1887

Abstract

Swine vesicular disease virus (SVDV) evolved from coxsackie B virus serotype 5 (CVB5) in the recent past, crossing the species barrier from humans to pigs. Here, SVDV isolates from early and recent outbreaks have been compared for their capacity to utilize the progenitor virus receptors coxsackie–adenovirus receptor (CAR) and decay-accelerating factor (DAF; CD55). Virus titre of CVB5 and SVDV isolates It′66 and UK′72 on human HeLa cells was reduced by pre-incubation with either anti-DAF or anti-CAR antibodies; however, recent SVDV isolates R1072, R1120 and SPA′93 did not infect HeLa cells lytically. CVB5 and SVDV infection of the pig cell line IB-RS-2 was inhibited completely by anti-CAR antibodies for all isolates, and no reduction was observed following pre-incubation of cells with anti-pig DAF antibodies. Expression of human DAF in the pig cell line IB-RS-2 enhanced the virus titre of early SVDV isolates by 25-fold, but had no effect on recent SVDV isolate titre. Binding of radiolabelled CVB5 to IB-RS-2 cells was increased seven- to eightfold by expression of human DAF and binding of early SVDV isolates was increased 1·2–1·3-fold, whereas no increase in binding by recent SVDV isolates was mediated by human DAF expression. Addition of soluble hDAF-Fc inhibited CVB5, but not SVDV, infection of pig cells. Pre-incubation of all viruses with soluble hCAR-Fc blocked infection of IB-RS-2 pig cells completely; titration of the amount of soluble hCAR-Fc required to block infection revealed that early isolate UK′72 was the least susceptible to inhibition, and the most recent isolate, SPA′93, was the most susceptible.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80669-0
2005-05-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/5/vir861369.html?itemId=/content/journal/jgv/10.1099/vir.0.80669-0&mimeType=html&fmt=ahah

References

  1. Bergelson, J. M., Chan, M., Solomon, K. R., St John, N. F., Lin, H. & Finberg, R. W. ( 1994; ). Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc Natl Acad Sci U S A 91, 6245–6248.[CrossRef]
    [Google Scholar]
  2. Bergelson, J. M., Mohanty, J. G., Crowell, R. L., St John, N. F., Lublin, D. M. & Finberg, R. W. ( 1995; ). Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55). J Virol 69, 1903–1906.
    [Google Scholar]
  3. Bergelson, J. M., Modlin, J. F., Wieland-Alter, W., Cunningham, J. A., Crowell, R. L. & Finberg, R. W. ( 1997; ). Clinical coxsackievirus B isolates differ from laboratory strains in their interaction with two cell surface receptors. J Infect Dis 175, 697–700.[CrossRef]
    [Google Scholar]
  4. Borrego, B., Carra, E., García-Ranea, J. A. & Brocchi, E. ( 2002; ). Characterization of neutralization sites on the circulating variant of swine vesicular disease virus (SVDV): a new site is shared by SVDV and the related coxsackie B5 virus. J Gen Virol 83, 35–44.
    [Google Scholar]
  5. Brocchi, E., Zhang, G., Knowles, N. J., Wilsden, G., McCauley, J. W., Marquardt, O., Ohlinger, V. F. & De Simone, F. ( 1997; ). Molecular epidemiology of recent outbreaks of swine vesicular disease: two genetically and antigenically distinct variants in Europe, 1987-94. Epidemiol Infect 118, 51–61.[CrossRef]
    [Google Scholar]
  6. Brown, F., Talbot, P. & Burrows, R. ( 1973; ). Antigenic differences between isolates of swine vesicular disease virus and their relationship to coxsackie B5 virus. Nature 245, 315–316.[CrossRef]
    [Google Scholar]
  7. Clarkson, N. A., Kaufman, R., Lublin, D. M., Ward, T., Pipkin, P. A., Minor, P. D., Evans, D. J. & Almond, J. W. ( 1995; ). Characterization of the echovirus 7 receptor: domains of CD55 critical for virus binding. J Virol 69, 5497–5501.
    [Google Scholar]
  8. de Castro, M. P. ( 1964; ). Behaviour of the foot-and-mouth disease virus in cell cultures: susceptibility of the IB-RS-2 cell line. Arq Inst Biol Sao Paulo 31, 63–78.
    [Google Scholar]
  9. Dekker, A., Moonen, P., de Boer-Luijtze, E. A. & Terpstra, C. ( 1995; ). Pathogenesis of swine vesicular disease after exposure of pigs to an infected environment. Vet Microbiol 45, 243–250.[CrossRef]
    [Google Scholar]
  10. Escribano-Romero, E., Jimenez-Clavero, M. A. & Ley, V. ( 2000; ). Swine vesicular disease virus. Pathology of the disease and molecular characteristics of the virion. Anim Health Res Rev 1, 119–126.[CrossRef]
    [Google Scholar]
  11. Escribano-Romero, E., Jimenez-Clavero, M. A., Gomes, P., García-Ranea, J. A. & Ley, V. ( 2004; ). Heparan sulphate mediates swine vesicular disease virus attachment to the host cell. J Gen Virol 85, 653–663.[CrossRef]
    [Google Scholar]
  12. Espuña, E., Alemany, R., Riera, P., Artigas, C., Rosell, R., Pujols, J., Sanmartín, J. & San Gabriel, A. ( 1993; ). Aislamiento del virus de la enfermedad vesicular porcina en España. Med Vet 10, 657–662 (in Spanish).
    [Google Scholar]
  13. Fry, E. E., Knowles, N. J., Newman, J. W. I., Wilsden, G., Rao, Z., King, A. M. Q. & Stuart, D. I. ( 2003; ). Crystal structure of swine vesicular disease virus and implications for host adaptation. J Virol 77, 5475–5486.[CrossRef]
    [Google Scholar]
  14. Graves, J. H. ( 1973; ). Serological relationship of swine vesicular disease virus and coxsackie B5 virus. Nature 245, 314–315.[CrossRef]
    [Google Scholar]
  15. Harris, C. L., Spiller, O. B. & Morgan, B. P. ( 2000; ). Human and rodent decay-accelerating factors (CD55) are not species restricted in their complement-inhibiting activities. Immunology 100, 462–470.[CrossRef]
    [Google Scholar]
  16. He, Y., Chipman, P. R., Howitt, J. & 7 other authors ( 2001; ). Interaction of coxsackievirus B3 with the full length coxsackievirus-adenovirus receptor. Nat Struct Biol 8, 874–878.[CrossRef]
    [Google Scholar]
  17. He, Y., Lin, F., Chipman, P. R., Bator, C. M., Baker, T. S., Shoham, M., Kuhn, R. J., Medof, M. E. & Rossmann, M. G. ( 2002; ). Structure of decay-accelerating factor bound to echovirus 7: a virus-receptor complex. Proc Natl Acad Sci U S A 99, 10325–10329.[CrossRef]
    [Google Scholar]
  18. Inoue, T., Yamaguchi, S., Kanno, T., Sugita, S. & Saeki, T. ( 1993; ). The complete nucleotide sequence of a pathogenic swine vesicular disease virus isolated in Japan (J1′73) and phylogenetic analysis. Nucleic Acids Res 21, 3896.[CrossRef]
    [Google Scholar]
  19. Jiménez-Clavero, M. A., Escribano-Romero, E., Sánchez-Vizcaíno, J. M. & Ley, V. ( 1998; ). Molecular cloning, expression and immunological analysis of the capsid precursor polypeptide (P1) from swine vesicular disease virus. Virus Res 57, 163–170.[CrossRef]
    [Google Scholar]
  20. Karnauchow, T. M., Tolson, D. L., Harrison, B. A., Altman, E., Lublin, D. M. & Dimock, K. ( 1996; ). The HeLa cell receptor for enterovirus 70 is decay-accelerating factor (CD55). J Virol 70, 5143–5152.
    [Google Scholar]
  21. Karnauchow, T. M., Dawe, S., Lublin, D. M. & Dimock, K. ( 1998; ). Short consensus repeat domain 1 of decay-accelerating factor is required for enterovirus 70 binding. J Virol 72, 9380–9383.
    [Google Scholar]
  22. Knowles, N. J. & McCauley, J. W. ( 1997; ). Coxsackievirus B5 and the relationship to swine vesicular disease virus. Curr Top Microbiol Immunol 223, 153–167.
    [Google Scholar]
  23. Martino, T. A., Petric, M., Weingartl, H. & 9 other authors ( 2000; ). The coxsackie-adenovirus receptor (CAR) is used by reference strains and clinical isolates representing all six serotypes of coxsackievirus group B and by swine vesicular disease virus. Virology 271, 99–108.[CrossRef]
    [Google Scholar]
  24. Nardelli, L., Lodetti, E., Gualandi, G. L., Burrows, R., Goodridge, D., Brown, F. & Cartwright, B. ( 1968; ). A foot and mouth disease syndrome in pigs caused by an enterovirus. Nature 219, 1275–1276.[CrossRef]
    [Google Scholar]
  25. Pérez de la Lastra, J. M., Harris, C. L., Hinchliffe, S. J., Holt, D. S., Rushmere, N. K. & Morgan, B. P. ( 2000; ). Pigs express multiple forms of decay-accelerating factor (CD55), all of which contain only three short consensus repeats. J Immunol 165, 2563–2573.[CrossRef]
    [Google Scholar]
  26. Seechurn, P., Knowles, N. J. & McCauley, J. W. ( 1990; ). The complete nucleotide sequence of a pathogenic swine vesicular disease virus. Virus Res 16, 255–274.[CrossRef]
    [Google Scholar]
  27. Shafren, D. R., Bates, R. C., Agrez, M. V., Herd, R. L., Burns, G. F. & Barry, R. D. ( 1995; ). Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J Virol 69, 3873–3877.
    [Google Scholar]
  28. Shafren, D. R., Dorahy, D. J., Ingham, R. A., Burns, G. F. & Barry, R. D. ( 1997; ). Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. J Virol 71, 4736–4743.
    [Google Scholar]
  29. Spiller, O. B., Goodfellow, I. G., Evans, D. J., Almond, J. W. & Morgan, B. P. ( 2000; ). Echoviruses and coxsackie B viruses that use human decay-accelerating factor (DAF) as a receptor do not bind the rodent analogues of DAF. J Infect Dis 181, 340–343.[CrossRef]
    [Google Scholar]
  30. Spiller, O. B., Goodfellow, I. G., Evans, D. J., Hinchliffe, S. J. & Morgan, B. P. ( 2002; ). Coxsackie B viruses that use human DAF as a receptor infect pig cells via pig CAR and do not use pig DAF. J Gen Virol 83, 45–52.
    [Google Scholar]
  31. Stuart, A. D., McKee, T. A., Williams, P. A., Harley, C., Shen, S., Stuart, D. I., Brown, T. D. K. & Lea, S. M. ( 2002; ). Determination of the structure of a decay accelerating factor-binding clinical isolate of echovirus 11 allows mapping of mutants with altered receptor requirements for infection. J Virol 76, 7694–7704.[CrossRef]
    [Google Scholar]
  32. Verdaguer, N., Jimenez-Clavero, M. A., Fita, I. & Ley, V. ( 2003; ). Structure of swine vesicular disease virus: mapping of changes occurring during adaptation of human coxsackie B5 virus to infect swine. J Virol 77, 9780–9789.[CrossRef]
    [Google Scholar]
  33. Ward, T., Pipkin, P. A., Clarkson, N. A., Stone, D. M., Minor, P. D. & Almond, J. W. ( 1994; ). Decay-accelerating factor CD55 is identified as the receptor for echovirus 7 using CELICS, a rapid immuno-focal cloning method. EMBO J 13, 5070–5074.
    [Google Scholar]
  34. Yanagawa, B., Spiller, O. B., Choy, J. & 8 other authors ( 2003; ). Coxsackievirus B3-associated myocardial pathology and viral load reduced by recombinant soluble human decay-accelerating factor in mice. Lab Invest 83, 75–85.[CrossRef]
    [Google Scholar]
  35. Yanagawa, B., Spiller, O. B., Proctor, D. G., Choy, J., Luo, H., Zhang, H. M., Suarez, A., Yang, D. & McManus, B. M. ( 2004; ). Soluble recombinant coxsackie and adenovirus receptor abrogates coxsackievirus B3-mediated pancreatitis and myocarditis in mice. J Infect Dis 189, 1431–1439.[CrossRef]
    [Google Scholar]
  36. Zhang, G., Wilsden, G., Knowles, N. J. & McCauley, J. W. ( 1993; ). Complete nucleotide sequence of a coxsackie B5 virus and its relationship to swine vesicular disease virus. J Gen Virol 74, 845–853.[CrossRef]
    [Google Scholar]
  37. Zhang, G., Haydon, D. T., Knowles, N. J. & McCauley, J. W. ( 1999; ). Molecular evolution of swine vesicular disease virus. J Gen Virol 80, 639–651.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80669-0
Loading
/content/journal/jgv/10.1099/vir.0.80669-0
Loading

Data & Media loading...

Most Cited This Month

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