lancet 383 2014 714 721
5. S. Chutinimitkul, D. van Riel, V.J. Munster, J.M. van den Brand, G.F. Rimmelzwaan, T. Kuiken, A.D. Osterhaus, R.A. Fouchier, and E. de Wit In vitro assessment of attachment pattern and replication efficiency of H5N1 influenza A viruses with altered receptor specificity J. Virol. 84 2010 6825 6833
6. J. Concepcion, K. Witte, C. Wartchow, S. Choo, D. Yao, H. Persson, J. Wei, P. Li, B. Heidecker, and W. Ma Label-free detection of biomolecular interactions using BioLayer interferometry for kinetic characterization Comb. Chem. High Throughput Screen. 12 2009 791 800
7. R.J. Connor, Y. Kawaoka, R.G. Webster, and J.C. Paulson Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates Virology 205 1994 17 23
8. R.P. de Vries, E. de Vries, K.S. Moore, A. Rigter, P.J. Rottier, and C.A. de Haan Only two residues are responsible for the dramatic difference in receptor binding between swine and new pandemic H1 hemagglutinin J. Biol. Chem. 286 2011 5868 5875
9. R.P. de Vries, X. Zhu, R. McBride, A. Rigter, A. Hanson, G. Zhong, M. Hatta, R. Xu, W. Yu, and Y. Kawaoka Hemagglutinin receptor specificity and structural analyses of respiratory droplet-transmissible H5N1 viruses J. Virol. 88 2014 768 773
10. L. Englund Studies on influenza viruses H10N4 and H10N7 of avian origin in mink Vet. Microbiol. 74 2000 101 107
11. S.J. Gamblin, L.F. Haire, R.J. Russell, D.J. Stevens, B. Xiao, Y. Ha, N. Vasisht, D.A. Steinhauer, R.S. Daniels, and A. Elliot The structure and receptor binding properties of the 1918 influenza hemagglutinin Science 303 2004 1838 1842
12. A. García-Sastre, and M. Schmolke Avian influenza A H10N8 - a virus on the verge? Lancet 383 2014 676 677
13. Y. Ha, D.J. Stevens, J.J. Skehel, and D.C. Wiley H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes EMBO J. 21 2002 865 875
14. S. Herfst, E.J. Schrauwen, M. Linster, S. Chutinimitkul, E. de Wit, V.J. Munster, E.M. Sorrell, T.M. Bestebroer, D.F. Burke, and D.J. Smith Airborne transmission of influenza A/H5N1 virus between ferrets Science 336 2012 1534 1541
15. M. Imai, T. Watanabe, M. Hatta, S.C. Das, M. Ozawa, K. Shinya, G. Zhong, A. Hanson, H. Katsura, and S. Watanabe Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets Nature 486 2012 420 428
16. T. Lin, G. Wang, A. Li, Q. Zhang, C. Wu, R. Zhang, Q. Cai, W. Song, and K.Y. Yuen The hemagglutinin structure of an avian H1N1 influenza A virus Virology 392 2009 73 81
17. Y.P. Lin, X. Xiong, S.A. Wharton, S.R. Martin, P.J. Coombs, S.G. Vachieri, E. Christodoulou, P.A. Walker, J. Liu, and J.J. Skehel Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin Proc. Natl. Acad. Sci. USA 109 2012 21474 21479
18. M. Linster, S. van Boheemen, M. de Graaf, E.J. Schrauwen, P. Lexmond, B. Mänz, T.M. Bestebroer, J. Baumann, D. van Riel, and G.F. Rimmelzwaan Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus Cell 157 2014 329 339
19. J. Liu, D.J. Stevens, L.F. Haire, P.A. Walker, P.J. Coombs, R.J. Russell, S.J. Gamblin, and J.J. Skehel Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957 Proc. Natl. Acad. Sci. USA 106 2009 17175 17180
20. M. Liu, X. Li, H. Yuan, J. Zhou, J. Wu, H. Bo, W. Xia, Y. Xiong, L. Yang, and R. Gao Genetic diversity of avian influenza A (H10N8) virus in live poultry markets and its association with human infections in China Sci Rep 5 2015 7632
21. M. Matrosovich, A. Tuzikov, N. Bovin, A. Gambaryan, A. Klimov, M.R. Castrucci, I. Donatelli, and Y. Kawaoka Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals J. Virol. 74 2000 8502 8512
22. E. Nobusawa, H. Ishihara, T. Morishita, K. Sato, and K. Nakajima Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides Virology 278 2000 587 596
23. Pan American Health Organization (2004). Avian influenza virus A (H10N7) circulating among humans in Egypt. EID Weekly Updates 2, 2. Available online at: http://www1.paho.org/english/ad/dpc/cd/eid-eer-07-may-2004.htm.
24. J.C. Paulson, and R.P. de Vries H5N1 receptor specificity as a factor in pandemic risk Virus Res. 178 2013 99 113
25. Report of Health and Family Planning Commission of Jiangxi Province (2014). The third human case of H10N8 bird flu was confirmed. (http://www.jxwst.gov.cn/gzdt/201402/t20140213-308109.htm).
26. G.N. Rogers, J.C. Paulson, R.S. Daniels, J.J. Skehel, I.A. Wilson, and D.C. Wiley Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity Nature 304 1983 76 78
27. S. Sabesan, K. Bock, and J.C. Paulson Conformational analysis of sialyloligosaccharides Carbohydr. Res. 218 1991 27 54
28. Y. Shi, W. Zhang, F. Wang, J. Qi, Y. Wu, H. Song, F. Gao, Y. Bi, Y. Zhang, and Z. Fan Structures and receptor binding of hemagglutinins from human-infecting H7N9 influenza viruses Science 342 2013 243 247
29. W. Shi, W. Li, X. Li, J. Haywood, J. Ma, G.F. Gao, and D. Liu Phylogenetics of varied subtypes of avian influenza viruses in China: potential threat to humans Protein Cell 5 2014 253 257
30. J. Stevens, O. Blixt, L. Glaser, J.K. Taubenberger, P. Palese, J.C. Paulson, and I.A. Wilson Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities J. Mol. Biol. 355 2006 1143 1155
31. J. Stevens, O. Blixt, J.C. Paulson, and I.A. Wilson Glycan microarray technologies: tools to survey host specificity of influenza viruses Nat. Rev. Microbiol. 4 2006 857 864
32. J. Stevens, O. Blixt, T.M. Tumpey, J.K. Taubenberger, J.C. Paulson, and I.A. Wilson Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus Science 312 2006 404 410
33. S. Su, W. Qi, P. Zhou, C. Xiao, Z. Yan, J. Cui, K. Jia, G. Zhang, G.C. Gray, M. Liao, and S. Li First evidence of H10N8 Avian influenza virus infections among feral dogs in live poultry markets in Guangdong province, China Clin. Infect. Dis. 59 2014 748 750
34. N. Tzarum, R.P. de Vries, X. Zhu, W. Yu, R. McBride, J.C. Paulson, and I.A. Wilson Structure and receptor binding of the hemagglutinin from a human H6N1 influenza virus Cell Host Microbe 17 2015 369 376 this issue
35. S.G. Vachieri, X. Xiong, P.J. Collins, P.A. Walker, S.R. Martin, L.F. Haire, Y. Zhang, J.W. McCauley, S.J. Gamblin, and J.J. Skehel Receptor binding by H10 influenza viruses Nature 511 2014 475 477
36. W. Wang, B. Lu, H. Zhou, A.L. Suguitan Jr., X. Cheng, K. Subbarao, G. Kemble, and H. Jin 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 J. Virol. 84 2010 6570 6577
37. M. Wang, W. Zhang, J. Qi, F. Wang, J. Zhou, Y. Bi, Y. Wu, H. Sun, J. Liu, and C. Huang Structural basis for preferential avian receptor binding by the human-infecting H10N8 avian influenza virus Nat. Commun. 6 2015 5600
38. X. Xiong, P.J. Coombs, S.R. Martin, J. Liu, H. Xiao, J.W. McCauley, K. Locher, P.A. Walker, P.J. Collins, and Y. Kawaoka Receptor binding by a ferret-transmissible H5 avian influenza virus Nature 497 2013 392 396
39. Xu, R., and Wilson, I.A. (2012). (Boca Raton, FL, CRC Press). In Structural Glycomics, E. Yuriev and P.A. Ramsland, eds. (Boca Raton, FL: CRC Press), pp. 235-257.
40. R. Xu, R. McBride, C.M. Nycholat, J.C. Paulson, and I.A. Wilson Structural characterization of the hemagglutinin receptor specificity from the 2009 H1N1 influenza pandemic J. Virol. 86 2012 982 990
41. R. Xu, R.P. de Vries, X. Zhu, C.M. Nycholat, R. McBride, W. Yu, J.C. Paulson, and I.A. Wilson Preferential recognition of avian-like receptors in human influenza A H7N9 viruses Science 342 2013 1230 1235
42. H. Zhang, B. Xu, Q. Chen, J. Chen, and Z. Chen Characterization of an H10N8 influenza virus isolated from Dongting lake wetland Virol. J. 8 2011 42
43. W. Zhang, Y. Shi, X. Lu, Y. Shu, J. Qi, and G.F. Gao An airborne transmissible avian influenza H5 hemagglutinin seen at the atomic level Science 340 2013 1463 1467
44. S. Zohari, A. Neimanis, T. Härkönen, C. Moraeus, and J.F. Valarcher Avian influenza A(H10N7) virus involvement in mass mortality of harbour seals (Phoca vitulina) in Sweden, March through October 2014 Euro Surveill. 19 2014 20967