Structure and receptor binding specificity of hemagglutinin H13 from avian influenza a virus H13N6

Journal of Virology

Volumn 87, Issue 16, 2013, Pages 9077-9085

  Lu, Xishan ^a,b   Qi, Jianxun ^a   Shi, Yi ^a,f   Wang, Ming ^a   Smith, David F ^c   Heimburg Molinaro, Jamie ^c   Zhang, Yanfang ^e   Paulson, James C ^d   Xiao, Haixia ^e   Gao, George F ^a,b,e,f,g  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e Chinese Academy of Sciences   (China)

^f INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^g CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 3 LINKED SIALIC ACID RECEPTOR; INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS RECEPTOR;

ARTICLE; AVIAN INFLUENZA VIRUS; BINDING AFFINITY; BINDING SITE; COMPARATIVE STUDY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; INFLUENZA VIRUS A H13N6; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; RECEPTOR BINDING; RESIDUE ANALYSIS; VIRUS IDENTIFICATION;

ANIMALS; BIRDS; CRYSTALLOGRAPHY, X-RAY; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, VIRUS; SIALIC ACIDS; VIRAL TROPISM;

EID: 84881225028     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00235-13     Document Type: Article

References (52)

1. Frank AL, Taber LH, Glezen WP, Geyer EA, McIlwain S, Paredes A. 1983. Influenza B virus infections in the community and the family. The epidemics of 1976-1977 and 1979-1980 in Houston, Texas. Am. J. Epidemiol. 118:313-325.
2. Gao GF, Sun Y. 2010. It is not just AIV: from avian to swine-origin influenza virus. Sci. China Life Sci. 53:151-153.
3. Guan Y, Vijaykrishna D, Bahl J, Zhu H, Wang J, Smith GJ. 2010. The emergence of pandemic influenza viruses. Protein Cell 1:9-13.
4. Neumann G, Noda T, Kawaoka Y. 2009. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931-939.
5. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56:152-179.
6. WHO. 1980. A revision of the system of nomenclature for influenza viruses: a WHO memorandum. Bull. World Health Organ. 58:585-591.
7. Air GM. 1981. Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc. Natl. Acad. Sci. U. S. A. 78:7639- 7643.
8. Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K. 1991. Comparison of complete amino acid sequences and receptorbinding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 182:475-485.
9. Gamblin SJ, Skehel JJ. 2010. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J. Biol. Chem. 285:28403-28409.
10. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO. 2012. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. U. S. A. 109:4269-4274.
11. Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ. 2006. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443:45-49.
12. Rogers GN, Pritchett TJ, Lane JL, Paulson JC. 1983. Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants. Virology 131: 394-408.
13. Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG. 1978. Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 84:268-278.
14. Naeve CW, Hinshaw VS, Webster RG. 1984. Mutations in the hemagglutinin receptor-binding site can change the biological properties of an influenza virus. J. Virol. 51:567-569.
15. Baum LG, Paulson JC. 1990. Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem. Suppl. 40:35-38.
16. Couceiro JN, Paulson JC, Baum LG. 1993. Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res. 29:155-165.
17. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. 2004. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc. Natl. Acad. Sci. U. S. A. 101: 4620-4624.
18. Medina RA, Garcia-Sastre A. 2011. Influenza A viruses: new research developments. Nat. Rev. Microbiol. 9:590-603.
19. Lu X, Shi Y, Gao F, Xiao H, Wang M, Qi J, Gao GF. 2012. 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. J. Virol. 86:12861-12870.
20. Wilson IA, Skehel JJ, Wiley DC. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289: 366-373.
21. Ha Y, Stevens DJ, Skehel JJ, Wiley DC. 2002. H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes. EMBO J. 21:865-875.
22. Russell RJ, Gamblin SJ, Haire LF, Stevens DJ, Xiao B, Ha Y, Skehel JJ. 2004. H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. Virology 325:287-296.
23. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866-1870.
24. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. 2006. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312:404-410.
25. Russell RJ, Kerry PS, Stevens DJ, Steinhauer DA, Martin SR, Gamblin SJ, Skehel JJ. 2008. Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 105: 17736-17741.
26. Liu J, Stevens DJ, Haire LF, Walker PA, Coombs PJ, Russell RJ, Gamblin SJ, Skehel JJ. 2009. Structures of receptor complexes formed by hemagglutinins from the Asian influenza pandemic of 1957. Proc. Natl. Acad. Sci. U. S. A. 106:17175-17180.
27. Sun X, Shi Y, Lu X, He J, Gao F, Yan J, Qi J, Gao GF. 2013. Bat-derived influenza hemagglutinin h17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep. 3:769-778.
28. Zhu X, Yu W, McBride R, Li Y, Chen LM, Donis RO, Tong S, Paulson JC, Wilson IA. 2013. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc. Natl. Acad. Sci. U. S. A. 110:1458-1463.
29. Brown IH. 2010. Summary of avian influenza activity in Europe, Asia, and Africa, 2006-2009. Avian Dis. 54:187-193.
30. de Jong JC, Rimmelzwaan GF, Bartelds AI, Wilbrink B, Fouchier RA, Osterhaus AD. 2003. The 2002/2003 influenza season in the Netherlands and the vaccine composition for the 2003/2004 season. Ned. Tijdschr. Geneeskd. 147:1971-1975.
31. Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW, Orr WK, Shortridge KF. 1999. Human infection with influenza H9N2. Lancet 354: 916-917.
32. Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, Perdue M, Swayne D, Bender C, Huang J, Hemphill M, Rowe T, Shaw M, Xu X, Fukuda K, Cox N. 1998. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279:393- 396.
33. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534-1541.
34. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, Li C, Kawakami E, Yamada S, Kiso M, Suzuki Y, Maher EA, Neumann G, Kawaoka Y. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420-428.
35. Velarde R, Calvin SE, Ojkic D, Barker IK, Nagy E. 2010. Avian influenza virus H13 circulating in ring-billed gulls (Larus delawarensis) in southern Ontario, Canada. Avian Dis. 54:411-419.
36. Hinshaw VS, Air GM, Gibbs AJ, Graves L, Prescott B, Karunakaran D. 1982. Antigenic and genetic characterization of a novel hemagglutinin subtype of influenza A viruses from gulls. J. Virol. 42:865-872.
37. Hofle U, Van de Bildt MW, Leijten LM, Van Amerongen G, Verhagen JH, Fouchier RA, Osterhaus AD, Kuiken T. 2012. Tissue tropism and pathology of natural influenza virus infection in black-headed gulls (Chroicocephalus ridibundus). Avian Pathol. 41:547-553.
38. Zhang W, Qi J, Shi Y, Li Q, Gao F, Sun Y, Lu X, Lu Q, Vavricka CJ, Liu D, Yan J, Gao GF. 2010. Crystal structure of the swine-origin A (H1N1)2009 influenza A virus hemagglutinin (HA) reveals similar antigenicity to that of the 1918 pandemic virus. Protein Cell 1:459-467.
39. Vaguine AA, Richelle J, Wodak SJ. 1999. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr. D Biol. Crystallogr. 55:191-205.
40. Read RJ. 2001. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 57:1373-1382.
41. Collaborative Computational Project. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760- 763.
42. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
43. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
44. Morris AL, MacArthur MW, Hutchinson EG, Thornton JM. 1992. Stereochemical quality of protein structure coordinates. Proteins 12:345- 364.
45. Ha Y, Stevens DJ, Skehel JJ, Wiley DC. 2001. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc. Natl. Acad. Sci. U. S. A. 98:11181-11186.
46. Xuan C, Shi Y, Qi J, Zhang W, Xiao H, Gao GF. 2011. Structural vaccinology: structure-based design of influenza A virus hemagglutinin subtype-specific subunit vaccines. Protein Cell 2:997-1005.
47. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, Yu W, Ophorst C, Cox F, Korse HJ, Brandenburg B, Vogels R, Brakenhoff JP, Kompier R, Koldijk MH, Cornelissen LA, Poon LL, Peiris M, Koudstaal W, Wilson IA, Goudsmit J. 2011. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333:843-850.
48. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, Vachieri SG, Pinna D, Minola A, Vanzetta F, Silacci C, FernandezRodriguez BM, Agatic G, Bianchi S, Giacchetto-Sasselli I, Calder L, Sallusto F, Collins P, Haire LF, Temperton N, Langedijk JP, Skehel JJ, Lanzavecchia A. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333:850-856.
49. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M, Goudsmit J, Wilson IA. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251.
50. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM, Santelli E, Stec B, Cadwell G, Ali M, Wan H, Murakami A, Yammanuru A, Han T, Cox NJ, Bankston LA, Donis RO, Liddington RC, Marasco WA. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16:265-273.
51. Neumann G, Macken CA, Karasin AI, Fouchier RA, Kawaoka Y. 2012. Egyptian H5N1 influenza viruses-cause for concern? PLoS Pathog. 8:e1002932. doi:10.1371/journal.ppat.1002932.
52. Nycholat CM, McBride R, Ekiert DC, Xu R, Rangarajan J, Peng W, Razi N, Gilbert M, Wakarchuk W, Wilson IA, Paulson JC. 2012. Recognition of sialylated poly-N-acetyllactosamine chains on Nand O-linked glycans by human and avian influenza A virus hemagglutinins. Angewandte Chemie. 51:4860-4863.