1887

Abstract

Bovine noroviruses belong to the family , genus . Two genotypes have been described and viruses genetically related to the Jena and Newbury2 strains have been classified into genotypes 1 and 2, respectively. In this study, virus-like particles (VLP) of the previously detected B309 Belgian strain, genetically related to genotype 2 bovine noroviruses, were used to investigate virus–host interactions . B309 VLP were shown to bind to several bovine cell lines. This binding was not affected by heparinase or chondroitinase treatment but was significantly inhibited by both sodium periodate, α-galactosidase, trypsin and phospholipase C treatment. Cell treatment by neuraminidase also moderately affected this binding. Taken together, these results show that, in addition to a galactosyl residue, sialic acid could also be involved in binding to susceptible cells. In addition, both the cholesterol-dependent pathway and macropinocytosis are used for B309 VLP internalization by Madin–Darby bovine kidney cells. The data increase the knowledge on bovine norovirus cell interactions.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.030072-0
2011-06-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/6/1398.html?itemId=/content/journal/jgv/10.1099/vir.0.030072-0&mimeType=html&fmt=ahah

References

  1. Baranowski E. , Ruiz-Jarabo C. M. , Domingo E. . ( 2001; ). Evolution of cell recognition by viruses. . Science 292:, 1102–1105. [CrossRef] [PubMed]
    [Google Scholar]
  2. Bridger J. C. , Hall G. A. , Brown J. F. . ( 1984; ). Characterization of a calici-like virus (Newbury agent) found in association with astrovirus in bovine diarrhea. . Infect Immun 43:, 133–138.[PubMed]
    [Google Scholar]
  3. Cilliers T. , Willey S. , Sullivan W. M. , Patience T. , Pugach P. , Coetzer M. , Papathanasopoulos M. , Moore J. P. , Trkola A. , Clapham P. . ( 2005; ). Use of alternate coreceptors on primary cells by two HIV-1 isolates. . Virology 339:, 136–144. [CrossRef] [PubMed]
    [Google Scholar]
  4. Crawford S. E. , Patel D. G. , Cheng E. , Berkova Z. , Hyser J. M. , Ciarlet M. , Finegold M. J. , Conner M. E. , Estes M. K. . ( 2006; ). Rotavirus viremia and extraintestinal viral infection in the neonatal rat model. . J Virol 80:, 4820–4832. [CrossRef] [PubMed]
    [Google Scholar]
  5. Duizer E. , Schwab K. J. , Neill F. H. , Atmar R. L. , Koopmans M. P. , Estes M. K. . ( 2004; ). Laboratory efforts to cultivate noroviruses. . J Gen Virol 85:, 79–87. [CrossRef] [PubMed]
    [Google Scholar]
  6. Gerondopoulos A. , Jackson T. , Monaghan P. , Doyle N. , Roberts L. O. . ( 2010; ). Murine norovirus-1 cell entry is mediated through a non-clathrin-, non-caveolae-, dynamin- and cholesterol-dependent pathway. . J Gen Virol 91:, 1428–1438. [CrossRef] [PubMed]
    [Google Scholar]
  7. Girao H. , Geli M. I. , Idrissi F. Z. . ( 2008; ). Actin in the endocytic pathway: from yeast to mammals. . FEBS Lett 582:, 2112–2119. [CrossRef] [PubMed]
    [Google Scholar]
  8. Green K. Y. . ( 2007; ). Caliciviridae: The Noroviruses. . In Fields Virology, , 5th edn., pp. 949–979. Edited by Knipe D. M. . . Philadelphia, USA:: Lippinscott Williams & Wilkins;.
    [Google Scholar]
  9. Han M. G. , Smiley J. R. , Thomas C. , Saif L. J. . ( 2004; ). Genetic recombination between two genotypes of genogroup III bovine noroviruses (BoNVs) and capsid sequence diversity among BoNVs and Nebraska-like bovine enteric caliciviruses. . J Clin Microbiol 42:, 5214–5224. [CrossRef] [PubMed]
    [Google Scholar]
  10. Han M. G. , Wang Q. , Smiley J. R. , Chang K. O. , Saif L. J. . ( 2005; ). Self-assembly of the recombinant capsid protein of a bovine norovirus (BoNV) into virus-like particles and evaluation of cross-reactivity of BoNV with human noroviruses. . J Clin Microbiol 43:, 778–785. [CrossRef] [PubMed]
    [Google Scholar]
  11. Harouse J. M. , Laughlin M. A. , Pletcher C. , Friedman H. M. , Gonzalez-Scarano F. . ( 1991; ). Entry of human immunodeficiency virus-1 into glial cells proceeds via an alternate, efficient pathway. . J Leukoc Biol 49:, 605–609.[PubMed]
    [Google Scholar]
  12. Ike A. C. , Roth B. N. , Böhm R. , Pfitzner A. J. , Marschang R. E. . ( 2007; ). Identification of bovine enteric Caliciviruses (BEC) from cattle in Baden-Württemberg. . Dtsch Tierarztl Wochenschr 114:, 12–15.[PubMed]
    [Google Scholar]
  13. Jiang X. , Wang M. , Graham D. Y. , Estes M. K. . ( 1992; ). Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. . J Virol 66:, 6527–6532.[PubMed]
    [Google Scholar]
  14. Jin Q. , Alkhatib B. , Cornetta K. , Alkhatib G. . ( 2010; ). Alternate receptor usage of neuropilin-1 and glucose transporter protein 1 by the human T cell leukemia virus type 1. . Virology 396:, 203–212. [CrossRef] [PubMed]
    [Google Scholar]
  15. Khan A. G. , Pichler J. , Rosemann A. , Blaas D. . ( 2007; ). Human rhinovirus type 54 infection via heparan sulfate is less efficient and strictly dependent on low endosomal pH. . J Virol 81:, 4625–4632. [CrossRef] [PubMed]
    [Google Scholar]
  16. Liu B. L. , Lambden P. R. , Günther H. , Otto P. , Elschner M. , Clarke I. N. . ( 1999; ). Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. . J Virol 73:, 819–825.[PubMed]
    [Google Scholar]
  17. Loret S. , Rusu D. , El Moualij B. , Taminiau B. , Heinen E. , Dandrifosse G. , Mainil J. . ( 2009; ). Preliminary characterization of jejunocyte and colonocyte cell lines isolated by enzymatic digestion from adult and young cattle. . Res Vet Sci 87:, 123–132. [CrossRef] [PubMed]
    [Google Scholar]
  18. Macher B. A. , Galili U. . ( 2008; ). The Galα1,3Galβ1,4GlcNAc-R (α-Gal) epitope: a carbohydrate of unique evolution and clinical relevance. . Biochim Biophys Acta 1780:, 75–88.[PubMed] [CrossRef]
    [Google Scholar]
  19. Makino A. , Shimojima M. , Miyazawa T. , Kato K. , Tohya Y. , Akashi H. . ( 2006; ). Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. . J Virol 80:, 4482–4490. [CrossRef] [PubMed]
    [Google Scholar]
  20. Marsh M. , Helenius A. . ( 2006; ). Virus entry: open sesame. . Cell 124:, 729–740. [CrossRef] [PubMed]
    [Google Scholar]
  21. Mauroy A. , Scipioni A. , Mathijs E. , Miry C. , Ziant D. , Thys C. , Thiry E. . ( 2008; ). Noroviruses and sapoviruses in pigs in Belgium. . Arch Virol 153:, 1927–1931. [CrossRef] [PubMed]
    [Google Scholar]
  22. Mauroy A. , Scipioni A. , Mathijs E. , Saegerman C. , Mast J. , Bridger J. C. , Ziant D. , Thys C. , Thiry E. . ( 2009; a). Epidemiological study of bovine norovirus infection by RT-PCR and a VLP-based antibody ELISA. . Vet Microbiol 137:, 243–251. [CrossRef] [PubMed]
    [Google Scholar]
  23. Mauroy A. , Scipioni A. , Mathijs E. , Thys C. , Thiry E. . ( 2009; b). Molecular detection of kobuviruses and recombinant noroviruses in cattle in continental Europe. . Arch Virol 154:, 1841–1845. [CrossRef] [PubMed]
    [Google Scholar]
  24. Miller N. , Hutt-Fletcher L. M. . ( 1992; ). Epstein–Barr virus enters B cells and epithelial cells by different routes. . J Virol 66:, 3409–3414.[PubMed]
    [Google Scholar]
  25. Milnes A. S. , Binns S. H. , Oliver S. L. , Bridger J. C. . ( 2007; ). Retrospective study of noroviruses in samples of diarrhoea from cattle, using the Veterinary Laboratories Agency’s Farmfile database. . Vet Rec 160:, 326–330. [CrossRef] [PubMed]
    [Google Scholar]
  26. Negrete O. A. , Wolf M. C. , Aguilar H. C. , Enterlein S. , Wang W. , Mühlberger E. , Su S. V. , Bertolotti-Ciarlet A. , Flick R. , Lee B. . ( 2006; ). Two key residues in ephrinB3 are critical for its use as an alternative receptor for Nipah virus. . PLoS Pathog 2:, e7. [CrossRef] [PubMed]
    [Google Scholar]
  27. Nilsson J. , Rydell G. E. , Le Pendu J. , Larson G. . ( 2009; ). Norwalk virus-like particles bind specifically to A, H and difucosylated Lewis but not to B histo-blood group active glycosphingolipids. . Glycoconj J 26:, 1171–1180. [CrossRef] [PubMed]
    [Google Scholar]
  28. Nordgren J. , Kindberg E. , Lindgren P. E. , Matussek A. , Svensson L. . ( 2010; ). Norovirus gastroenteritis outbreak with a secretor-independent susceptibility pattern, Sweden. . Emerg Infect Dis 16:, 81–87. [CrossRef] [PubMed]
    [Google Scholar]
  29. Oliver S. L. , Asobayire E. , Charpilienne A. , Cohen J. , Bridger J. C. . ( 2007; ). Complete genomic characterization and antigenic relatedness of genogroup III, genotype 2 bovine noroviruses. . Arch Virol 152:, 257–272. [CrossRef] [PubMed]
    [Google Scholar]
  30. Ossiboff R. J. , Parker J. S. . ( 2007; ). Identification of regions and residues in feline junctional adhesion molecule required for feline calicivirus binding and infection. . J Virol 81:, 13608–13621. [CrossRef] [PubMed]
    [Google Scholar]
  31. Park S. I. , Jeong C. , Kim H. H. , Park S. H. , Park S. J. , Hyun B. H. , Yang D. K. , Kim S. K. , Kang M. I. , Cho K. O. . ( 2007; ). Molecular epidemiology of bovine noroviruses in South Korea. . Vet Microbiol 124:, 125–133. [CrossRef] [PubMed]
    [Google Scholar]
  32. Perry J. W. , Wobus C. E. . ( 2010; ). Endocytosis of murine norovirus 1 into murine macrophages is dependent on dynamin II and cholesterol. . J Virol 84:, 6163–6176. [CrossRef] [PubMed]
    [Google Scholar]
  33. Perry J. W. , Taube S. , Wobus C. E. . ( 2009; ). Murine norovirus-1 entry into permissive macrophages and dendritic cells is pH-independent. . Virus Res 143:, 125–129. [CrossRef] [PubMed]
    [Google Scholar]
  34. Ruvoën-Clouet N. , Ganière J. P. , André-Fontaine G. , Blanchard D. , Le Pendu J. . ( 2000; ). Binding of rabbit hemorrhagic disease virus to antigens of the ABH histo-blood group family. . J Virol 74:, 11950–11954. [CrossRef] [PubMed]
    [Google Scholar]
  35. Rydell G. E. , Nilsson J. , Rodriguez-Diaz J. , Ruvoën-Clouet N. , Svensson L. , Le Pendu J. , Larson G. . ( 2009; ). Human noroviruses recognize sialyl Lewis x neoglycoprotein. . Glycobiology 19:, 309–320. [CrossRef] [PubMed]
    [Google Scholar]
  36. Scipioni A. , Mauroy A. , Vinjé J. , Thiry E. . ( 2008; ). Animal noroviruses. . Vet J 178:, 32–45. [CrossRef] [PubMed]
    [Google Scholar]
  37. Sieczkarski S. B. , Whittaker G. R. . ( 2002; ). Dissecting virus entry via endocytosis. . J Gen Virol 83:, 1535–1545.[PubMed]
    [Google Scholar]
  38. Smith A. E. , Helenius A. . ( 2004; ). How viruses enter animal cells. . Science 304:, 237–242. [CrossRef] [PubMed]
    [Google Scholar]
  39. Stuart A. D. , Brown T. D. . ( 2006; ). Entry of feline calicivirus is dependent on clathrin-mediated endocytosis and acidification in endosomes. . J Virol 80:, 7500–7509. [CrossRef] [PubMed]
    [Google Scholar]
  40. Stuart A. D. , Brown T. D. . ( 2007; ). α2,6-linked sialic acid acts as a receptor for Feline calicivirus. . J Gen Virol 88:, 177–186. [CrossRef] [PubMed]
    [Google Scholar]
  41. Tamura M. , Natori K. , Kobayashi M. , Miyamura T. , Takeda N. . ( 2004; ). Genogroup II noroviruses efficiently bind to heparan sulfate proteoglycan associated with the cellular membrane. . J Virol 78:, 3817–3826. [CrossRef] [PubMed]
    [Google Scholar]
  42. Tan M. , Jiang X. . ( 2005; ). Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. . Trends Microbiol 13:, 285–293. [CrossRef] [PubMed]
    [Google Scholar]
  43. Tan M. , Huang P. , Meller J. , Zhong W. , Farkas T. , Jiang X. . ( 2003; ). Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket. . J Virol 77:, 12562–12571. [CrossRef] [PubMed]
    [Google Scholar]
  44. Taube S. , Perry J. W. , Yetming K. , Patel S. P. , Auble H. , Shu L. , Nawar H. F. , Lee C. H. , Connell T. D. et al. ( 2009; ). Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. . J Virol 83:, 4092–4101. [CrossRef] [PubMed]
    [Google Scholar]
  45. van der Poel W. H. , van der Heide R. , Verschoor F. , Gelderblom H. , Vinjé J. , Koopmans M. P. . ( 2003; ). Epidemiology of Norwalk-like virus infections in cattle in The Netherlands. . Vet Microbiol 92:, 297–309. [CrossRef] [PubMed]
    [Google Scholar]
  46. Vanderplasschen A. , Bublot M. , Dubuisson J. , Pastoret P. P. , Thiry E. . ( 1993; ). Attachment of the gammaherpesvirus bovine herpesvirus 4 is mediated by the interaction of gp8 glycoprotein with heparinlike moieties on the cell surface. . Virology 196:, 232–240. [CrossRef] [PubMed]
    [Google Scholar]
  47. Villanueva R. A. , Rouillé Y. , Dubuisson J. . ( 2005; ). Interactions between virus proteins and host cell membranes during the viral life cycle. . Int Rev Cytol 245:, 171–244. [CrossRef] [PubMed]
    [Google Scholar]
  48. Wise A. G. , Monroe S. S. , Hanson L. E. , Grooms D. L. , Sockett D. , Maes R. K. . ( 2004; ). Molecular characterization of noroviruses detected in diarrheic stools of Michigan and Wisconsin dairy calves: circulation of two distinct subgroups. . Virus Res 100:, 165–177. [CrossRef] [PubMed]
    [Google Scholar]
  49. Woode G. N. , Bridger J. C. . ( 1978; ). Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. . J Med Microbiol 11:, 441–452. [CrossRef] [PubMed]
    [Google Scholar]
  50. Yanagi Y. , Takeda M. , Ohno S. , Hashiguchi T. . ( 2009; ). Measles virus receptors. . Curr Top Microbiol Immunol 329:, 13–30. [CrossRef] [PubMed]
    [Google Scholar]
  51. Zakhour M. , Ruvoën-Clouet N. , Charpilienne A. , Langpap B. , Poncet D. , Peters T. , Bovin N. , Le Pendu J. . ( 2009; ). The αGal epitope of the histo-blood group antigen family is a ligand for bovine norovirus Newbury2 expected to prevent cross-species transmission. . PLoS Pathog 5:, e1000504. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.030072-0
Loading
/content/journal/jgv/10.1099/vir.0.030072-0
Loading

Data & Media loading...

Supplements

vol. , part 6, pp. 1398 - 1409

[Single PDF file](584 KB)



PDF

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error