Analysis of influenza virus hemagglutinin receptor binding mutants with limited receptor recognition properties and conditional replication characteristics

Journal of Virology

Volumn 85, Issue 23, 2011, Pages 12387-12398

  Bradley, Konrad C ^a   Galloway, Summer E ^a   Lasanajak, Yi ^a   Song, Xuezheng ^a   Heimburg Molinaro, Jamie ^a   Yu, Hai ^b   Chen, Xi ^b   Talekar, Ganesh R ^a   Smith, David F ^a   Cummings, Richard D ^a   Steinhauer, David A ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; INFLUENZA VIRUS HEMAGGLUTININ; PHENYLALANINE; SIALIC ACID DERIVATIVE; TYROSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING KINETICS; BINDING SITE; CELL CULTURE; CONTROLLED STUDY; ERYTHROCYTE; HEMAGGLUTINATION; INFLUENZA VIRUS; MICROARRAY ANALYSIS; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; RESPIRATORY SYSTEM; VIRUS ATTACHMENT; VIRUS MUTANT; VIRUS REPLICATION;

ANIMALS; BINDING SITES; CATTLE; CELLS, CULTURED; CHICKENS; DOGS; ERYTHROCYTES; GENETIC VECTORS; GUINEA PIGS; HEMAGGLUTINATION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HORSES; KIDNEY; MICE; MICROARRAY ANALYSIS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, VIRUS; SHEEP; TURKEY; VIRUS REPLICATION;

MUS; ORTHOMYXOVIRIDAE;

EID: 81255123327     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05570-11     Document Type: Article

References (85)

1. Abe, Y., et al. 2004. Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin. J. Virol. 78:9605-9611.
2. Alexander, D. J. 2000. A review of avian influenza in different bird species. Vet. Microbiol. 74:3-13.
3. Becker, W. B., and C. J. Uys. 1967. Experimental infection of chickens with influenza A-Tern/South Africa/1961 and Chicken/Scotland/1959 viruses. I. Clinical picture and virology. J. Comp. Pathol. 77:159-165.
4. Blixt, O., et al. 2004. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. U. S. A. 101:17033-17038.
5. Bradley, K. C., et al. 2011. Comparison of the receptor binding properties of contemporary swine isolates and early human pandemic H1N1 isolates (novel 2009 H1N1). Virology 413:169-182.
6. Chen, L., et al. 2011. Receptor specificity of subtype H1 influenza A viruses isolated from swine and humans in the United States. Virology 412:401-410.
7. Chen, X., and A. Varki. 2010. Advances in the biology and chemistry of sialic acids. ACS Chem. Biol. 5:163-176.
8. Chu, V. C., and G. R. Whittaker. 2004. Influenza virus entry and infection require host cell N-linked glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 101:18153-18158.
9. Connor, R. J., Y. Kawaoka, R. G. Webster, and J. C. Paulson. 1994. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205:17-23.
10. Cummings, R. D. 2009. The repertoire of glycan determinants in the human glycome. Mol. Biosyst. 5:1087-1104.
11. Eisen, M. B., S. Sabesan, J. J. Skehel, and D. C. Wiley. 1997. Binding of the influenza A virus to cell-surface receptors: structures of five hemagglutininsialyloligosaccharide complexes determined by X-ray crystallography. Virology 232:19-31.
12. Fouchier, R. A., et al. 2004. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl. Acad. Sci. U. S. A. 101:1356-1361.
13. Gambaryan, A., et al. 2006. Evolution of the receptor binding phenotype of influenza A (H5) viruses. Virology 344:432-438.
14. Gambaryan, A., et al. 2005. Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain. Virology 334:276-283.
15. Gambaryan, A. S., et al. 2005. Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus Res. 114:15-22.
16. Gambaryan, A. S., J. S. Robertson, and M. N. Matrosovich. 1999. Effects of egg-adaptation on the receptor-binding properties of human influenza A and B viruses. Virology 258:232-239.
17. Gamblin, S. J., et al. 2004. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838-1842.
18. Glaser, L., G. Conenello, J. Paulson, and P. Palese. 2007. Effective replication of human influenza viruses in mice lacking a major alpha2,6 sialyltransferase. Virus Res. 126:9-18.
19. Glaser, L., et al. 2005. A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J. Virol. 79:11533-11536.
20. Gottschalk, A. 1957. Neuraminidase: the specific enzyme of influenza virus and Vibrio cholerae. Biochim. Biophys. Acta 23:645-646.
21. Gottschalk, A. 1959. On the mechanism underlying initiation of influenza virus infection. Ergeb. Mikrobiol. Immunitatsforsch. Exp. Ther. 32:1-22.
22. Gulati, U., et al. 2005. Mismatched hemagglutinin and neuraminidase specificities in recent human H3N2 influenza viruses. Virology 339:12-20.
23. Hulse, D. J., R. G. Webster, R. J. Russell, and D. R. Perez. 2004. Molecular determinants within the surface proteins involved in the pathogenicity of H5N1 influenza viruses in chickens. J. Virol. 78:9954-9964.
24. Ibricevic, A., et al. 2006. Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J. Virol. 80:7469-7480.
25. Inoue, S., K. Kitajima, and Y. Inoue. 1996. Identification of 2-keto-3-deoxy-Dglycero-galactonononic acid (KDN, deaminoneuraminic acid) residues in mammalian tissues and human lung carcinoma cells. Chemical evidence of the occurrence of KDN glycoconjugates in mammals. J. Biol. Chem. 271:24341-24344.
26. Inoue, S., et al. 1998. Identification of free deaminated sialic acid (2-keto-3-deoxy-D-glycero-D-galacto-nononic acid) in human red blood cells and its elevated expression in fetal cord red blood cells and ovarian cancer cells. J. Biol. Chem. 273:27199-27204.
27. Ito, T., et al. 1998. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 72:7367-7373.
28. Ito, T., and Y. Kawaoka. 2000. Host-range barrier of influenza A viruses. Vet. Microbiol. 74:71-75.
29. Ito, T., et al. 1997. Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 227:493-499.
30. Katz, J. M., and R. G. Webster. 1988. Antigenic and structural characterization of multiple subpopulations of H3N2 influenza virus from an individual. Virology 165:446-456.
31. Kimble, B., G. R. Nieto, and D. Perez. 2010. Characterization of influenza virus sialic acid receptors in minor poultry species. Virol. J. 7:365.
32. Klenk, E., H. Faillard, and H. Lempfrid. 1955. Enzymatic effect of the influenza virus. Hoppe Seylers Z. Physiol. Chem. 301:235-246.
33. Kumari, K., et al. 2007. Receptor binding specificity of recent human H3N2 influenza viruses. Virol. J. 4:42.
34. Lin, Y. P., et al. 2000. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc. Natl. Acad. Sci. U. S. A. 97:9654-9658.
35. Lugovtsev, V. Y., D. F. Smith, and J. P. Weir. 2009. Changes of the receptorbinding properties of influenza B virus B/Victoria/504/2000 during adaptation in chicken eggs. Virology 394:218-226.
36. Maines, T. R., et al. 2009. Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 325:484-487.
37. Martin, J., et al. 1998. Studies of the binding properties of influenza hemagglutinin receptor-site mutants. Virology 241:101-111.
38. Mase, M., et al. 2005. Characterization of H5N1 influenza A viruses isolated during the 2003-2004 influenza outbreaks in Japan. Virology 332:167-176.
39. Matrosovich, M. N., et al. 1997. 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. Virology 233:224-234.
40. Medeiros, R., N. Escriou, N. Naffakh, J. C. Manuguerra, and S. van der Werf. 2001. Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 289:74-85.
41. Meisner, J., et al. 2008. Infectivity studies of influenza virus hemagglutinin receptor binding site mutants in mice. J. Virol. 82:5079-5083.
42. Mitnaul, L. J., et al. 2000. Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J. Virol. 74:6015-6020.
43. Munster, V., et al. 2007. The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J. Infect. Dis. 196:258-265.
44. Neumann, G., et al. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U. S. A. 96:9345-9350.
45. Nicholls, J. M., R. W. Chan, R. J. Russell, G. M. Air, and J. S. Peiris. 2008. Evolving complexities of influenza virus and its receptors. Trends Microbiol. 16:149-157.
46. Ohuchi, M., R. Ohuchi, A. Feldmann, and H. D. Klenk. 1997. Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J. Virol. 71:8377-8384.
47. Palese, P., K. Tobita, M. Ueda, and R. W. Compans. 1974. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 61:397-410.
48. Peiris, M., et al. 1999. Human infection with influenza H9N2. Lancet 354: 916-917.
49. Ping, J., et al. 2008. Single-amino-acid mutation in the HA alters the recognition of H9N2 influenza virus by a monoclonal antibody. Biochem. Biophys. Res. Commun. 371:168-171.
50. Reading, P. C., J. L. Miller, and E. M. Anders. 2000. Involvement of the mannose receptor in infection of macrophages by influenza virus. J. Virol. 74:5190-5197.
51. Rogers, G. N., and B. L. D'Souza. 1989. Receptor binding properties of human and animal H1 influenza virus isolates. Virology 173:317-322.
52. Rogers, G. N., G. Herrler, J. C. Paulson, and H. D. Klenk. 1986. Influenza C virus uses 9-O-acetyl-N-acetylneuraminic acid as a high affinity receptor determinant for attachment to cells. J. Biol. Chem. 261:5947-5951.
53. Rogers, G. N., et al. 1983. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 304:76-78.
54. Russell, R. J., D. J. Stevens, L. F. Haire, S. J. Gamblin, and J. J. Skehel. 2006. Avian and human receptor binding by hemagglutinins of influenza A viruses. Glycoconj. J. 23:85-92.
55. Sauter, N. K., et al. 1992. Binding of influenza virus hemagglutinin to analogs of its cell-surface receptor, sialic acid: analysis by proton nuclear magnetic resonance spectroscopy and X-ray crystallography. Biochemistry 31:9609-9621.
56. Seidel, W., et al. 1991. Intraepidemic variants of influenza virus H3 hemagglutinin differing in the number of carbohydrate side chains. Arch. Virol. 120:289-296.
57. Shelton, H., et al. 2011. Receptor binding profiles of avian influenza virus hemagglutinin subtypes on human cells as a predictor of pandemic potential. J. Virol. 85:1875-1880.
58. Shinya, K., et al. 2006. Avian flu: influenza virus receptors in the human airway. Nature 440:435-436.
59. Shortridge, K. F., et al. 1998. Characterization of avian H5N1 influenza viruses from poultry in Hong Kong. Virology 252:331-342.
60. Sillanaukee, P., M. Pönniö, and I. P. Jääskeläinen. 1999. Occurrence of sialic acids in healthy humans and different disorders. Eur. J. Clin. Invest. 29:413-425.
61. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
62. Smith, D. F., X. Song, and R. D. Cummings. 2010. Use of glycan microarrays to explore specificity of glycan-binding proteins. Methods Enzymol. 480:417-444.
63. Song, X., et al. 2009. Generation of a natural glycan microarray using 9-fluorenylmethyl chloroformate (FmocCl) as a cleavable fluorescent tag. Anal. Biochem. 395:151-160.
64. Song, X., et al. 2011. Shotgun glycomics: a microarray strategy for functional glycomics. Nat. Methods 8:85-90.
65. Song, X., et al. 2011. A sialylated glycan microarray reveals novel interactions of modified sialic acids with proteins and viruses. J. Biol. Chem. 286:31610-31622.
66. Stevens, D. J., et al. 2008. Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J. Mol. Biol. 381:1382-1394.
67. Stevens, J., et al. 2006. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 355:1143-1155.
68. Stevens, J., et al. 2010. Receptor specificity of influenza A H3N2 viruses isolated in mammalian cells and embryonated chicken eggs. J. Virol. 84: 8287-8299.
69. Stray, S. J., R. D. Cummings, and G. M. Air. 2000. Influenza virus infection of desialylated cells. Glycobiology 10:649-658.
70. Van Poucke, S. G., J. M. Nicholls, H. J. Nauwynck, and K. Van Reeth. 2010. Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. Virol. J. 7:38.
71. Varki, A. 2010. Colloquium paper: uniquely human evolution of sialic acid genetics and biology. Proc. Natl. Acad. Sci. U. S. A. 107(Suppl. 2):8939-8946.
72. Varki, A. 1992. Diversity in the sialic acids. Glycobiology 2:25-40.
73. Viswanathan, K., et al. 2010. Determinants of glycan receptor specificity of H2N2 influenza A virus hemagglutinin. PLoS One 5:e13768.
74. Wagner, R., M. Matrosovich, and H. D. Klenk. 2002. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev. Med. Virol. 12:159-166.
75. Wagner, R., T. Wolff, A. Herwig, S. Pleschka, and H. D. Klenk. 2000. Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: a study by reverse genetics. J. Virol. 74:6316-6323.
76. Wang, C. C., et al. 2009. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc. Natl. Acad. Sci. U. S. A. 106:18137-18142.
77. Watowich, S. J., J. J. Skehel, and D. C. Wiley. 1994. Crystal structures of influenza virus hemagglutinin in complex with high-affinity receptor analogs. Structure 2:719-731.
78. Webster, R. G., W. J. Bean, O. T. Gorman, T. M. Chambers, and Y. Kawaoka. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56:152-179.
79. Weis, W., et al. 1988. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333:426-431.
80. Wiley, D. C., I. A. Wilson, and J. J. Skehel. 1981. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373-378.
81. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-373.
82. Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza A (H5N1) Virus, et al. 2008. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 358:261-273.
83. Yamada, S., et al. 2006. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444:378-382.
84. Yang, Z. Y., et al. 2007. Immunization by avian H5 influenza hemagglutinin mutants with altered receptor binding specificity. Science 317:825-828.
85. Yen, H. L., et al. 2009. Changes in H5N1 influenza virus hemagglutinin receptor binding domain affect systemic spread. Proc. Natl. Acad. Sci. U. S. A. 106:286-291.