Differential effects of bovine viral diarrhoea virus on monocytes and dendritic cells Free

Abstract

Various pathogens have been shown to infect antigen-presenting cells and affect their capacity to interact with and stimulate T-cell responses. We have used an antigenically identical pair of non-cytopathic (ncp) and cytopathic (cp) bovine viral diarrhoea virus (BVDV) isolates to determine how the two biotypes affect monocyte and dendritic cell (DC) function. We have shown that monocytes and DCs are both susceptible to infection with ncp BVDV and cp BVDV . In addition, monocytes infected with ncp BVDV were compromised in their ability to stimulate allogeneic and memory CD4 T cell responses, but DCs were not affected. This was not due to down-regulation of a number of recognized co-stimulatory molecules including CD80, CD86 and CD40. Striking differences in the response of the two cell types to infection with cytopathic virus were seen. Dendritic cells were not susceptible to the cytopathic effect caused by cp BVDV, whereas monocytes were killed. Analysis of interferon (IFN)-/ production showed similar levels in monocytes and DCs exposed to cp BVDV, but none was detected in cells exposed to ncp BVDV. We conclude that the prevention of cell death in DCs is not associated with enhanced production of IFN-/, as proposed for influenza virus, but is by a distinct mechanism.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18964-0
2003-07-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/7/vir841771.html?itemId=/content/journal/jgv/10.1099/vir.0.18964-0&mimeType=html&fmt=ahah

References

  1. Adler B., Adler H., Pfister H., Jungi T. W., Peterhans E. 1997; Macrophages infected with cytopathic bovine viral diarrhoea virus release a factor(s) capable of priming uninfected macrophages for activation-induced apoptosis. J Virol 71:3255–3258
    [Google Scholar]
  2. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y. J., Pulendran B., Palucka K. 2000; Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811
    [Google Scholar]
  3. Bender A., Albert M., Reddy A., Feldman M., Sauter B., Kaplan G., Hellman W., Bhardwaj N. 1998; The distinctive features of influenza virus infection of dendritic cells. Immunobiology 198:552–567
    [Google Scholar]
  4. Bonini C., Lee S. P., Riddell S. R., Greenberg P. D. 2001; Targeting antigen in mature dendritic cells for simultaneous stimulation of CD4+ and CD8+ T cells. J Immunol 166:5250–5257
    [Google Scholar]
  5. Borrow P., Evans C. F., Oldstone M. B. 1995; Virus-induced immunosuppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J Virol 69:1059–1070
    [Google Scholar]
  6. Brooke G. P., Parsons K. R., Howard C. J. 1998; Cloning of two members of the SIRP alpha family of protein tyrosine phosphatase binding proteins in cattle that are expressed on monocytes and a subpopulation of dendritic cells and which mediate binding to CD4 T cells. Eur J Immunol 28:1–11
    [Google Scholar]
  7. Brownlie J., Clarke M. C., Howard C. J. 1984; Experimental production of fatal mucosal disease in cattle. Vet Rec 114:535–536
    [Google Scholar]
  8. Cella M., Salio M. Y., Sakakibara H., Langen I., Julkunen I., Lanzavecchia A. 1999; Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med 189:821–829
    [Google Scholar]
  9. Charleston B., Hope J. C., Carr B. V., Howard C. J. 2001; Masking of two in vitro immunological assays for Mycobacterium bovis (BCG) in calves acutely infected with non-cytopathic bovine viral diarrhoea virus. Vet Rec 149:481–484
    [Google Scholar]
  10. Charleston B., Brackenbury L. S., Carr B. V., Fray M. D., Hope J. C., Howard C. J., Morrison W. I. 2002; Alpha/beta and gamma interferons are induced by infection with noncytopathic bovine viral diarrhea virus in vivo. J Virol 76:923–927
    [Google Scholar]
  11. Collen T., Morrison W. I. 2000; CD4+ T-cell responses to bovine viral diarrhoea virus in cattle. Virus Res 67:67–80
    [Google Scholar]
  12. Edwards S., Moennig V., Wensvoort G. 1991; The development of an international reference panel of monoclonal antibodies for the differentiation of hog cholera virus from other pestiviruses. Vet Microbiol 29:101–108
    [Google Scholar]
  13. Ellis S. A., Staines K. A., Stear M. J., Hensen E. J., Morrison W. I. 1998; DNA typing for BoLA class I using sequence-specific primers (PCR-SSP). Eur J Immunogenet 25:365–370
    [Google Scholar]
  14. Fray M. D., Mann G. E., Clarke M. C., Charleston B. 1999; Bovine viral diarrhea virus: its effects on estradiol, progesterone and prostaglandin secretion in the cow. Theriogenology 51:1533–1546
    [Google Scholar]
  15. Fray M. D., Mann G. E., Charleston B. 2001; Validation of a Mx/CAT reporter gene assay for the quantification of bovine type-I interferon. J Immunol Methods 249:235–244
    [Google Scholar]
  16. Glew E. J., Howard C. J. 2001; Antigen-presenting cells from calves persistently infected with bovine viral diarrhoea virus, a member of the Flaviviridae , are not compromised in their ability to present viral antigen. J Gen Virol 82:1677–1685
    [Google Scholar]
  17. Hamers C., Dehan P., Couvreur B., Letellier C., Kerkhofs P., Pastoret P.-P. 2001; Diversity among bovine pestiviruses. Vet J 161:112–122
    [Google Scholar]
  18. Hoff H. S., Donis R. O. 1997; Induction of apoptosis and cleavage of poly(ADP-ribose) polymerase by cytopathic bovine viral diarrhea virus infection. Virus Res 149:101–113
    [Google Scholar]
  19. Hope J. C., Kwong L. S., Sopp P., Collins R. A., Howard C. J. 2000; Dendritic cells induce CD4+ and CD8+ T-cell responses to Mycobacterium bovis and M . avium antigens in Bacille Calmette Guerin vaccinated and nonvaccinated cattle. Scand J Immunol 52:285–291
    [Google Scholar]
  20. Houe H. 1999; Epidemiological features and economical importance of bovine virus diarrhoea virus (BVDV) infections. Vet Microbiol 64:89–107
    [Google Scholar]
  21. Howard C. J., Sopp P., Brownlie J., Kwong L. S., Parsons K. R., Taylor G. 1997; Identification of two distinct populations of dendritic cells in afferent lymph that vary in their ability to stimulate T cells. J Immunol 159:5372–5382
    [Google Scholar]
  22. Meyers G., Thiel H. J. 1996; Molecular characterization of pestiviruses. Adv Virus Res 47:53–118
    [Google Scholar]
  23. Plotnicky-Gilquin H., Cyblat D., Aubry J. P., Delneste Y., Blaecke A., Bonnefoy J. Y., Corvaia N., Jeannin P. 2001; Differential effects of parainfluenza virus type 3 on human monocytes and dendritic cells. Virology 285:82–90
    [Google Scholar]
  24. Potgieter L. N. D. 1995; Immunology of bovine viral diarrhea virus. Vet Clin North Am 11:501–520
    [Google Scholar]
  25. Renjifo X., Letellier C., Keil G. M. 11 other authors 1999; Susceptibility of bovine antigen-presenting cells to infection by bovine herpesvirus 1 and in vitro presentation to T cells: two independent events. J Virol 73:4840–4846
    [Google Scholar]
  26. Rescigno M., Borrow P. 2001; The host–pathogen interaction: new themes from dendritic cell biology. Cell 106:267–270
    [Google Scholar]
  27. Sarobe P., Lasarte J. J., Casares N., Lopez-Diaz de Cerio A., Baixeras E., Labarga P., Garcia N., Borras-Cuesta F., Prieto J. 2002; Abnormal priming of CD4+ T cells by dendritic cells expressing hepatitis C virus core and E1 proteins. J Virol 76:5062–5070
    [Google Scholar]
  28. Schneider-Schaulies S., Bieback K., Avota E., Klagge I., ter Meulen V. 2002; Regulation of gene expression in lymphocytes and antigen-presenting cells by measles virus: consequences for immunomodulation. J Mol Med 80:73–85
    [Google Scholar]
  29. Servet-Delprat C., Vidalain P. O., Azocar O., Le Deist F., Fischer A., Rabourdin-Combe C. 2000; Consequences of Fas-mediated human dendritic cell apoptosis induced by measles virus. J Virol 74:4387–4393
    [Google Scholar]
  30. Solomon T., Mallewa M. 2001; Dengue and other emerging flaviviruses. J Infect 42:104–115
    [Google Scholar]
  31. Sopp P., Hooper L. B., Clarke M. C., Howard C. J., Brownlie J. 1994; Detection of bovine viral diarrhoea virus p80 protein in subpopulations of bovine leukocytes. J Gen Virol 75:1189–1194
    [Google Scholar]
  32. Teichmann U., Liebler-Tenorio E. M., Pohlenz J. F. 2000; Ultrastructural changes in follicles of small-intestinal aggregated lymphoid nodules in early and advanced phases of experimentally induced mucosal diseases in calves. Am J Vet Res 61:174–182
    [Google Scholar]
  33. Zhang G., Aldridge S., Clarke M. C., McCauley J. W. 1996; Cell death induced by cytopathic bovine viral diarrhoea virus is mediated by apoptosis. J Gen Virol 77:1677–1681
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18964-0
Loading
/content/journal/jgv/10.1099/vir.0.18964-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed