Human H3N2 Influenza Viruses Isolated from 1968 To 2012 Show Varying Preference for Receptor Substructures with No Apparent Consequences for Disease or Spread

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Gulati, Shelly ^a   Smith, David F ^b   Cummings, Richard D ^b   Couch, Robert B ^c   Griesemer, Sara B ^d   St George, Kirsten ^d   Webster, Robert G ^e   Air, Gillian M ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d WADSWORTH CENTER   (United States)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; N ACETYLGALACTOSAMINE; OSELTAMIVIR; POLYLACTOSAMINE; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; POLYSACCHARIDE; SIALIC ACID DERIVATIVE; VIRUS RECEPTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EGG; EPIDEMIC; FEMALE; GENETIC VARIABILITY; INFLUENZA VIRUS A H3N2; MAMMAL CELL; MDCK CELL; NONHUMAN; PROTEIN STRUCTURE; RECEPTOR BINDING; VIRUS ATTACHMENT; VIRUS CULTURE; VIRUS ENTRY; VIRUS GENE; VIRUS ISOLATION; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; DOG; GENETICS; HUMAN; INFLUENZA; INFLUENZA A VIRUS (H3N2); ISOLATION AND PURIFICATION; MALE; MDCK CELL LINE; METABOLISM;

AVIAN INFLUENZA VIRUS; HUMAN INFLUENZA VIRUS; MAMMALIA; ORTHOMYXOVIRIDAE;

ANIMALS; DOGS; FEMALE; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MALE; POLYSACCHARIDES; RECEPTORS, VIRUS; SIALIC ACIDS;

EID: 84879273256     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066325     Document Type: Article

References (43)

1. Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, et al. (1983) Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 304: 76-78.
2. Amonsen M, Smith DF, Cummings RD, Air GM, (2007) Human parainfluenza viruses hPIV1 and hPIV3 bind oligosaccharides with alpha2-3-linked sialic acids that are distinct from those bound by H5 avian influenza virus hemagglutinin. J Virol 81: 8341-8345.
3. Tappert MM, Smith DF, Air GM, (2011) Fixation of oligosaccharides to a surface may increase the susceptibility to human parainfluenza virus 1, 2, or 3 hemagglutinin-neuraminidase. J Virol 85: 12146-12159.
4. Gulati S, Smith DF, Air GM, (2009) Deletions of neuraminidase and resistance to oseltamivir may be a consequence of restricted receptor specificity in recent H3N2 influenza viruses. Virol J 6: 22.
5. Kumari K, Gulati S, Smith DF, Gulati U, Cummings RD, et al. (2007) Receptor binding specificity of recent human H3N2 influenza viruses. Virol J 4: 42.
6. Meisen I, Dzudzek T, Ehrhardt C, Ludwig S, Mormann M, et al. (2012) The human H3N2 influenza viruses A/Victoria/3/75 and A/Hiroshima/52/2005 preferentially bind to alpha2-3-sialylated monosialogangliosides with fucosylated poly-N-acetyllactosaminyl chains. Glycobiology 22: 1055-1076.
7. Nycholat CM, McBride R, Ekiert DC, Xu R, Rangarajan J, et al. (2012) Recognition of sialylated poly-N-acetyllactosamine chains on N- and O-linked glycans by human and avian influenza A virus hemagglutinins. Angew Chem Int Ed Engl 51: 4860-4863.
8. Stevens J, Chen LM, Carney PJ, Garten R, Foust A, et al. (2010) Receptor specificity of influenza A H3N2 viruses isolated in mammalian cells and embryonated chicken eggs. J Virol 84: 8287-8299.
9. Ito T, Suzuki Y, Mitnaul L, Vines A, Kida H, et al. (1997) Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 227: 493-499.
10. Lin YP, Xiong X, Wharton SA, Martin SR, Coombs PJ, et al. (2012) Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. Proc Natl Acad Sci U S A 109: 21474-21479.
11. Lin YP, Gregory V, Collins P, Kloess J, Wharton S, et al. (2010) Neuraminidase receptor binding variants of human influenza A(H3N2) viruses resulting from substitution of aspartic acid 151 in the catalytic site: a role in virus attachment? J Virol 84: 6769-6781.
12. Zhu X, McBride R, Nycholat CM, Yu W, Paulson JC, et al. (2012) Influenza virus neuraminidases with reduced enzymatic activity that avidly bind sialic acid receptors. J Virol 86: 13371-13383.
13. Squires RB, Noronha J, Hunt V, Garcia-Sastre A, Macken C, et al. (2012) Influenza research database: an integrated bioinformatics resource for influenza research and surveillance. Influenza Other Respi Viruses 6: 404-416.
14. Rocha EP, Xu X, Hall HE, Allen JR, Regnery HL, et al. (1993) Comparison of 10 influenza A (H1N1 and H3N2) haemagglutinin sequences obtained directly from clinical specimens to those of MDCK cell- and egg-grown viruses. J Gen Virol 74: 2513-2518.
15. Katz JM, Wang M, Webster RG, (1990) Direct sequencing of the HA gene of influenza (H3N2) virus in original clinical samples reveals sequence identity with mammalian cell-grown virus. J Virol 64: 1808-1811.
16. Li D, Saito R, Suzuki Y, Sato I, Zaraket H, et al. (2009) In vivo and in vitro alterations in influenza A/H3N2 virus M2 and hemagglutinin genes: effect of passage in MDCK-SIAT1 cells and conventional MDCK cells. J Clin Microbiol 47: 466-468.
17. Oh DY, Barr IG, Mosse JA, Laurie KL, (2008) MDCK-SIAT1 cells show improved isolation rates for recent human influenza viruses compared to conventional MDCK cells. J Clin Microbiol 46: 2189-2194.
18. Asaoka N, Tanaka Y, Sakai T, Fujii Y, Ohuchi R, et al. (2006) Low growth ability of recent influenza clinical isolates in MDCK cells is due to their low receptor binding affinities. Microbes Infect 8: 511-519.
19. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
20. Sauter NK, Hanson JE, Glick GD, Brown JH, Crowther RL, 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.
21. Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, 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.
22. Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P, (2008) Cellular proteins in influenza virus particles. PLoS Pathog 4: e1000085.
23. Arinaminpathy N, Grenfell B, (2010) Dynamics of glycoprotein charge in the evolutionary history of human influenza. PLoS One 5: e15674.
24. Kobayashi Y, Suzuki Y, (2012) Compensatory evolution of net-charge in influenza A virus hemagglutinin. PLoS One 7: e40422.
25. Rice P, Longden I, Bleasby A, (2000) EMBOSS: The European Molecular Biology Open Software Suite (2000) Trends in Genetics. 16: 276-277.
26. Gulati S, Lasanajak Y, Smith DF, Cummings RD, Air GM. Glycan array analysis of influenza H1N1 binding and release. Disease Markers in press.
27. Laver WG, Air GM, Webster RG, (1981) Antigenicity of influenza virus hemagglutinin following chemical modification. Virology 111: 538-548.
28. Prieto PA, Smith DF, (1985) A new ganglioside in human meconium detected by antiserum against the human milk sialyloligosaccharide, LS-tetrasaccharide b. Arch Biochem Biophys 241: 281-289.
29. Lee EU, Roth J, Paulson JC, (1989) Alteration of terminal glycosylation sequences on N-linked oligosaccharides of Chinese hamster ovary cells by expression of beta-galactoside alpha 2,6-sialyltransferase. J Biol Chem 264: 13848-13855.
30. Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S, (2001) Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 289: 74-85.
31. Nobusawa E, Ishihara H, Morishita T, Sato K, Nakajima K, (2000) 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: 587-596.
32. Aich U, Beckley N, Shriver Z, Raman R, Viswanathan K, et al. (2011) Glycomics-based analysis of chicken red blood cells provides insight into the selectivity of the viral agglutination assay. FEBS J 278: 1699-1712.
33. Ghate AA, Air GM, (1998) Site-directed mutagenesis of catalytic residues of influenza virus neuraminidase as an aid to drug design. Eur J Biochem 258: 320-331.
34. Fazekas de St Groth S (1977) Antigenic, adaptive and adsorptive variants of the influenza haemagglutinin. In: Laver WG, Bachmayer H, Weil R, editors. The influenza hemagglutinin (Symposium, Baden near Vienna, March 21-23, 1977). Wien: Springer-Verlag.
35. Hensley SE, Das SR, Bailey AL, Schmidt LM, Hickman HD, et al. (2009) Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326: 734-736.
36. Nobusawa E, Omagari K, Nakajima S, Nakajima K, (2012) Reactivity of human convalescent sera with influenza virus hemagglutinin protein mutants at antigenic site A. Microbiol Immunol. 56: 99-106.
37. Laver WG, Air GM, Webster RG, (1981) Mechanism of antigenic drift in influenza virus. Amino acid sequence changes in an antigenically active region of Hong Kong (H3N2) influenza virus hemagglutinin. J Mol Biol 145: 339-361.
38. Sato K, Morishita T, Nobusawa E, Tonegawa K, Sakae K, et al. (2004) Amino-acid change on the antigenic region B1 of H3 haemagglutinin may be a trigger for the emergence of drift strain of influenza A virus. Epidemiol Infect 132: 399-406.
39. Popova L, Smith K, West AH, Wilson PC, James JA, et al. (2012) Immunodominance of antigenic site B over site A of hemagglutinin of recent H3N2 influenza viruses. PLoS One 7: e41895.
40. Walther T, Karamanska R, Chan RW, Chan MC, Jia N, et al. (2013) Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection. PLoS Pathog 9: e1003223.
41. Heimburg-Molinaro J, Tappert M, Song X, Lasanajak Y, Air G, et al. (2012) Probing virus-glycan interactions using glycan microarrays. Methods Mol Biol 808: 251-267.
42. Cholleti SR, Agravat S, Morris T, Saltz JH, Song X, et al. (2012) Automated motif discovery from glycan array data. OMICS 16: 497-512.
43. Macken C, Lu H, Goodman J, Boykin L (2001) The value of a database in surveillance and vaccine selection. In: Osterhaus ADME, Cox NJ, Hampson AW, editors. Options for the Control of Influenza IV. Amsterdam: Elsevier. 103-106.