SpringerLink
Log in

Roles of Glycans and Non-glycans on the Epithelium and in the Immune System in H1–H18 Influenza A Virus Infections

  • Protocol
  • First Online:
Glycovirology

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2556))

Abstract

The large variation of influenza A viruses (IAVs) in various susceptible hosts and their rapid evolution, which allows host/tissue switching, host immune escape, vaccine escape, and drug resistance, are difficult challenges for influenza control in all countries worldwide. Access and binding of the IAV to actual receptors at endocytic sites is critical for the establishment of influenza infection. In this chapter, the progress in identification of and roles of glycans and non-glycans on the epithelium and in the immune system in H1–H18 IAV infections are reviewed. The first part of the review is on current knowledge of H1–H16 IAV receptors on the epithelium including sialyl glycans, other negatively charged glycans, and annexins. The second part of the review focuses on H1–H16 IAV receptors in the immune system including acidic surfactant phospholipids, Sia on surfactant proteins, the carbohydrate recognition domain (CRD) of surfactant proteins, Sia on mucins, Sia and C-type lectins on macrophages and dendritic cells, and Sia on NK cells. The third part of the review is about a possible H17–H18 IAV receptor. Binding of these receptors to IAVs may result in inhibition or enhancement of IAV infection depending on their location, host cell type, and IAV strain. Among these receptors, host sialyl glycans are key determinants of viral hemagglutinin (HA) lectins for H1–H16 infections. HA must acquire mutations to bind to sialyl glycans that are dominant on a new target tissue when switching to a new host for efficient transmission and to bind to long sialyl glycans found in the case of seasonal HAs with multiple glycosylation sites as a consequence of immune evasion. Although sialyl receptors/C-type lectins on immune cells are decoy receptors/pathogen recognition receptors for capturing viral HA lectin/glycans protecting HA antigenic sites, some IAV strains do not escape, such as by release with neuraminidase, but hijack these molecules to gain entry and replication in immune cells. An understanding of the virus–host battle tactics at the receptor level might lead to the establishment of novel strategies for effective control of influenza.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. WHO (2021) Influenza update: 22 November 2021, based on data up to 7 November 2021. https://www.who.int/teams/global-influenza-programme/surveillance-and-monitoring/influenza-updates/current-influenza-update

  2. Wu Y, Wu Y, Tefsen B et al (2014) Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol 22:183–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Fouchier RA, Munster V, Wallensten A et al (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79:2814–2822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kandeil A, Gomaa MR, Shehata MM et al (2019) Isolation and characterization of a distinct influenza A virus from Egyptian bats. J Virol 93:e01059-18

    Article  PubMed  PubMed Central  Google Scholar 

  5. Sriwilaijaroen N, Suzuki Y (2014) Molecular basis of a pandemic of avian-type influenza virus. Methods Mol Biol 1200:447–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Johnson NP, Mueller J (2002) Updating the accounts: global mortality of the 1918-1920 “Spanish” influenza pandemic. Bull Hist Med 76:105–115

    Article  PubMed  Google Scholar 

  7. Yang L, Zhao X, Li X et al (2020) Case report for human infection with a highly pathogenic avian influenza A(H5N6) virus in Bei**g, China 2019. Biosaf Health 2:49–52

    Article  Google Scholar 

  8. Yu D, **ang G, Zhu W et al (2019) The re-emergence of highly pathogenic avian influenza H7N9 viruses in humans in mainland China, 2019. Euro Surveill 24:1900273

    Article  PubMed Central  Google Scholar 

  9. Sun H, **ao Y, Liu J et al (2020) Prevalent Eurasian avian-like H1N1 swine influenza virus with 2009 pandemic viral genes facilitating human infection. Proc Natl Acad Sci U S A 117:17204–17210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. OIE (2006) OIE information document on avian influenza vaccination. https://www.oie.int/app/uploads/2013/04/guidelines20on20ai20vaccination.pdf

  11. FAO. Epidemiology of avian influenza. https://www.fao.org/avianflu/en/clinical.html

  12. CDC (2014) What people who raise pigs need to know about influenza (flu). https://www.cdc.gov/flu/swineflu/people-raise-pigs-flu.htm

  13. Tong S, Zhu X, Li Y et al (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657

    Article  PubMed  PubMed Central  Google Scholar 

  14. Zhu X, Yang H, Guo Z et al (2012) Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc Natl Acad Sci U S A 109:18903–18908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Tong S, Li Y, Rivailler P et al (2012) A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A 109:4269–4274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Campos ACA, Goes LGB, Moreira-Soto A et al (2019) Bat influenza A(HL18NL11) virus in fruit bats, Brazil. Emerg Infect Dis 25:333–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Sriwilaijaroen N, Suzuki Y (2012) Molecular basis of the structure and function of H1 hemagglutinin of influenza virus. Proc Jpn Acad Ser B Phys Biol Sci 88:226–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kida H, Yanagawa R, Matsuoka Y (1980) Duck influenza lacking evidence of disease signs and immune response. Infect Immun 30:547–553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Karakus U, Thamamongood T, Ciminski K et al (2019) MHC class II proteins mediate cross-species entry of bat influenza viruses. Nature 567:109–112

    Article  CAS  PubMed  Google Scholar 

  20. Giotis ES, Carnell G, Young EF et al (2019) Entry of the bat influenza H17N10 virus into mammalian cells is enabled by the MHC class II HLA-DR receptor. Nat Microbiol 4:2035–2038

    Article  PubMed  Google Scholar 

  21. Leyson C, Youk SS, Smith D et al (2019) Pathogenicity and genomic changes of a 2016 European H5N8 highly pathogenic avian influenza virus (clade 2.3.4.4) in experimentally infected mallards and chickens. Virology 537:172–185

    Article  CAS  PubMed  Google Scholar 

  22. Kuiken T, Taubenberger JK (2008) Pathology of human influenza revisited. Vaccine 26(Suppl 4):D59–D66

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gottschalk A (1959) Chemistry of virus receptors. In: Burnet FM, Stanley WM (eds) The viruses: biochemical, biological, and biophysical properties. Academic Press, Inc., New York, pp 51–61

    Google Scholar 

  24. Suzuki Y, Matsunaga M, Matsumoto M (1985) N-acetylneuraminyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. Binding specificity of influenza virus A/Aichi/2/68 (H3N2) to membrane-associated GM3 with different molecular species of sialic acid. J Biol Chem 260:1362–1365

    Article  CAS  PubMed  Google Scholar 

  25. Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366–373

    Article  CAS  PubMed  Google Scholar 

  26. Wu NC, Otwinowski J, Thompson AJ et al (2020) Major antigenic site B of human influenza H3N2 viruses has an evolving local fitness landscape. Nat Commun 11:1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chandrasekaran A, Srinivasan A, Raman R et al (2008) Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat Biotechnol 26:107–113

    Article  CAS  PubMed  Google Scholar 

  28. Gambaryan AS, Matrosovich TY, Boravleva EY et al (2018) Receptor-binding properties of influenza viruses isolated from gulls. Virology 522:37–45

    Article  CAS  PubMed  Google Scholar 

  29. Suzuki Y, Ito T, Suzuki T et al (2000) Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 74:11825–11831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Iwasaki M, Inoue S, Troy FA (1990) A new sialic acid analogue, 9-O-acetyl-deaminated neuraminic acid, and α2,8-linked O-acetylated poly(N-glycolylneuraminyl) chains in a novel polysialoglycoprotein from salmon eggs. J Biol Chem 265:2596–2602

    Article  CAS  PubMed  Google Scholar 

  31. Inoue S, Lin SL, Chang T 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

    Article  CAS  PubMed  Google Scholar 

  32. Suzuki Y, Nagao Y, Kato H et al (1986) Human influenza A virus hemagglutinin distinguishes sialyloligosaccharides in membrane-associated gangliosides as its receptor which mediates the adsorption and fusion processes of virus infection. Specificity for oligosaccharides and sialic acids and the sequence to which sialic acid is attached. J Biol Chem 261:17057–17061

    Article  CAS  PubMed  Google Scholar 

  33. Ito T, Suzuki Y, Suzuki T et al (2000) Recognition of N-glycolylneuraminic acid linked to galactose by the α2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J Virol 74:9300–9305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Samraj AN, Pearce OM, Laubli H et al (2015) A red meat-derived glycan promotes inflammation and cancer progression. Proc Natl Acad Sci U S A 112:542–547

    Article  CAS  PubMed  Google Scholar 

  35. Liu Y, Han C, Wang X et al (2009) Influenza A virus receptors in the respiratory and intestinal tracts of pigeons. Avian Pathol 38:263–266

    Article  CAS  PubMed  Google Scholar 

  36. Suzuki T, Horiike G, Yamazaki Y et al (1997) Swine influenza virus strains recognize sialylsugar chains containing the molecular species of sialic acid predominantly present in the swine tracheal epithelium. FEBS Lett 404:192–196

    Article  CAS  PubMed  Google Scholar 

  37. Sriwilaijaroen N, Kondo S, Yagi H et al (2011) N-glycans from porcine trachea and lung: predominant NeuAcα2-6Gal could be a selective pressure for influenza variants in favor of human-type receptor. PLoS One 6:e16302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sriwilaijaroen N, Nakakita SI, Kondo S et al (2018) N-glycan structures of human alveoli provide insight into influenza A virus infection and pathogenesis. FEBS J 285:1611–1634

    Article  CAS  PubMed  Google Scholar 

  39. Walther T, Karamanska R, Chan RW et al (2013) Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection. PLoS Pathog 9:e1003223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Bardor M, Nguyen DH, Diaz S et al (2005) Mechanism of uptake and incorporation of the non-human sialic acid N-glycolylneuraminic acid into human cells. J Biol Chem 280:4228–4237

    Article  CAS  PubMed  Google Scholar 

  41. Varki A (2009) Multiple changes in sialic acid biology during human evolution. Glycoconj J 26:231–245

    Article  CAS  PubMed  Google Scholar 

  42. Sriwilaijaroen N, Kondo S, Yagi H et al (2012) Bovine milk whey for preparation of natural N-glycans: structural and quantitative analysis. Open Glycosci 5:41–50

    Article  CAS  Google Scholar 

  43. Sack A, Cullinane A, Daramragchaa U et al (2019) Equine influenza virus—a neglected, reemergent disease threat. Emerg Infect Dis 25(6):1185–1191

    Article  PubMed Central  Google Scholar 

  44. Sriwilaijaroen N, Suzuki Y (2020) Host receptors of influenza viruses and coronaviruses-molecular mechanisms of recognition. Vaccines (Basel) 8:587

    Article  CAS  Google Scholar 

  45. Chen LM, Rivailler P, Hossain J et al (2011) Receptor specificity of subtype H1 influenza A viruses isolated from swine and humans in the United States. Virology 412:401–410

    Article  CAS  PubMed  Google Scholar 

  46. Takahashi T, Hashimoto A, Maruyama M et al (2009) Identification of amino acid residues of influenza A virus H3 HA contributing to the recognition of molecular species of sialic acid. FEBS Lett 583:3171–3174

    Article  CAS  PubMed  Google Scholar 

  47. Broszeit F, Tzarum N, Zhu X et al (2019) N-glycolylneuraminic acid as a receptor for influenza A viruses. Cell Rep 27:3284–3294.e3286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sriwilaijaroen N, Suzuki Y (2020) Sialoglycovirology of lectins: sialyl glycan binding of enveloped and non-enveloped viruses. Methods Mol Biol 2132:483–545

    Article  CAS  PubMed  Google Scholar 

  49. Sriwilaijaroen N, Suzuki K, Takashita E et al (2015) 6SLN-lipo PGA specifically catches (coats) human influenza virus and synergizes neuraminidase-targeting drugs for human influenza therapeutic potential. J Antimicrob Chemother 70:2797–2809

    Article  CAS  PubMed  Google Scholar 

  50. Gao R, Pan M, Li X et al (2016) Post-mortem findings in a patient with avian influenza A (H5N6) virus infection. Clin Microbiol Infect 22(574):e571–e575

    Google Scholar 

  51. Wu W, Air GM (2004) Binding of influenza viruses to sialic acids: reassortant viruses with A/NWS/33 hemagglutinin bind to α2,8-linked sialic acid. Virology 325:340–350

    Article  CAS  PubMed  Google Scholar 

  52. Childs RA, Palma AS, Wharton S et al (2009) Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray. Nat Biotechnol 27:797–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Matrosovich M, Stech J, Klenk HD (2009) Influenza receptors, polymerase and host range. Rev Sci Tech 28:203–217

    Article  CAS  PubMed  Google Scholar 

  54. Suzuki Y, Matsunaga M, Nagao Y et al (1985) Ganglioside GM1b as an influenza virus receptor. Vaccine 3:201–203

    Article  CAS  PubMed  Google Scholar 

  55. Gambaryan A, Yamnikova S, Lvov D 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

    Article  CAS  PubMed  Google Scholar 

  56. Suzuki Y, Nakao T, Ito T et al (1992) Structural determination of gangliosides that bind to influenza A, B, and C viruses by an improved binding assay: strain-specific receptor epitopes in sialo-sugar chains. Virology 189:121–131

    Article  CAS  PubMed  Google Scholar 

  57. Ogata M, Murata T, Murakami K et al (2007) Chemoenzymatic synthesis of artificial glycopolypeptides containing multivalent sialyloligosaccharides with a gamma-polyglutamic acid backbone and their effect on inhibition of infection by influenza viruses. Bioorg Med Chem 15:1383–1393

    Article  CAS  PubMed  Google Scholar 

  58. Hiono T, Okamatsu M, Igarashi M et al (2016) Amino acid residues at positions 222 and 227 of the hemagglutinin together with the neuraminidase determine binding of H5 avian influenza viruses to sialyl Lewis X. Arch Virol 161:307–316

    Article  CAS  PubMed  Google Scholar 

  59. Guo CT, Takahashi N, Yagi H et al (2007) The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 17:713–724

    Article  CAS  PubMed  Google Scholar 

  60. Sriwilaijaroen N, Kondo S, Yagi H et al (2009) Analysis of N-glycans in embryonated chicken egg chorioallantoic and amniotic cells responsible for binding and adaptation of human and avian influenza viruses. Glycoconj J 26:433–443

    Article  CAS  PubMed  Google Scholar 

  61. Hiono T, Okamatsu M, Nishihara S et al (2014) A chicken influenza virus recognizes fucosylated α2,3 sialoglycan receptors on the epithelial cells lining upper respiratory tracts of chickens. Virology 456–457:131–138

    Article  PubMed  Google Scholar 

  62. Lin YP, **ong X, Wharton SA 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Yang H, Carney P, Stevens J (2010) Structure and receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr 2:RRN1152

    Article  PubMed  PubMed Central  Google Scholar 

  64. Gulati S, Smith DF, Cummings RD et al (2013) 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 8:e66325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kuiken T, Fouchier R, Rimmelzwaan G et al (2011) Pigs, poultry, and pandemic influenza: how zoonotic pathogens threaten human health. Adv Exp Med Biol 719:59–66

    Article  PubMed  PubMed Central  Google Scholar 

  66. WHO (2009) Clinical management of human infection with pandemic (H1N1) 2009: revised guidance. http://who.int/csr/resources/publications/swineflu/clinical_management_h1n1.pdf

  67. Shieh WJ, Blau DM, Denison AM et al (2010) 2009 pandemic influenza A (H1N1): pathology and pathogenesis of 100 fatal cases in the United States. Am J Pathol 177:166–175

    Article  PubMed  PubMed Central  Google Scholar 

  68. Chu VC, Whittaker GR (2004) Influenza virus entry and infection require host cell N-linked glycoprotein. Proc Natl Acad Sci U S A 101:18153–18158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. de Vries E, de Vries RP, Wienholts MJ et al (2012) Influenza A virus entry into cells lacking sialylated N-glycans. Proc Natl Acad Sci U S A 109:7457–7462

    Article  PubMed  PubMed Central  Google Scholar 

  70. Fujioka Y, Nishide S, Ose T et al (2018) A sialylated voltage-dependent Ca2+ channel binds hemagglutinin and mediates influenza A virus entry into mammalian cells. Cell Host Microbe 23:809–818.e805

    Article  CAS  PubMed  Google Scholar 

  71. Eierhoff T, Hrincius ER, Rescher U et al (2010) The epidermal growth factor receptor (EGFR) promotes uptake of influenza A viruses (IAV) into host cells. PLoS Pathog 6:e1001099

    Article  PubMed  PubMed Central  Google Scholar 

  72. Chan CM, Chu H, Zhang AJ et al (2016) Hemagglutinin of influenza A virus binds specifically to cell surface nucleolin and plays a role in virus internalization. Virology 494:78–88

    Article  CAS  PubMed  Google Scholar 

  73. Upham JP, Pickett D, Irimura T et al (2010) Macrophage receptors for influenza A virus: role of the macrophage galactose-type lectin and mannose receptor in viral entry. J Virol 84:3730–3737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Mao H, Tu W, Qin G et al (2009) Influenza virus directly infects human natural killer cells and induces cell apoptosis. J Virol 83:9215–9222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Rapoport EM, Mochalova LV, Gabius HJ et al (2006) Search for additional influenza virus to cell interactions. Glycoconj J 23:115–125

    Article  CAS  PubMed  Google Scholar 

  76. Byrd-Leotis L, Jia N, Dutta S et al (2019) Influenza binds phosphorylated glycans from human lung. Sci Adv 5:eaav2554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Otto M, Gunther A, Fan H et al (1994) Identification of annexin 33 kDa in cultured cells as a binding protein of influenza viruses. FEBS Lett 356:125–129

    Article  CAS  PubMed  Google Scholar 

  78. Huang RT, Lichtenberg B, Rick O (1996) Involvement of annexin V in the entry of influenza viruses and role of phospholipids in infection. FEBS Lett 392:59–62

    Article  CAS  PubMed  Google Scholar 

  79. Arora S, Lim W, Bist P et al (2016) Influenza A virus enhances its propagation through the modulation of Annexin-A1 dependent endosomal trafficking and apoptosis. Cell Death Differ 23:1243–1256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Guo CT, Ohta S, Yoshimoto A et al (2001) A unique phosphatidylinositol bearing a novel branched-chain fatty acid from Rhodococcus equi binds to influenza virus hemagglutinin and inhibits the infection of cells. J Biochem 130:377–384

    Article  CAS  PubMed  Google Scholar 

  81. Numata M, Mitchell JR, Tipper JL et al (2020) Pulmonary surfactant lipids inhibit infections with the pandemic H1N1 influenza virus in several animal models. J Biol Chem 295:1704–1715

    Article  CAS  PubMed  Google Scholar 

  82. Veldhuizen R, Nag K, Orgeig S et al (1998) The role of lipids in pulmonary surfactant. Biochim Biophys Acta 1408:90–108

    Article  CAS  PubMed  Google Scholar 

  83. Svane-Knudsen V, Rasmussen G, Clausen PP (1990) Surfactant-like lamellar bodies in the mucosa of the human nose. Acta Otolaryngol 109:307–313

    Article  CAS  PubMed  Google Scholar 

  84. Schlosser RJ (2006) Surfactant and its role in chronic sinusitis. Ann Otol Rhinol Laryngol Suppl 196:40–44

    Article  PubMed  Google Scholar 

  85. Parra E, Perez-Gil J (2015) Composition, structure and mechanical properties define performance of pulmonary surfactant membranes and films. Chem Phys Lipids 185:153–175

    Article  CAS  PubMed  Google Scholar 

  86. Haagsman HP (1998) Interactions of surfactant protein A with pathogens. Biochim Biophys Acta 1408:264–277

    Article  CAS  PubMed  Google Scholar 

  87. Guagliardo R, Perez-Gil J, De Smedt S et al (2018) Pulmonary surfactant and drug delivery: focusing on the role of surfactant proteins. J Control Release 291:116–126

    Article  CAS  PubMed  Google Scholar 

  88. Goss KL, Kumar AR, Snyder JM (1998) SP-A2 gene expression in human fetal lung airways. Am J Respir Cell Mol Biol 19:613–621

    Article  CAS  PubMed  Google Scholar 

  89. Kim JK, Kim SS, Rha KW et al (2007) Expression and localization of surfactant proteins in human nasal epithelium. Am J Physiol Lung Cell Mol Physiol 292:L879–L884

    Article  CAS  PubMed  Google Scholar 

  90. Gaunsbaek MQ, Kjeldsen AD, Svane-Knudsen V et al (2014) Surfactant proteins A, B, C and D in the human nasal airway: associated with mucosal glands and ciliated epithelium but absent in fluid-phase secretions and mucus. ORL J Otorhinolaryngol Relat Spec 76:288–301

    Article  CAS  PubMed  Google Scholar 

  91. van Eijk M, White MR, Batenburg JJ et al (2004) Interactions of influenza A virus with sialic acids present on porcine surfactant protein D. Am J Respir Cell Mol Biol 30:871–879

    Article  PubMed  Google Scholar 

  92. Mikerov AN, White M, Hartshorn K et al (2008) Inhibition of hemagglutination activity of influenza A viruses by SP-A1 and SP-A2 variants expressed in CHO cells. Med Microbiol Immunol 197:9–12

    Article  CAS  PubMed  Google Scholar 

  93. Benne CA, Kraaijeveld CA, van Strijp JA et al (1995) Interactions of surfactant protein A with influenza A viruses: binding and neutralization. J Infect Dis 171:335–341

    Article  CAS  PubMed  Google Scholar 

  94. van Eijk M, White MR, Crouch EC et al (2003) Porcine pulmonary collectins show distinct interactions with influenza A viruses: role of the N-linked oligosaccharides in the carbohydrate recognition domain. J Immunol 171:1431–1440

    Article  PubMed  Google Scholar 

  95. van Eijk M, Rynkiewicz MJ, Khatri K et al (2018) Lectin-mediated binding and sialoglycans of porcine surfactant protein D synergistically neutralize influenza A virus. J Biol Chem 293:10646–10662

    Article  PubMed  PubMed Central  Google Scholar 

  96. Sriwilaijaroen N, Suzuki Y (2020) Hemagglutinin inhibitors are potential future anti-influenza drugs for mono- and combination therapies. Methods Mol Biol 2132:547–565

    Article  CAS  PubMed  Google Scholar 

  97. Hartshorn KL, White MR, Voelker DR et al (2000) Mechanism of binding of surfactant protein D to influenza A viruses: importance of binding to haemagglutinin to antiviral activity. Biochem J 351(Pt 2):449–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Hartshorn KL, Webby R, White MR et al (2008) Role of viral hemagglutinin glycosylation in anti-influenza activities of recombinant surfactant protein D. Respir Res 9:65

    Article  PubMed  PubMed Central  Google Scholar 

  99. Suzuki Y (2005) Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull 28:399–408

    Article  CAS  PubMed  Google Scholar 

  100. Malhotra R, Haurum JS, Thiel S et al (1994) Binding of human collectins (SP-A and MBP) to influenza virus. Biochem J 304(Pt 2):455–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Al-Qahtani AA, Murugaiah V, Bashir HA et al (2019) Full-length human surfactant protein A inhibits influenza A virus infection of A549 lung epithelial cells: a recombinant form containing neck and lectin domains promotes infectivity. Immunobiology 224:408–418

    Article  CAS  PubMed  Google Scholar 

  102. LeVine AM, Whitsett JA, Hartshorn KL et al (2001) Surfactant protein D enhances clearance of influenza A virus from the lung in vivo. J Immunol 167:5868–5873

    Article  CAS  PubMed  Google Scholar 

  103. Benne CA, Benaissa-Trouw B, van Strijp JA et al (1997) Surfactant protein A, but not surfactant protein D, is an opsonin for influenza A virus phagocytosis by rat alveolar macrophages. Eur J Immunol 27:886–890

    Article  CAS  PubMed  Google Scholar 

  104. Rose MC, Voynow JA (2006) Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev 86:245–278

    Article  CAS  PubMed  Google Scholar 

  105. O’Riordan N, Kane M, Joshi L et al (2014) Structural and functional characteristics of bovine milk protein glycosylation. Glycobiology 24:220–236

    Article  PubMed  Google Scholar 

  106. Parry S, Hanisch FG, Leir SH et al (2006) N-Glycosylation of the MUC1 mucin in epithelial cells and secretions. Glycobiology 16:623–634

    Article  CAS  PubMed  Google Scholar 

  107. Taniguchi T, Woodward AM, Magnelli P et al (2017) N-Glycosylation affects the stability and barrier function of the MUC16 mucin. J Biol Chem 292:11079–11090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Kim J, Lee J, Jang Y et al (2019) N-Glycans of bovine submaxillary mucin contain core-fucosylated and sulfated glycans but not sialylated glycans. Int J Biol Macromol 138:1072–1078

    Article  CAS  PubMed  Google Scholar 

  109. Zanin M, Baviskar P, Webster R et al (2016) The interaction between respiratory pathogens and mucus. Cell Host Microbe 19:159–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Yang X, Steukers L, Forier K et al (2014) A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus. PLoS One 9:e110026

    Article  PubMed  PubMed Central  Google Scholar 

  111. Matrosovich MN, Matrosovich TY, Gray T et al (2004) Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J Virol 78:12665–12667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Cohen M, Zhang XQ, Senaati HP et al (2013) Influenza A penetrates host mucus by cleaving sialic acids with neuraminidase. Virol J 10:321

    Article  PubMed  PubMed Central  Google Scholar 

  113. Barbier D, Garcia-Verdugo I, Pothlichet J et al (2012) Influenza A induces the major secreted airway mucin MUC5AC in a protease-EGFR-extracellular regulated kinase-Sp1-dependent pathway. Am J Respir Cell Mol Biol 47:149–157

    Article  CAS  PubMed  Google Scholar 

  114. Ehre C, Worthington EN, Liesman RM et al (2012) Overexpressing mouse model demonstrates the protective role of Muc5ac in the lungs. Proc Natl Acad Sci U S A 109:16528–16533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Kesimer M, Scull M, Brighton B et al (2009) Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: a possible role in innate defense. FASEB J 23:1858–1868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. McAuley JL, Corcilius L, Tan HX et al (2017) The cell surface mucin MUC1 limits the severity of influenza A virus infection. Mucosal Immunol 10:1581–1593

    Article  CAS  PubMed  Google Scholar 

  117. Verhagen JH, Eriksson P, Leijten L et al (2021) Host range of influenza A virus H1 to H16 in Eurasian ducks based on tissue and receptor binding studies. J Virol 95:e01873-01820

    Article  Google Scholar 

  118. Delaveris CS, Webster ER, Banik SM et al (2020) Membrane-tethered mucin-like polypeptides sterically inhibit binding and slow fusion kinetics of influenza A virus. Proc Natl Acad Sci U S A 117:12643–12650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Short KR, Brooks AG, Reading PC et al (2012) The fate of influenza A virus after infection of human macrophages and dendritic cells. J Gen Virol 93:2315–2325

    Article  CAS  PubMed  Google Scholar 

  120. Ng WC, Liong S, Tate MD et al (2014) The macrophage galactose-type lectin can function as an attachment and entry receptor for influenza virus. J Virol 88:1659–1672

    Article  PubMed  PubMed Central  Google Scholar 

  121. Hillaire ML, Nieuwkoop NJ, Boon AC et al (2013) Binding of DC-SIGN to the hemagglutinin of influenza A viruses supports virus replication in DC-SIGN expressing cells. PLoS One 8:e56164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Ng WC, Londrigan SL, Nasr N et al (2016) The C-type lectin langerin functions as a receptor for attachment and infectious entry of influenza A virus. J Virol 90:206–221

    Article  CAS  PubMed  Google Scholar 

  123. Gillespie L, Roosendahl P, Ng WC et al (2016) Endocytic function is critical for influenza A virus infection via DC-SIGN and L-SIGN. Sci Rep 6:19428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Marvin SA, Russier M, Huerta CT et al (2017) Influenza virus overcomes cellular blocks to productively replicate, impacting macrophage function. J Virol 91:e01417-01416

    Article  Google Scholar 

  125. Sakabe S, Iwatsuki-Horimoto K, Takano R et al (2011) Cytokine production by primary human macrophages infected with highly pathogenic H5N1 or pandemic H1N1 2009 influenza viruses. J Gen Virol 92:1428–1434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Yu WC, Chan RW, Wang J et al (2011) Viral replication and innate host responses in primary human alveolar epithelial cells and alveolar macrophages infected with influenza H5N1 and H1N1 viruses. J Virol 85:6844–6855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. van Riel D, Leijten LM, van der Eerden M et al (2011) Highly pathogenic avian influenza virus H5N1 infects alveolar macrophages without virus production or excessive TNF-alpha induction. PLoS Pathog 7:e1002099

    Article  PubMed  PubMed Central  Google Scholar 

  128. Sun S, Wang Q, Zhao F et al (2011) Glycosylation site alteration in the evolution of influenza A (H1N1) viruses. PLoS One 6:e22844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Cline TD, Karlsson EA, Seufzer BJ et al (2013) The hemagglutinin protein of highly pathogenic H5N1 influenza viruses overcomes an early block in the replication cycle to promote productive replication in macrophages. J Virol 87:1411–1419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Friesenhagen J, Boergeling Y, Hrincius E et al (2012) Highly pathogenic avian influenza viruses inhibit effective immune responses of human blood-derived macrophages. J Leukoc Biol 92:11–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Bender A, Albert M, Reddy A et al (1998) The distinctive features of influenza virus infection of dendritic cells. Immunobiology 198:552–567

    Article  CAS  PubMed  Google Scholar 

  132. Osterlund P, Pirhonen J, Ikonen N et al (2010) Pandemic H1N1 2009 influenza A virus induces weak cytokine responses in human macrophages and dendritic cells and is highly sensitive to the antiviral actions of interferons. J Virol 84:1414–1422

    Article  CAS  PubMed  Google Scholar 

  133. Perrone LA, Plowden JK, Garcia-Sastre A et al (2008) H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4:e1000115

    Article  PubMed  PubMed Central  Google Scholar 

  134. Thitithanyanont A, Engering A, Ekchariyawat P et al (2007) High susceptibility of human dendritic cells to avian influenza H5N1 virus infection and protection by IFN-alpha and TLR ligands. J Immunol 179:5220–5227

    Article  CAS  PubMed  Google Scholar 

  135. Smed-Sorensen A, Chalouni C, Chatterjee B et al (2012) Influenza A virus infection of human primary dendritic cells impairs their ability to cross-present antigen to CD8 T cells. PLoS Pathog 8:e1002572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Cella M, Salio M, Sakakibara Y et al (1999) Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med 189:821–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. van Vliet SJ, van Liempt E, Geijtenbeek TB et al (2006) Differential regulation of C-type lectin expression on tolerogenic dendritic cell subsets. Immunobiology 211:577–585

    Article  PubMed  Google Scholar 

  138. Jegaskanda S, Vanderven HA, Tan HX et al (2019) Influenza virus infection enhances antibody-mediated NK cell functions via type I interferon-dependent pathways. J Virol 93:e02090-02018

    Article  Google Scholar 

  139. Mandelboim O, Lieberman N, Lev M et al (2001) Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409:1055–1060

    Article  CAS  PubMed  Google Scholar 

  140. Arnon TI, Lev M, Katz G et al (2001) Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 31:2680–2689

    Article  CAS  PubMed  Google Scholar 

  141. Ophir Y, Duev-Cohen A, Yamin R et al (2016) PILRalpha binds an unknown receptor expressed primarily on CD56bright and decidual-NK cells and activates NK cell functions. Oncotarget 7:40953–40964

    Article  PubMed  PubMed Central  Google Scholar 

  142. Arnon TI, Achdout H, Lieberman N et al (2004) The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood 103:664–672

    Article  CAS  PubMed  Google Scholar 

  143. Bar-On Y, Glasner A, Meningher T et al (2013) Neuraminidase-mediated, NKp46-dependent immune-evasion mechanism of influenza viruses. Cell Rep 3:1044–1050

    Article  CAS  PubMed  Google Scholar 

  144. Rosenstock P, Bork K, Massa C et al (2020) Sialylation of human natural killer (NK) cells is regulated by IL-2. J Clin Med 9:1816

    Article  CAS  PubMed Central  Google Scholar 

  145. Guo H, Kumar P, Moran TM et al (2009) The functional impairment of natural killer cells during influenza virus infection. Immunol Cell Biol 87:579–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Mao H, Liu Y, Sia SF et al (2017) Avian influenza virus directly infects human natural killer cells and inhibits cell activity. Virol Sin 32:122–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Karakus U, Pohl MO, Stertz S (2020) Breaking the convention: sialoglycan variants, coreceptors, and alternative receptors for influenza A virus entry. J Virol 94:e01357-19

    Article  PubMed  PubMed Central  Google Scholar 

  148. Maruyama J, Nao N, Miyamoto H et al (2016) Characterization of the glycoproteins of bat-derived influenza viruses. Virology 488:43–50

    Article  CAS  PubMed  Google Scholar 

  149. Ciminski K, Ran W, Gorka M et al (2019) Bat influenza viruses transmit among bats but are poorly adapted to non-bat species. Nat Microbiol 4:2298–2309

    Article  PubMed  PubMed Central  Google Scholar 

  150. Fujioka Y, Tsuda M, Nanbo A et al (2013) A Ca2+-dependent signalling circuit regulates influenza A virus internalization and infection. Nat Commun 4:2763

    Article  PubMed  Google Scholar 

  151. Banerjee A, Mossman KL, Miller MS (2020) Bat influenza viruses: making a double agent of MHC class II. Trends Microbiol 28:703–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Peng W, de Vries RP, Grant OC et al (2017) Recent H3N2 viruses have evolved specificity for extended, branched human-type receptors, conferring potential for increased avidity. Cell Host Microbe 21:23–34

    Article  CAS  PubMed  Google Scholar 

  153. Klein A, Carnoy C, Wieruszeski JM et al (1992) The broad diversity of neutral and sialylated oligosaccharides derived from human salivary mucins. Biochemistry 31:6152–6165

    Article  CAS  PubMed  Google Scholar 

  154. Gerken TA, Jentoft N (1987) Structure and dynamics of porcine submaxillary mucin as determined by natural abundance carbon-13 NMR spectroscopy. Biochemistry 26:4689–4699

    Article  CAS  PubMed  Google Scholar 

  155. Stray SJ, Pittman LB (2012) Subtype- and antigenic site-specific differences in biophysical influences on evolution of influenza virus hemagglutinin. Virol J 9:91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. de Vries E, Du W, Guo H et al (2020) Influenza A virus hemagglutinin-neuraminidase-receptor balance: preserving virus motility. Trends Microbiol 28:57–67

    Article  PubMed  Google Scholar 

  157. Lambertz RLO, Pippel J, Gerhauser I et al (2018) Exchange of amino acids in the H1-haemagglutinin to H3 residues is required for efficient influenza A virus replication and pathology in Tmprss2 knock-out mice. J Gen Virol 99:1187–1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Preclinical Sciences, Faculty of Medicine, Thammasat University, Pathumthani, Thailand

    Nongluk Sriwilaijaroen

  2. Department of Medical Biochemistry, School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, Japan

    Nongluk Sriwilaijaroen & Yasuo Suzuki

Authors
  1. Nongluk Sriwilaijaroen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasuo Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nongluk Sriwilaijaroen .

Editor information

Editors and Affiliations

  1. Department of Medical Biochemistry, University of Shizuoka School of Pharmaceutical Sciences, Shizuoka, Japan

    Yasuo Suzuki

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Sriwilaijaroen, N., Suzuki, Y. (2022). Roles of Glycans and Non-glycans on the Epithelium and in the Immune System in H1–H18 Influenza A Virus Infections. In: Suzuki, Y. (eds) Glycovirology. Methods in Molecular Biology, vol 2556. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2635-1_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2635-1_16

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2634-4

  • Online ISBN: 978-1-0716-2635-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation