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Review

Sialic acid receptors: focus on their role in influenza infection

Pages 1-11 | Published online: 10 Apr 2018

References

  • Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinin of influenza A viruses. Virology. 1991;182(2):475–485.
  • Wiley DC, Skehel JJ. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu Rev Biochem. 1981;56:365–394.
  • Matrosovich MN, Gambarayan AS, Teneberg S, et al. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and ganglosides and by a higher conservation of the HA receptor-binding site. Virology. 1997;233(1):224–234.
  • Varki A, Cummings R, Esko J, Freeze H, Hart G, Marth J. Essentials of Glycobiology. NY, USA: Cold Spring Harbor Laboratory Press; 1999.
  • Couceiro JN, Paulson JC, Baum LG. Influenza virus strains selectively recognize sialyloligosaccarides on human respiratory epithelium, the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res. 1993;29(2):155–165.
  • Costa T, Chaves AJ, Valle R, et al. Distribution patterns of influenza virus receptors and viral attachment patterns in the respiratory and intestinal tracts of seven avian species. Vet Res. 2012;43:28.
  • Thontiravong A, Kitikoon P, Wannaratana S, et al. Quail as a potential mixing vessel for the generation of new reassortant influenza A viruses. Vet Microbiol. 2012;160(3–4):305–313.
  • Matrosovich M, Tuzikov A, Bovin N, et al. Early alterations of the receptor-binding properties of H1, H2 and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol. 2000;74(18):8502–8512.
  • Ito T, Suzuki Y, Mitnaul L, Vines A, Kida H, Kawaoka Y. Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology. 1997;227(2):493–499.
  • Baum LG, Paulson JC. Sialyloligosaccarides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl. 1990;40:35–38.
  • Gambarayan AS, Robertson JS, Matrosovich MN. Effects of egg-adaptation on the receptor binding properties of human influenza A and B viruses. Virology. 1999;258(2):232–239.
  • Mochalova L, Gambarayan A, Romanova J, et al. Receptor-binding properties of modern human influenza viruses primarily isolated in Vero and MDCK cells and chicken embryionated eggs. Virology. 2003;313(2):473–480.
  • Paulson JC, Blixt O, Collins BE. Sweet spots in functional glycomics. Nat Chem Biol. 2006;2(5):238–248.
  • Blixt O, Head S, Mondala T, et al. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci U S A. 2004;101(49):17033–17038.
  • Stevens J, Blixt O, Glaser L, et al. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol. 2006;355(5):1143–1155.
  • Childs RA, Palma AS, Wharton S, et al. Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray. Nat Biotechnol. 2009;27(9):797–799.
  • Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A. 2004;101(13):4620–4624.
  • Thompson C, Barclay WS, Zambon MC, Pickles RJ. Infection of human airway epithelium by human and avian strains of influenza A virus. J Virol. 2006;80(16):8060–8068.
  • Yamada S, Suzuki Y, Suzuki T, et al. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature. 2006;444(7117):378–382.
  • Medeiros R, Escriou N, Naffakh N, Manuguerra JC, van der Werf S. Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology. 2001;289(1):74–85.
  • Nobusawa E, Ishihara H. Morishita T, Sato K, Nakajima K. 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. 2000;278(2):587–596.
  • Glaser L, Stevens J, Zamarin D, et al. A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J Virol. 2005;79(17):11533–11536.
  • Tumpey TM, Maines TR, Van Hoeven N, et al. A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science. 2007;315(5812):655–659.
  • Scholtissek C. Source for influenza pandemics. Eur J Epidemiol. 1994;10:455–458.
  • Ito T, Couceiro JN, Kelm S, et al. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol. 1998;72(9):7367–7373.
  • Bradley KC, Jones CA, Tompkins SM, et al. Comparison of the receptor binding properties of contemporary swine isolates and early human pandemic H1N1 isolates (Novel 2009 H1N1). Virology. 2011;413(2):169–182.
  • Chen LM, Rivailler P, Hossain J, et al. Receptor specificity of subtype H1 influenza A viruses isolated from swine and humans in the United States. Virology. 2011;412(2):401–410.
  • Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y. Influenza virus receptors in the human airway. Nature. 2006;440(7083):435–436.
  • Shinya K, Hatta M, Yamada S, et al. Characterization of a human H5N1 influenza A virus isolated in 2003. J Virol. 2005;79(15):9926–9932.
  • Chen H, Wen X, To KK, et al. Quasispecies of the D225G substitution in the hemagglutinin of pandemic influenza A(H1N1) 2009 virus from patients with severe disease in Hong Kong, China. J Infect Dis. 2010;201(10):1517–1521.
  • Moussi AE, Kacem MA, Pozo F, et al. Frequency of D222G haemagglutinin mutant of pandemic (H1N1) pdm09 influenza virus in Tunisia between 2009 and 2011. Diagn Pathol. 2013;8:124.
  • Ledesma J, Pozoa F, Pérez Ruiz M, et al. Substitutions in position 222 of haemagglutinin of pandemic influenza A (H1N1) 2009 viruses in Spain. J Clin Virol. 2011;51(1):75–78.
  • Rykkvin R, Kilander A, Dudman SG, Hungnes O. Within-patient emergence of the influenza A(H1N1) pdm09 HA1 222G variant and clear association with severe disease, Norway. Euro Surveill. 2013;18(3):20369.
  • Vazquez-Perez JA, Isa P, Kobasa D, et al. A (H1N1) pdm09 HA D222 variants associated with severity and mortality in patients during a second wave in Mexico. Virol J. 2013;10:41.
  • Abed Y, Pizzorno A, Hamelin ME, et al. The 2009 pandemic H1N1 D222G hemagglutinin mutation alters receptor specificity and increases virulence in mice but not in ferrets. J Infect Dis. 2011;204(7):1008–1016.
  • Casalegno JS, Ferraris O, Escuret V, et al. Functional balance between the hemagglutinin and neuraminidase of influenza A(H1N1)pdm09 HA D222 variants. PLos One. 2014;9(8):e104009.
  • Chutinimitkul S, Herfst S, Steel J, et al. Virulence-associated substitution D222G in the hemagglutinin of 2009 pandemic influenza A(H1N1) virus affects receptor binding. J Virol. 2010;84(22):11802–22813.
  • Baldanti F, Campanini G, Piralla A, et al. Severe outcome of influenza A/H1N1/09v infection associated with 222G/N polymorphisms in the haemagglutinin: a multicentre study. Clin Microbiol Infect. 2011;17(8):1166–1169.
  • Resende PC, Motta FC, Oliveira MLA, et al. Polymorphisms at residue 222 of the hemagglutinin of pandemic influenza A(H1N1)pdm09: association of quasispecies to morbidity and mortality in different risk categories. PLos One. 2014;9(3):e92789.
  • Houng HS, Garner J, Zhou Y, et al. Emergent 2009 influenza A(H1N1) viruses containing HA D222N mutation associated with severe clinical outcomes in the Americas. J Clin Virol. 2012;53(1):12–15.
  • Matos-Patrón A, Byrd-Leotis L, Steinhauer DA, Barclay WS, Ayora-Talavera G. Amino acid substitution D222N from fatal influenza infections affects receptor-binding properties of the influenza A(H1N1)pdm09 virus. Virology. 2015;484:15–21.
  • McCauley J, Daniels R, Lin YP, Xiang Z, Gregory V, Whittaker L. Report Prepared for the WHO Annual Consultation on the Composition of Influenza Vaccine for the Northern Hemisphere 2016–2017. World Health Organization: Place, Geneva, Switzerland; 2016.
  • de Vries RP, de Vries E, Martínez-Romero C, et al. Evolution of the hemagglutinin protein of the new pandemic H1N1 influenza virus: maintaining optimal receptor binding by compensatory substitutions. J Virol. 2013;87(24):13868–13877.
  • Hensley SE, Das SR, Bailey AL, et al. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science. 2009;326(5953):734–736.
  • Koel BF, Mögling R, Chutinimitkul S, et al. Identification of amino acid substitutions supporting antigenic change in influenza A(H1N1)pdm09 viruses. J Virol. 2015;89(7):3763–3775.
  • Koel BF, Burke DF, Bestebroer TM, et al. Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution. Science. 2013;342(6161):976–979.
  • Smith DJ, Lapedes AS, de Jong JC, et al. Mapping the antigenic and genetic evolution of influenza virus. Science. 2004;305(5682):371–376.
  • Lin YP, Xiong X, Wharton SA, et al. Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. Proc Natl Acad Sci U S A. 2012;109(52):21474–21479.
  • Gulati S, Smith DF, Cummings RD, et al. 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. 2013;8(6):e66325.
  • Peng W, de Vries RP, Grant OC, et al. Recent H3N2 viruses have evolved specificity for extended, branched huma-type receptors, confering potential for increased avidity. Cell Host Microbe. 2017;21(1):23–34.
  • Ampofo WK, Al Busaidy S, Cox NJ, et al; WHO Writing Group. Strengthening the influenza vaccine virus selection and development process: outcome of the 2nd WHO informal consultation for improving influenza vaccine virus selection held at the Centre International de Conférences (CICG) Geneva, Switzerland, 7 to 9 December 2011. Vaccine. 2013;31(32):3209–3221.
  • Kurtz J, Manvell RJ, Banks J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet. 1996;348(9031):901–902.
  • Webster RG, Geraci J, Petursson G, Skirnisson K. Conjunctivitis in human beings caused by influenza A virus of seals. N Engl J Med. 1981;304(15):911.
  • Connor RJ, Kawaoka Y, Webster RG, Paulson JC. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology. 1994;205(1):17–23.
  • WHO. Evolution of H5N1 avian influenza viruses in Asia. Global influenza program surveillance network. Emerg Infect Dis. 2005;11(10):1515–1521.
  • WHO/OIE/FAO H5N1 Evolution Working Group. Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis. 2008;14(7):e1.
  • de Vries E, Guo H, Dai M, Rottier PJ, van Kuppeveld FJ, de Haan CA. Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 hemagglutinin variant. Emerg Infect Dis. 2015;21(5):842–846.
  • Saito T, Tanikawa T, Uchida Y, Takemae N, Kanehira K, Tsunekuni R. Intracontinental and intercontinental dissemination of Asian H5 highly pathogenic avian influenza virus (clade 2.3.4.4) in the winter of 2014–2015. Rev Med Virol. 2015;25(6):388–405.
  • Ip HS, Torchetti MK, Crespo R, et al. Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014. Emerg Infect Dis. 2015;21(5):886–890.
  • Bi Y, Chen Q, Wang Q, et al. Genesis, evolution and prevalence of H5N6 avian influenza viruses in China. Cell Host Microbe. 2016;20(6):810–821.
  • Herfst S, Mok CKP, van den Brans JMA, et al. Human clade 2.3.4.4 A/H5N6 influenza virus lacks mammalian adaptation markers and does not transmit via the airborne route between ferrets. mSphere. 2018;3(1):e00405–e00417.
  • Gambarayan AS, Tuzikov AB, Pazynina GV, Webster RG, Matrosovich MN, Bovin NV. H5N1 chicken influenza viruses display a high binding affinity for Neu5Aca2-3GalB1-4(6-HS03)GlcNac-containing receptors. Virology. 2004;326(2):310–316.
  • Gambarayan A, Tuzikov A, Pazynina G, Bovin N, Balish A, Klimov A. Evolution of the receptor binding phenotype of influenza A(H5) viruses. Virology. 2006;344(2):432–438.
  • Ha Y, Stevens DJ, Skehel JJ, Wiley DC. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinin bound to avian and human receptor analogs. Proc Natl Acad Sci U S A. 2001;98(20):11181–11186.
  • Iwatsuki-Horimoto K, Kanazawa R, Sugii S, Kawaoka Y, Horimoto T. The index influenza A virus subtype H5N1 isolated from a human in 1997 differs in its receptor-binding properties from a virulent avian influenza virus. J Gen Virol. 2004;85(Pt 4):1001–1005.
  • Matrosovich M, Zhou N, Kawaoka Y, Webster R. The surface glycoprotein of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol. 1999;73(2):1146–1155.
  • Puthavathana P, Auewarakul P, Charoenying PC, et al. Molecular characterization of the complete genome of human influenza H5N1 virus isolated from Thailand. J Gen Virol. 2005;86(Pt 2):423–433.
  • Guo H, de Vries E, McBride R, et al. Highly pathogenic influenza A(H5Nx) viruses with altered H5 receptor-binding specificity. Emerg Infect Dis. 2017;23(2):220–231.
  • Kaplan BS, Russier M, Jeevan T, et al. Novel highly pathogenic avian A(H5N2) and A(H5N8) influenza viruses of clade 2.3.4.4 from North America have limited capacity for replication and transmission in mammals. mSphere. 2016;1(2):e00003–e00016.
  • Ayora-Talavera G, Shelton H, Scull MA, et al. Mutations in H5N1 influenza virus hemagglutinin that confer binding to human tracheal airway epithelium. PLos One. 2009;4(11):e7836.
  • Xiong X, Tuzikov A, Coombs PJ, et al. Recognition of sulphated and fucosylated receptor sialosides by A/Vietnam/1194/2004 (H5N1) influenza virus. Virus Res. 2013;178(1):12–14.
  • Herfst S, Schrauwen EJ, Linster M, et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science. 2012;336(6088):1534–1541.
  • Imai M, Watanabe T, Hatta M, et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature. 2012;486(7403):420–428.
  • Hatta M, Gao P, Halfmann P, Kawaoka Y. Molecular basis for high virulence of Hong Kong H5N1 inluenza A viruses. Science. 2001;293(5536):1840–1842.
  • Subbarao EK, London W, Murphy BR. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol. 1993;67(4):1761–1764.
  • WHO. Influenza at the Human-Animal Interface. Summary and Assessment, 16 June 2017 to 25 July 2017. World Health Organization: Place, Geneva, Switzerland; 2017.
  • Gao R, Cao B, Hu Y, et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013;368(20):1888–1897.
  • Belser JA Gustin K, Pearce MB, et al. Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature. 2013;501(7468):556–559.
  • Watanabe T, Kiso M, Fukuyama S, et al. Characterization of H7N9 influenza A viruses isolated from humans. Nature. 2013;501(7468):551–555.
  • Richard M, Schrauwen EJ, de Graaf M, et al. Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature. 2013;501(7468):560–563.
  • Xu L, Bao L, Deng W, et al. Novel avian-origin human influenza A(H7N9) can be transmitted between ferrets via respiratory droplets. J Infect Dis. 2014;209(4):551–556.
  • Zhang Q Shi J, Deng G, et al. H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science. 2013;341(6144):410–414.
  • Dormant JC, Dekkers J, Wickramasinghe IN, et al. Adaptation of novel H7N9 influenza A virus to human receptors. Sci Rep. 2013;3:3058.
  • Schrauwen EJ, Richard M, Burke DF, Rimmelzwaan GF, Herfst S, Fouchier RA. Amino acid substitutions that affect receptor binding and stability of the hemagglutinin of influenza A/H7N9 virus. J Virol. 2016;90(7):3794–3799.
  • Shi Y, Zhang W, Wang F, et al. Structures and Receptor binding of hemagglutinins from human-infecting H7N9 influenza viruses. Science. 2013;342(6155):243–247.
  • Xiong X, Martin SR, Haire LF, et al. Receptor binding by an H7N9 influenza virus from humans. Nature. 2013;499(7459):496–499.
  • Xu R, de Vries RP, Zhu X, et al. Preferential recognition of avian-like receptors in human influenza A H7N9 viruses. Science. 2013;342(6163):1230–1235.
  • Tharakaraman K, Jayaraman A, Raman R, et al. Glycan receptor binding of the influenza A virus H7N9 hemagglutinin. Cell. 2013;153(7):1486–1493.
  • de Vries RP, Peng W, Grant OC, et al. Three mutations switch H7N9 influenza to human-type receptor specificity. PLoS Pathog. 2017;13(6):e1006390.
  • Fouchier RA, Schneeberger PM, Rozendaal FW, et al. 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. 2004;101(5):1356–1361.
  • Puzelli S, Di Trani L, Fabiani C, et al. Serological analysis of serum samples from humans exposed to avian H7 influenza viruses in Italy between 1999 and 2003. J Infect Dis. 2005;192(8):1318–1322.
  • Belser JA, Blixt O, Chen LM, et al. Contemporary North American influenza H7 viruses possess human receptor specificity: implications for virus transmissibility. Proc Natl Acad Sci U S A. 2008;105(21):7558–7563.
  • Belser JA, Creager H, Zeng H, Maines TR, Tumpey TM. Pathogenesis, transmissibility, and tropism of a highly pathogenic avian influenza A(H7N7) virus associated with human conjunctivits in Italy, 2013. J Infect Dis. 2017;216(Suppl 4):S508–S511.
  • Olofsson S, Kumlin U, Dimock K, Arnberg N. Avian influenza and sialic acid receptors: more than meets the eye? Lancet Infect Dis. 2005;5(3):184–188.
  • Tweed SA, Skowronski DM, David ST, et al. Human illness from avian influenza H7N3, British Columbia. Emerg Infect Dis. 2004;10(12):2196–2199.
  • Nguyen-Van-Tam JS, Nair P, Acheson P, et al; Incident Response Team. Outbreak of low pathogenicity H7N3 avian influenza in UK, including associated case of human conjunctivitis. Euro Surveill. 2006;11(5):E060504.
  • Lopez-Martinez I, Balish A, Barrera-Badillo G, et al. Highly pathogenic avian influenza A(H7N3) virus in poultry workers, Mexico, 2012. Emerg Infect Dis. 2013;19(9):1531–1534.
  • Marinova-Petkova A, Laplante J, Jang Y, et al. Avian influenza A(H7N2) virus in human exposed to sick cats, New York, USA, 2016. Emerg Infect Dis. 2017;23(12):2046–2049.