1887

Abstract

Porcine circovirus type 2 (PCV2) is the necessary agent for the occurrence of post-weaning multisystemic wasting syndrome (PMWS) in pigs. It has been suggested that PMWS-affected pigs are immunosuppressed and, therefore, more prone to develop co-infections. In this study, we elucidated that PCV2 downregulates the immune cell functions during recall antigen responses. We showed that PCV2, but not the non-pathogenic porcine circovirus type 1, induces interleukin (IL)-10 secretion by monocytic cells. Notably, PCV2-induced IL-10 led to effective repression of IL-12 in blood peripheral mononuclear cells (PBMCs). Besides alpha and gamma interferon synthesis by PBMCs from pseudorabies virus (PRV)-immunized animals, activated PRV also was repressed by subsequent infection by PCV2. The ability of PCV2 to hamper the development of immune responses may contribute to the Th1 suppressed responses, immune suppression and co-infections.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83354-0
2008-03-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/3/760.html?itemId=/content/journal/jgv/10.1099/vir.0.83354-0&mimeType=html&fmt=ahah

References

  1. Allan, G., Meehan, B., Todd, D., Kennedy, S., McNeilly, F., Ellis, J., Clark, E. G., Harding, J., Espuna, E. & other authors ( 1998; ). Novel porcine circoviruses from pigs with wasting disease syndromes. Vet Rec 142, 467–468.
    [Google Scholar]
  2. Brady, M. T., MacDonald, A. J., Rowan, A. G. & Mills, K. H. ( 2003; ). Hepatitis C virus non-structural protein 4 suppresses Th1 responses by stimulating IL-10 production from monocytes. Eur J Immunol 33, 3448–3457.[CrossRef]
    [Google Scholar]
  3. Brooks, D. G., Trifilo, M. J., Edelmann, K. H., Teyton, L., McGavern, D. B. & Oldstone, M. B. A. ( 2006; ). Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 12, 1301–1309.[CrossRef]
    [Google Scholar]
  4. Cacciarelli, T. V., Martinez, O. M., Gish, R. G., Villanueva, J. C. & Krams, S. M. ( 1996; ). Immunoregulatory cytokines in chronic hepatitis C virus infection: pre- and posttreatment with interferon alfa. Hepatology 24, 6–9.[CrossRef]
    [Google Scholar]
  5. Carrasco, C. P., Rigden, R. C., Schaffner, R., Gerber, H., Neuhaus, V., Inumaru, S., Takamatsu, H., Bertoni, G., McCullough, K. C. & Summerfield, A. ( 2001; ). Porcine dendritic cells generated in vitro: morphological, phenotypic and functional properties. Immunology 104, 175–184.[CrossRef]
    [Google Scholar]
  6. Clerici, M., Balotta, C., Salvaggio, A., Riva, C., Trabattoni, D., Papagno, L., Berlusconi, A., Rusconi, S., Villa, M. L. & other authors ( 1996; ). Human immunodeficiency virus (HIV) phenotype and interleukin-2/interleukin-10 ratio are associated markers of protection and progression in HIV infection. Blood 88, 574–579.
    [Google Scholar]
  7. Darwich, L., Balasch, M., Plana-Duran, J., Segales, J., Domingo, M. & Mateu, E. ( 2003a; ). Cytokine profiles of peripheral blood mononuclear cells from pigs with postweaning multisystemic wasting syndrome in response to mitogen, superantigen or recall viral antigens. J Gen Virol 84, 3453–3457.[CrossRef]
    [Google Scholar]
  8. Darwich, L., Pie, S., Rovira, A., Segales, J., Domingo, M., Oswald, I. P. & Mateu, E. ( 2003b; ). Cytokine mRNA expression profiles in lymphoid tissues of pigs naturally affected by postweaning multisystemic wasting syndrome. J Gen Virol 84, 2117–2125.[CrossRef]
    [Google Scholar]
  9. Darwich, L., Segales, J., Resendes, A., Balasch, M., Plana-Duran, J. & Mateu, E. ( 2008; ). Transient correlation between viremia levels and IL-10 expression in pigs subclinically infected with porcine circovirus type 2 (PCV2). Res Vet Sci 84, 194–198.[CrossRef]
    [Google Scholar]
  10. Dolganiuc, A., Chang, S., Kodys, K., Mandrekar, P., Bakis, G., Cormier, M. & Szabo, G. ( 2006; ). Hepatitis C virus (HCV) core protein-induced, monocyte-mediated mechanisms of reduced IFN-α and plasmacytoid dendritic cell loss in chronic HCV infection. J Immunol 177, 6758–6768.[CrossRef]
    [Google Scholar]
  11. Ellis, J., Clark, E., Haines, D., West, K., Krakowka, S., Kennedy, S. & Allan, G. M. ( 2004; ). Porcine circovirus-2 and concurrent infections in the field. Vet Microbiol 98, 159–163.[CrossRef]
    [Google Scholar]
  12. Guzylack-Piriou, L., Balmelli, C., McCullough, K. C. & Summerfield, A. ( 2004; ). Type-A CpG oligonucleotides activate exclusively porcine natural interferon-producing cells to secrete interferon-α, tumour necrosis factor-α and interleukin-12. Immunology 112, 28–37.[CrossRef]
    [Google Scholar]
  13. Hasslung, F., Wallgren, P., Ladekjaer-Hansen, A. S., Botner, A., Nielsen, J., Wattrang, E., Allan, G. M., McNeilly, F., Ellis, J. & other authors ( 2005; ). Experimental reproduction of postweaning multisystemic wasting syndrome (PMWS) in pigs in Sweden and Denmark with a Swedish isolate of porcine circovirus type 2. Vet Microbiol 106, 49–60.[CrossRef]
    [Google Scholar]
  14. Marin-Serrano, E., Rodriguez-Ramos, C., Diaz, F., Martin-Herrera, L. & Giron-Gonzalez, J. A. ( 2006; ). Modulation of the anti-inflammatory interleukin 10 and of proapoptotic IL-18 in patients with chronic hepatitis C treated with interferon alpha and ribavirin. J Viral Hepat 13, 230–234.[CrossRef]
    [Google Scholar]
  15. McNeilly, F., McNair, I., Mackie, D. P., Meehan, B. M., Kennedy, S., Moffett, D., Ellis, J., Krakowka, S. & Allan, G. M. ( 2001; ). Production, characterisation and applications of monoclonal antibodies to porcine circovirus 2. Arch Virol 146, 909–922.[CrossRef]
    [Google Scholar]
  16. Orsilles, M. A., Pieri, E., Cooke, P. & Caula, C. ( 2006; ). IL-2 and IL-10 serum levels in HIV-1-infected patients with or without active antiretroviral therapy. APMIS 114, 55–60.[CrossRef]
    [Google Scholar]
  17. Rico, M. A., Quiroga, J. A., Subira, D., Castanon, S., Esteban, J. M., Pardo, M. & Carreno, V. ( 2001; ). Hepatitis B virus-specific T-cell proliferation and cytokine secretion in chronic hepatitis B e antibody-positive patients treated with ribavirin and interferon alpha. Hepatology 33, 295–300.[CrossRef]
    [Google Scholar]
  18. Segalés, J., Allan, G. M. & Domingo, M. ( 2005; ). Porcine circovirus diseases. Anim Health Res Rev 6, 119–142.[CrossRef]
    [Google Scholar]
  19. Sipos, W., Duvigneau, J. C., Willheim, M., Schilcher, F., Hartl, R. T., Hofbauer, G., Exel, B., Pietschmann, P. & Schmoll, F. ( 2004; ). Systemic cytokine profile in feeder pigs suffering from natural postweaning multisystemic wasting syndrome (PMWS) as determined by semiquantitative RT-PCR and flow cytometric intracellular cytokine detection. Vet Immunol Immunopathol 99, 63–71.[CrossRef]
    [Google Scholar]
  20. Sipos, W., Duvigneau, J. C., Pietschmann, P., Schilcher, F., Hofbauer, G., Hartl, R. T. & Schmoll, F. ( 2005; ). Porcine dermatitis and nephropathy syndrome (PDNS) is associated with a systemic cytokine expression profile indicative of proinflammation and a Th1 bias. Vet Immunol Immunopathol 107, 303–313.[CrossRef]
    [Google Scholar]
  21. Stevenson, L. S., McCullough, K., Vincent, I., Gilpin, D. F., Summerfield, A., Nielsen, J., McNeilly, F., Adair, B. M. & Allan, G. M. ( 2006; ). Cytokine and C-reactive protein profiles induced by porcine circovirus type 2 experimental infection in 3-week-old piglets. Viral Immunol 19, 189–195.[CrossRef]
    [Google Scholar]
  22. Suzuki, M., Dezzutti, C. S., Okayama, A., Tachibana, N., Tsubouchi, H., Mueller, N. & Lal, R. B. ( 1999; ). Modulation of T-cell responses to a recall antigen in human T-cell leukemia virus type 1-infected individuals. Clin Diagn Lab Immunol 6, 713–717.
    [Google Scholar]
  23. Taga, K., Mostowski, H. & Tosato, G. ( 1993; ). Human interleukin-10 can directly inhibit T-cell growth. Blood 81, 2964–2971.
    [Google Scholar]
  24. Vincent, I. E., Carrasco, C. P., Guzylack-Piriou, L., Herrmann, B., McNeilly, F., Allan, G. M., Summerfield, A. & McCullough, K. C. ( 2005; ). Subset-dependent modulation of dendritic cell activity by circovirus type 2. Immunology 115, 388–398.[CrossRef]
    [Google Scholar]
  25. Vincent, I. E., Balmelli, C., Meehan, B., Allan, G., Summerfield, A. & McCullough, K. C. ( 2007; ). Silencing of natural interferon producing cell activation by porcine circovirus type 2 DNA. Immunology 120, 47–56.
    [Google Scholar]
  26. Yarchoan, R., Guo, H. G., Reitz, M., Jr, Maluish, A., Mitsuya, H. & Broder, S. ( 1986; ). Alterations in cytotoxic and helper T cell function after infection of T cell clones with human T cell leukemia virus, type I. J Clin Invest 77, 1466–1473.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83354-0
Loading
/content/journal/jgv/10.1099/vir.0.83354-0
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