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Journal of General Virology header logo Journal of General Virology

Volume 101, Issue 7

Turkey adenovirus 3, a siadenovirus, uses sialic acid on -linked glycoproteins as a cellular receptor No Access

Abstract

Turkey adenovirus 3 (TAdV-3) is the causative agent of an immune-mediated disease in turkeys, haemorrhagic enteritis, through targeting B lymphocytes. In the present study, we investigated the role of sialic acid in TAdV-3 entry and characterized the structural components of TAdV-3 receptor(s) on RP19, B lymphoblastoid cells. Removal of the cell-surface sialic acids by neuraminidases or blocking of sialic acids by wheat germ agglutinin lectin reduced virus infection. Pre-incubation of cells with lectin or agglutinin resulted in virus reduction, suggesting that TAdV-3 uses both α2,3-linked and α2,6-linked sialic acids as attachment receptor. Virus infectivity data from RP19 cells treated with sodium periodate, proteases (trypsin or bromelain) or metabolic inhibitors (--1-phenyl-2-decanoylamino-3-morpholino-1-propanol, tunicamycin, or benzyl -acetyl-α--galactosaminide) indicated that -linked, but not -linked, carbohydrates are part of the sialylated receptor and they are likely based on a membrane glycoprotein, rather than a glycolipid. Furthermore, our data, in conjunction with previous findings, implies that the secondary receptor for TAdV-3 is a protein molecule since the inhibition of glycolipid biosynthesis did not affect the virus infection, which was rather reduced by protease treatment. We can conclude that terminal sialic acids attached to -linked membrane glycoproteins on B cells are used for virus attachment and are essential for successful virus infection.

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Keyword(s): B lymphocytes , hemorrhagic enteritis , receptor , siadenovirus and turkey adenovirus 3
© 2020 The Authors
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/content/journal/jgv/10.1099/jgv.0.001429
2020-05-26
2025-03-23
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References

  1. Rautenschlein S, Mahsoub HM, Fitzgerald SD, Pierson FW et al. Hemorrhagic Enteritis and Related Infections. In Swayne DE, Boulianne M, Logue CM, McDougald LR, Nair V et al. (editors) Diseases of Poultry. 1, 14 ed. USA: John Wiley & Sons, Inc; 2020 pp 339–347
     [Google Scholar]
  2. Mayo (ICTV Secretary) MA. Virology division news: ICTV at the Paris ICV: results of the plenary session and the binomial ballot. Arch Virol 2002; 147:2254–2260 [View Article]
     [Google Scholar]
  3. Davison A, Harrach B. Siadenovirus. In Tidona C, Darai G. (editors) The Springer Index of Viruses New York: Springer; 2011 pp 49–56
     [Google Scholar]
  4. Cassmann E, Zaffarano B, Chen Q, Li G, Haynes J. Novel siadenovirus infection in a cockatiel with chronic liver disease. Virus Res 2019; 263:164–168 [View Article][PubMed]
     [Google Scholar]
  5. Kovács ER, Benkő M. Complete sequence of raptor adenovirus 1 confirms the characteristic genome organization of siadenoviruses. Infect Genet Evol 2011; 11:1058–1065 [View Article][PubMed]
     [Google Scholar]
  6. Park YM, Kim J-H, Gu SH, Lee SY, Lee M-G et al. Full genome analysis of a novel adenovirus from the South polar skua (Catharacta maccormicki) in Antarctica. Virology 2012; 422:144–150 [View Article][PubMed]
     [Google Scholar]
  7. Joseph HM, Ballmann MZ, Garner MM, Hanley CS, Berlinski R et al. A novel siadenovirus detected in the kidneys and liver of Gouldian finches (Erythura gouldiae). Vet Microbiol 2014; 172:35–43 [View Article][PubMed]
     [Google Scholar]
  8. Lee S-Y, Kim J-H, Park YM, Shin OS, Kim H et al. A novel adenovirus in Chinstrap penguins (Pygoscelis Antarctica) in Antarctica. Viruses 2014; 6:2052–2061 [View Article][PubMed]
     [Google Scholar]
  9. Kleine A, Hafez HM, Lüschow D. Investigations on aviadenoviruses isolated from turkey flocks in Germany. Avian Pathol 2017; 46:181–187 [View Article][PubMed]
     [Google Scholar]
  10. Marek A, Ballmann MZ, Kosiol C, Harrach B, Schlötterer C et al. Whole-Genome sequences of two turkey adenovirus types reveal the existence of two unknown lineages that merit the establishment of novel species within the genus Aviadenovirus. J Gen Virol 2014; 95:156–170 [View Article][PubMed]
     [Google Scholar]
  11. Kaján GL, Stefancsik R, Ursu K, Palya V, Benkő M. The first complete genome sequence of a non-chicken aviadenovirus, proposed to be turkey adenovirus 1. Virus Res 2010; 153:226–233 [View Article][PubMed]
     [Google Scholar]
  12. Nemerow GR. Cell receptors involved in adenovirus entry. Virology 2000; 274:1–4 [View Article][PubMed]
     [Google Scholar]
  13. Zhang Y, Bergelson JM, Receptors A. Adenovirus receptors. J Virol 2005; 79:12125–12131 [View Article][PubMed]
     [Google Scholar]
  14. Wickham TJ, Mathias P, Cheresh DA, Nemerow GR. Integrins αvβ3 and αvβ5 promote adenovirus internalization but not virus attachment. Cell 1993; 73:309–319 [View Article]
     [Google Scholar]
  15. Davison E, Diaz RM, Hart IR, Santis G, Marshall JF. Integrin alpha5beta1-mediated adenovirus infection is enhanced by the integrin-activating antibody TS2/16. J Virol 1997; 71:6204–6207 [View Article][PubMed]
     [Google Scholar]
  16. Salone B, Martina Y, Piersanti S, Cundari E, Cherubini G et al. Integrin α3β1 is an alternative cellular receptor for adenovirus serotype 5. J Virol 2003; 77:13448–13454 [View Article][PubMed]
     [Google Scholar]
  17. Tuve S, Wang H, Jacobs JD, Yumul RC, Smith DF et al. Role of cellular heparan sulfate proteoglycans in infection of human adenovirus serotype 3 and 35. PLoS Pathog 2008; 4:e1000189 [View Article][PubMed]
     [Google Scholar]
  18. Li X, Bangari DS, Sharma A, Mittal SK. Bovine adenovirus serotype 3 utilizes sialic acid as a cellular receptor for virus entry. Virology 2009; 392:162–168 [View Article][PubMed]
     [Google Scholar]
  19. Lenman A, Liaci AM, Liu Y, Årdahl C, Rajan A et al. Human adenovirus 52 uses sialic acid-containing glycoproteins and the Coxsackie and adenovirus receptor for binding to target cells. PLoS Pathog 2015; 11:e1004657 [View Article][PubMed]
     [Google Scholar]
  20. Wu E, Trauger SA, Pache L, Mullen T-M, von Seggern DJ et al. Membrane cofactor protein is a receptor for adenoviruses associated with epidemic keratoconjunctivitis. J Virol 2004; 78:3897–3905 [View Article][PubMed]
     [Google Scholar]
  21. Short JJ, Pereboev AV, Kawakami Y, Vasu C, Holterman MJ et al. Adenovirus serotype 3 utilizes CD80 (B7.1) and CD86 (B7.2) as cellular attachment receptors. Virology 2004; 322:349–359 [View Article][PubMed]
     [Google Scholar]
  22. Wang H, Li Z-Y, Liu Y, Persson J, Beyer I et al. Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nat Med 2011; 17:96–104 [View Article][PubMed]
     [Google Scholar]
  23. Nilsson EC, Storm RJ, Bauer J, Johansson SMC, Lookene A et al. The GD1a glycan is a cellular receptor for adenoviruses causing epidemic keratoconjunctivitis. Nat Med 2011; 17:105–109 [View Article][PubMed]
     [Google Scholar]
  24. Arnberg N. Adenovirus receptors: implications for tropism, treatment and targeting. Rev Med Virol 2009; 19:165–178 [View Article][PubMed]
     [Google Scholar]
  25. Baker AT, Mundy RM, Davies JA, Rizkallah PJ, Parker AL. Human adenovirus type 26 uses sialic acid-bearing glycans as a primary cell entry receptor. Sci Adv 2019; 5:eaax3567 [View Article][PubMed]
     [Google Scholar]
  26. Chandra N, Liu Y, Liu J-X, Frängsmyr L, Wu N et al. Sulfated glycosaminoglycans as viral decoy receptors for human adenovirus type 37. Viruses 2019; 11:247 [View Article][PubMed]
     [Google Scholar]
  27. Chandra N, Frängsmyr L, Imhof S, Caraballo R, Elofsson M et al. Sialic acid-containing glycans as cellular receptors for ocular human adenoviruses: implications for tropism and treatment. Viruses 2019; 11:395 [View Article][PubMed]
     [Google Scholar]
  28. Arnberg N, Edlund K, Kidd AH, Wadell G. Adenovirus type 37 uses sialic acid as a cellular receptor. J Virol 2000; 74:42–48 [View Article][PubMed]
     [Google Scholar]
  29. Stuart AD, Brown TDK. α2,6-Linked sialic acid acts as a receptor for feline calicivirus . J Gen Virol 2007; 88:177–186 [View Article][PubMed]
     [Google Scholar]
  30. Leon RP, Hedlund T, Meech SJ, Li S, Schaack J et al. Adenoviral-mediated gene transfer in lymphocytes. Proc Natl Acad Sci USA 1998; 95:13159–13164 [View Article][PubMed]
     [Google Scholar]
  31. Freimuth P, Philipson L, Carson SD. The coxsackievirus and adenovirus receptor group B coxsackieviruses. In Tracy S, Oberste MS, Drescher KM. (editors) Group B Coxsackieviruses. Current Topics in Microbiology and Immunology 323, 1 ed. Berlin Heidelberg: Springer; 2008 pp 67–87
     [Google Scholar]
  32. Law LK, Davidson BL. What does it take to bind CAR?. Mol Ther 2005; 12:599–609 [View Article][PubMed]
     [Google Scholar]
  33. Richardson C, Brennan P, Powell M, Prince S, Chen Y-H et al. Susceptibility of B lymphocytes to adenovirus type 5 infection is dependent upon both coxsackie-adenovirus receptor and αvβ5 integrin expression. J Gen Virol 2005; 86:1669–1679 [View Article][PubMed]
     [Google Scholar]
  34. Suresh M, Sharma JM. Pathogenesis of type II avian adenovirus infection in turkeys: in vivo immune cell tropism and tissue distribution of the virus. J Virol 1996; 70:30–36 [View Article][PubMed]
     [Google Scholar]
  35. Singh AK, Berbís M Álvaro, Ballmann MZ, Kilcoyne M, Menéndez M et al. Structure and sialyllactose binding of the carboxy-terminal head domain of the fibre from a Siadenovirus, Turkey adenovirus 3. PLoS One 2015; 10:e0139339 [View Article][PubMed]
     [Google Scholar]
  36. Mahsoub HM, Evans NP, Beach NM, Yuan L, Zimmerman K et al. Real-time PCR-based infectivity assay for the titration of turkey hemorrhagic enteritis virus, an adenovirus, in live vaccines. J Virol Methods 2017; 239:42–49 [View Article][PubMed]
     [Google Scholar]
  37. Woodward MP, Young Jr WW, Bloodgood RA. Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. J Immunol Methods 1985; 78:143–153 [View Article][PubMed]
     [Google Scholar]
  38. Stevenson RA, Huang J-A, Studdert MJ, Hartley CA. Sialic acid acts as a receptor for equine rhinitis A virus binding and infection. J Gen Virol 2004; 85:2535–2543 [View Article][PubMed]
     [Google Scholar]
  39. Kovács P, Pintér M, Csaba G. Effect of glucosphingolipid synthesis inhibitor (PPMP and PDMP) treatment on Tetrahymena pyriformis: data on the evolution of the signaling system. Cell Biochem Funct 2000; 18:269–280 [View Article][PubMed]
     [Google Scholar]
  40. Hale LP, Greer PK, Trinh CT, James CL. Proteinase activity and stability of natural bromelain preparations. Int Immunopharmacol 2005; 5:783–793 [View Article][PubMed]
     [Google Scholar]
  41. Di Cera E. Serine proteases. IUBMB Life 2009; 61:510–515 [View Article][PubMed]
     [Google Scholar]
  42. Harvey DJ. Proteomic analysis of glycosylation: structural determination of N- and O-linked glycans by mass spectrometry. Expert Rev Proteomics 2005; 2:87–101 [View Article]
     [Google Scholar]
  43. King IA, Tabiowo A. Effect of tunicamycin on epidermal glycoprotein and glycosaminoglycan synthesis in vitro. Biochem J 1981; 198:331–338 [View Article][PubMed]
     [Google Scholar]
  44. Dugan AS, Eash S, Atwood WJ. An N-linked glycoprotein with alpha(2,3)-linked sialic acid is a receptor for BK virus. J Virol 2005; 79:14442–14445 [View Article][PubMed]
     [Google Scholar]
  45. Brockhausen I, Möller G, Pollex-Krüger A, Rutz V, Paulsen H et al. Control of O-glycan synthesis: specificity and inhibition of O-glycan core 1 UDP-galactose:N-acetylgalactosamine-alpha-R beta 3-galactosyltransferase from rat liver. Biochem Cell Biol 1992; 70:99–108 [View Article][PubMed]
     [Google Scholar]
  46. França M, Stallknecht DE, Howerth EW. Expression and distribution of sialic acid influenza virus receptors in wild birds. Avian Pathol 2013; 42:60–71 [View Article][PubMed]
     [Google Scholar]
  47. Boulanger PA, Houdret N, Scharfman A, Lemay P. The role of surface sialic acid in adenovirus-cell adsorption. J Gen Virol 1972; 16:429–434 [View Article][PubMed]
     [Google Scholar]
  48. Arnberg N, Kidd AH, Edlund K, Olfat F, Wadell G. Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus alpha(v) integrins. J Virol 2000; 74:7691–7693 [View Article][PubMed]
     [Google Scholar]
  49. Mistry N, Inoue H, Jamshidi F, Storm RJ, Oberste MS et al. Coxsackievirus A24 variant uses sialic acid-containing O-linked glycoconjugates as cellular receptors on human ocular cells. J Virol 2011; 85:11283–11290 [View Article][PubMed]
     [Google Scholar]
  50. Ulloa F, Real FX. Differential distribution of sialic acid in alpha2,3 and alpha2,6 linkages in the apical membrane of cultured epithelial cells and tissues. J Histochem Cytochem 2001; 49:501–509 [View Article][PubMed]
     [Google Scholar]
  51. Burmeister WP, Guilligay D, Cusack S, Wadell G, Arnberg N. Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. J Virol 2004; 78:7727–7736 [View Article][PubMed]
     [Google Scholar]
  52. Li Y, Chen X. Sialic acid metabolism and sialyltransferases: natural functions and applications. Appl Microbiol Biotechnol 2012; 94:887–905 [View Article][PubMed]
     [Google Scholar]
  53. Sharma A, Li X, Bangari DS, Mittal SK. Adenovirus receptors and their implications in gene delivery. Virus Res 2009; 143:184–194 [View Article][PubMed]
     [Google Scholar]
  54. Zhu F, Li D, Song D, Xia H, Liu X et al. Precision mapping of N- and O-glycoproteins in viral resistant and susceptible strains of Bombyx mori . J Invertebr Pathol 2019; 167:107250 [View Article][PubMed]
     [Google Scholar]
  55. Liu CK, Wei G, Atwood WJ. Infection of glial cells by the human polyomavirus JC is mediated by an N-linked glycoprotein containing terminal alpha(2-6)-linked sialic acids. J Virol 1998; 72:4643–4649 [View Article][PubMed]
     [Google Scholar]
  56. Sánchez-Felipe L, Villar E, Muñoz-Barroso I. α2-3- and α2-6- N-linked sialic acids allow efficient interaction of Newcastle Disease Virus with target cells. Glycoconj J 2012; 29:539–549 [View Article][PubMed]
     [Google Scholar]
  57. Wu Z, Miller E, Agbandje-McKenna M, Samulski RJ. α2,3 and α2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J Virol 2006; 80:9093–9103 [View Article][PubMed]
     [Google Scholar]
  58. Chen MH, Benjamin T. Roles of N-glycans with α2,6 as well as α2,3 linked sialic acid in infection by polyoma virus. Virology 1997; 233:440–442 [View Article][PubMed]
     [Google Scholar]
  59. Kim D-S, Hosmillo M, Alfajaro MM, Kim J-Y, Park J-G et al. Both α2,3- and α2,6-linked sialic acids on O-linked glycoproteins act as functional receptors for porcine sapovirus. PLoS Pathog 2014; 10:e1004172 [View Article][PubMed]
     [Google Scholar]
  60. Aboezz ZR, Mahsoub HM, El-Bagoury G, Pierson FW. In vitro growth kinetics and gene expression analysis of the turkey adenovirus 3, a siadenovirus. Virus Res 2019; 263:47–54 [View Article][PubMed]
     [Google Scholar]
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Turkey adenovirus 3, a siadenovirus, uses sialic acid on N-linked glycoproteins as a cellular receptor
J. Gen. Virol. 101, 760 (2020); https://doi.org/10.1099/jgv.0.001429
/content/journal/jgv/10.1099/jgv.0.001429
/content/journal/jgv/10.1099/jgv.0.001429
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