1887

Abstract

Rabbit haemorrhagic disease, caused by rabbit hemorrhagic disease virus (RHDV), results in the death of millions of adult rabbits worldwide, with a mortality rate that exceeds 90 %. The sole capsid protein, VP60, is divided into shell (S) and protruding (P) domains, and the more exposed P domain likely contains determinants for cell attachment and antigenic diversity. Nine mAbs against VP60 were screened and identified. To map antigenic epitopes, a set of partially overlapping and consecutive truncated proteins spanning VP60 were expressed. The minimal determinants of the linear B-cell epitopes of VP60 in the P domain, NPISQV, DMSFV and KSTLVFNL, were recognized by one (5H3), four (1B8, 3D11, 4C2 and 4G2) and four mAbs (1D4, 3F7, 5G2 and 6B2), respectively. Sequence alignment showed epitope DMSFV was conserved among all RHDV isolates. Epitopes NPISQV and KSTLVFNL were highly conserved among RHDV G1–G6 and variable in RHDV2 strains. Previous studies demonstrated that native viral particles and virus-like particles (VLPs) of RHDV specifically bound to synthetic blood group H type 2 oligosaccharides. We established an oligosaccharide-based assay to analyse the binding of VP60 and epitopes to histo-blood group antigens (HBGAs). Results showed VP60 and its epitopes (aa 326–331 and 338–342) in the P2 subdomain could significantly bind to blood group H type 2. Furthermore, mAbs 1B8 and 5H3 could block RHDV VLP binding to synthetic H type 2. Collectively, these two epitopes might play a key role in the antigenic structure of VP60 and interaction of RHDV and HBGA.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000355
2016-02-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/2/356.html?itemId=/content/journal/jgv/10.1099/jgv.0.000355&mimeType=html&fmt=ahah

References

  1. Abrantes J., van der Loo W., Le Pendu J., Esteves P. J.. 2012; Rabbit haemorrhagic disease (RHD) and rabbit haemorrhagic disease virus (RHDV): a review. Vet Res43:12 [CrossRef][PubMed]
    [Google Scholar]
  2. Bárcena J., Verdaguer N., Roca R., Morales M., Angulo I., Risco C., Carrascosa J. L., Torres J. M., Castón J. R.. 2004; The coat protein of Rabbit hemorrhagic disease virus contains a molecular switch at the N-terminal region facing the inner surface of the capsid. Virology322:118–134 [CrossRef][PubMed]
    [Google Scholar]
  3. Capucci L., Frigoli G., Rønshold L., Lavazza A., Brocchi E., Rossi C.. 1995; Antigenicity of the rabbit hemorrhagic disease virus studied by its reactivity with monoclonal antibodies. Virus Res37:221–238 [CrossRef][PubMed]
    [Google Scholar]
  4. Capucci L., Fallacara F., Grazioli S., Lavazza A., Pacciarini M. L., Brocchi E.. 1998; A further step in the evolution of rabbit hemorrhagic disease virus: the appearance of the first consistent antigenic variant. Virus Res58:115–126 [CrossRef][PubMed]
    [Google Scholar]
  5. Castañón S., Marín M. S., Martín-Alonso J. M., Boga J. A., Casais R., Humara J. M., Ordás R. J., Parra F.. 1999; Immunization with potato plants expressing VP60 protein protects against rabbit hemorrhagic disease virus. J Virol73:4452–4455[PubMed]
    [Google Scholar]
  6. Chaithirayanon K., Wanichanon C., Vichasri-Grams S., Ardseungneon P., Grams R., Viyanant V., Upatham E. S., Sobhon P.. 2002; Production and characterization of a monoclonal antibody against 28.5 kDa tegument antigen of Fasciola gigantica. Acta Trop84:1–8 [CrossRef][PubMed]
    [Google Scholar]
  7. Chakravarty S., Hutson A. M., Estes M. K., Prasad B. V.. 2005; Evolutionary trace residues in noroviruses: importance in receptor binding, antigenicity, virion assembly, and strain diversity. J Virol79:554–568 [CrossRef][PubMed]
    [Google Scholar]
  8. Chen M., Song Y., Fan Z., Jiang P., Hu B., Xue J., Wei H., Wang F.. 2014; Immunogenicity of different recombinant rabbit hemorrhagic disease virus-like particles carrying CD8+T cell epitope from chicken ovalbumin (OVA). Virus Res183:15–22 [CrossRef][PubMed]
    [Google Scholar]
  9. Dalton K. P., Nicieza I., Balseiro A., Muguerza M. A., Rosell J. M., Casais R., Álvarez A. L., Parra F.. 2012; Variant rabbit hemorrhagic disease virus in young rabbits, Spain. Emerg Infect Dis18:2009–2012 [CrossRef][PubMed]
    [Google Scholar]
  10. Debbink K., Donaldson E. F., Lindesmith L. C., Baric R. S.. 2012; Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J Virol86:1214–1226 [CrossRef][PubMed]
    [Google Scholar]
  11. Farkas T., Cross R. W., Hargitt E. III, Lerche N. W., Morrow A. L., Sestak K.. 2010; Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. J Virol84:8617–8625 [CrossRef][PubMed]
    [Google Scholar]
  12. Ferreira P. G., Costa-E-Silva A., Oliveira M. J., Monteiro E., Aguas A. P.. 2005; Leukocyte-hepatocyte interaction in calicivirus infection: differences between rabbits that are resistant or susceptible to rabbit haemorrhagic disease (RHD). Vet Immunol Immunopathol103:217–221 [CrossRef][PubMed]
    [Google Scholar]
  13. Khawsuk W., Soonklang N., Grams R., Vichasri-Grams S., Wanichanon C., Meepool A., Chaithirayanon K., Ardseungneon P., Viyanant V., other authors. 2002; Production and characterization of a monoclonal antibody against recombinant glutathione S-transferase (GST) of Fasciola gigantica. Asian Pac J Allergy Immunol20:257–266[PubMed]
    [Google Scholar]
  14. Kinnear M., Linde C. C.. 2010; Capsid gene divergence in rabbit hemorrhagic disease virus. J Gen Virol91:174–181 [CrossRef][PubMed]
    [Google Scholar]
  15. König M., Thiel H. J., Meyers G.. 1998; Detection of viral proteins after infection of cultured hepatocytes with rabbit hemorrhagic disease virus. J Virol72:4492–4497[PubMed]
    [Google Scholar]
  16. Laurent S., Vautherot J. F., Madelaine M. F., Le Gall G., Rasschaert D.. 1994; Recombinant rabbit hemorrhagic disease virus capsid protein expressed in baculovirus self-assembles into viruslike particles and induces protection. J Virol68:6794–6798[PubMed]
    [Google Scholar]
  17. Laurent S., Vautherot J. F., Le Gall G., Madelaine M. F., Rasschaert D.. 1997; Structural, antigenic and immunogenic relationships between European brown hare syndrome virus and rabbit haemorrhagic disease virus. J Gen Virol78:2803–2811 [CrossRef][PubMed]
    [Google Scholar]
  18. Laurent S., Kut E., Remy-Delaunay S., Rasschaert D.. 2002; Folding of the rabbit hemorrhagic disease virus capsid protein and delineation of N-terminal domains dispensable for assembly. Arch Virol147:1559–1571 [CrossRef][PubMed]
    [Google Scholar]
  19. Le Gall G., Arnauld C., Boilletot E., Morisse J. P., Rasschaert D.. 1998; Molecular epidemiology of rabbit haemorrhagic disease virus outbreaks in France during 1988 to 1995. J Gen Virol79:11–16 [CrossRef][PubMed]
    [Google Scholar]
  20. Le Gall-Reculé G., Zwingelstein F., Laurent S., de Boisséson C., Portejoie Y., Rasschaert D.. 2003; Phylogenetic analysis of rabbit haemorrhagic disease virus in France between 1993 and 2000, and the characterisation of RHDV antigenic variants. Arch Virol148:65–81 [CrossRef][PubMed]
    [Google Scholar]
  21. Le Gall-Reculé G., Lavazza A., Marchandeau S., Bertagnoli S., Zwingelstein F., Cavadini P., Martinelli N., Lombardi G., Guérin J. L., other authors. 2013; Emergence of a new lagovirus related to rabbit haemorrhagic disease virus. Vet Res44:81 [CrossRef][PubMed]
    [Google Scholar]
  22. Leuthold M. M., Dalton K. P., Hansman G. S.. 2015; Structural analysis of a rabbit hemorrhagic disease virus binding to histo-blood group antigens. J Virol89:2378–2387 [CrossRef][PubMed]
    [Google Scholar]
  23. Martínez-Torrecuadrada J. L., Cortés E., Vela C., Langeveld J. P., Meloen R. H., Dalsgaard K., Hamilton W. D., Casal J. I.. 1998; Antigenic structure of the capsid protein of rabbit haemorrhagic disease virus. J Gen Virol79:1901–1909 [CrossRef][PubMed]
    [Google Scholar]
  24. Meyers G., Wirblich C., Thiel H. J.. 1991a; Genomic and subgenomic RNAs of rabbit hemorrhagic disease virus are both protein-linked and packaged into particles. Virology184:677–686 [CrossRef][PubMed]
    [Google Scholar]
  25. Meyers G., Wirblich C., Thiel H. J.. 1991b; Rabbit hemorrhagic disease virus—molecular cloning and nucleotide sequencing of a calicivirus genome. Virology184:664–676 [CrossRef][PubMed]
    [Google Scholar]
  26. Meyers G., Wirblich C., Thiel H. J., Thumfart J. O.. 2000; Rabbit hemorrhagic disease virus: genome organization and polyprotein processing of a calicivirus studied after transient expression of cDNA constructs. Virology276:349–363 [CrossRef][PubMed]
    [Google Scholar]
  27. Nyström K., Le Gall-Reculé G., Grassi P., Abrantes J., Ruvoën-Clouet N., Le Moullac-Vaidye B., Lopes A. M., Esteves P. J., Strive T., other authors. 2011; Histo-blood group antigens act as attachment factors of rabbit hemorrhagic disease virus infection in a virus strain-dependent manner. PLoS Pathog7:e1002188 [CrossRef][PubMed]
    [Google Scholar]
  28. Parra F., Prieto M.. 1990; Purification and characterization of a calicivirus as the causative agent of a lethal hemorrhagic disease in rabbits. J Virol64:4013–4015[PubMed]
    [Google Scholar]
  29. Puggioni G., Cavadini P., Maestrale C., Scivoli R., Botti G., Ligios C., Le Gall-Reculé G., Lavazza A., Capucci L.. 2013; The new French 2010 rabbit hemorrhagic disease virus causes an RHD-like disease in the Sardinian Cape hare (Lepus capensis mediterraneus). Vet Res44:96 [CrossRef][PubMed]
    [Google Scholar]
  30. Rohayem J., Bergmann M., Gebhardt J., Gould E., Tucker P., Mattevi A., Unge T., Hilgenfeld R., Neyts J.. 2010; Antiviral strategies to control calicivirus infections. Antiviral Res87:162–178 [CrossRef][PubMed]
    [Google Scholar]
  31. 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 Virol74:11950–11954 [CrossRef][PubMed]
    [Google Scholar]
  32. Song Y., Zhou Y., Li Y., Wang X., Bai J., Cao J., Jiang P.. 2012; Identification of B-cell epitopes in the NSP1 protein of porcine reproductive and respiratory syndrome virus. Vet Microbiol155:220–229 [CrossRef][PubMed]
    [Google Scholar]
  33. Thiel H. J., König M.. 1999; Caliciviruses: an overview. Vet Microbiol69:55–62 [CrossRef][PubMed]
    [Google Scholar]
  34. Uusi-Kerttula H., Tamminen K., Malm M., Vesikari T., Blazevic V.. 2014; Comparison of human saliva and synthetic histo-blood group antigens usage as ligands in norovirus-like particle binding and blocking assays. Microbes Infect16:472–480 [CrossRef][PubMed]
    [Google Scholar]
  35. Wang X., Hao H., Qiu L., Dang R., Du E., Zhang S., Yang Z.. 2012; Phylogenetic analysis of rabbit hemorrhagic disease virus in China and the antigenic variation of new strains. Arch Virol157:1523–1530 [CrossRef][PubMed]
    [Google Scholar]
  36. Wang X., Xu F., Liu J., Gao B., Liu Y., Zhai Y., Ma J., Zhang K., Baker T. S., other authors. 2013; Atomic model of rabbit hemorrhagic disease virus by cryo-electron microscopy and crystallography. PLoS Pathog9:e1003132 [CrossRef][PubMed]
    [Google Scholar]
  37. Xu Z. J., Chen W. X.. 1989; Viral haemorrhagic disease in rabbits: a review. Vet Res Commun13:205–212 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000355
Loading
/content/journal/jgv/10.1099/jgv.0.000355
Loading

Data & Media loading...

Supplements

Supplementary Data

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