1887

Abstract

(ORFV) is a parapoxvirus that infects sheep, goats and man. In humans, the virus induces acute, pustular skin lesions that can develop into a progressive disease. Humans are susceptible to reinfection with ORFV and rare cases of persistent infection have been reported. ORFV encodes several immunomodulators, including a homologue of interleukin-10 (ORFV IL-10), that may explain these phenomena. The immunosuppressive effects of ORFV IL-10 on immature human dendritic cells (DCs) cultured from blood-derived monocytes (MoDCs) were investigated. MoDCs exposed simultaneously to lipopolysaccharide and ORFV IL-10 showed enhanced ovalbumin–FITC uptake and reduced IL-12 expression, indicating inhibition of maturation. Moreover, ORFV IL-10 inhibited the upregulation of DC cell-surface activation and maturation markers MHC II, CD80, CD83 and CD86 and inhibited the capacity of MoDCs to activate CD4 T cells in an oxidative mitogenesis assay. These findings suggest that ORFV IL-10 may influence the development of acquired immunity in humans by impairing DC function.

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2006-11-01
2024-05-10
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References

  1. Agger W. A., Webster S. B. 1983; Human orf infection complicated by erythema multiforme. Cutis 31:334–338
    [Google Scholar]
  2. Blakemore F., Abdussalam M., Goldsmith W. N. 1948; A case of orf (contagious pustular dermatitis): identification of the virus. Br J Dermatol 60:404–409 [CrossRef]
    [Google Scholar]
  3. Buddle B. M., Pulford H. D. 1984; Effect of passively-acquired antibodies and vaccination on the immune response to contagious ecthyma virus. Vet Microbiol 9:515–522 [CrossRef]
    [Google Scholar]
  4. Chang W. L., Baumgarth N., Yu D., Barry P. A. 2004; Human cytomegalovirus-encoded interleukin-10 homolog inhibits maturation of dendritic cells and alters their functionality. J Virol 78:8720–8731 [CrossRef]
    [Google Scholar]
  5. Copland M. J., Baird M. A., Rades T., McKenzie J. L., Becker B., Reck F., Tyler P. C., Davies N. M. 2003; Liposomal delivery of antigen to human dendritic cells. Vaccine 21:883–890 [CrossRef]
    [Google Scholar]
  6. De Smedt T., Van Mechelen M., De Becker G., Urbain J., Leo O., Moser M. 1997; Effect of interleukin-10 on dendritic cell maturation and function. Eur J Immunol 27:1229–1235 [CrossRef]
    [Google Scholar]
  7. Erickson G. A., Carbrey E. A., Gustafson G. A. 1975; Generalized contagious ecthyma in a sheep rancher: diagnostic considerations. J Am Vet Med Assoc 166:262–263
    [Google Scholar]
  8. Fastier L. B. 1957; Human infections with the virus of ovine contagious pustular dermatitis (scabby mouth). N Z Med J 56:121–123
    [Google Scholar]
  9. Faulkner L., Buchan G., Baird M. 2000; Interleukin-10 does not affect phagocytosis of particulate antigen by bone marrow-derived dendritic cells but does impair antigen presentation. Immunology 99:523–531 [CrossRef]
    [Google Scholar]
  10. Fickenscher H., Hör S., Küpers H., Knappe A., Wittmann S., Sticht H. 2002; The interleukin-10 family of cytokines. Trends Immunol 23:89–96 [CrossRef]
    [Google Scholar]
  11. Fleming S. B., McCaughan C. A., Andrews A. E., Nash A. D., Mercer A. A. 1997; A homolog of interleukin-10 is encoded by the poxvirus orf virus. J Virol 71:4857–4861
    [Google Scholar]
  12. Fleming S. B., Haig D. M., Nettleton P., Reid H. W., McCaughan C. A., Wise L. M., Mercer A. A. 2000; Sequence and functional analysis of a homolog of interleukin-10 encoded by the parapoxvirus orf virus. Virus Genes 21:85–95 [CrossRef]
    [Google Scholar]
  13. Freudenthal P. S., Steinman R. M. 1990; The distinct surface of human blood dendritic cells, as observed after an improved isolation method. Proc Natl Acad Sci U S A 87:7698–7702 [CrossRef]
    [Google Scholar]
  14. Grütz G. 2005; New insights into the molecular mechanism of interleukin-10-mediated immunosupression. J Leukoc Biol 77:3–15
    [Google Scholar]
  15. Gunzer M., Schäfer A., Borgmann S., Grabbe S., Zänker K. S., Bröcker E.-B., Kämpgen E., Friedl P. 2000; Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 13:323–332 [CrossRef]
    [Google Scholar]
  16. Haig D. M., McInnes C. J. 2002; Immunity and counter-immunity during infection with the parapoxvirus orf virus. Virus Res 88:3–16 [CrossRef]
    [Google Scholar]
  17. Haig D. M., Thomson J., McInnes C. J. & 7 other authors 2002; A comparison of the anti-inflammatory and immuno-stimulatory activities of orf virus and ovine interleukin-10. Virus Res 90:303–316 [CrossRef]
    [Google Scholar]
  18. Imlach W., McCaughan C. A., Mercer A. A., Haig D., Fleming S. B. 2002; Orf virus-encoded interleukin-10 stimulates the proliferation of murine mast cells and inhibits cytokine synthesis in murine peritoneal macrophages. J Gen Virol 83:1049–1058
    [Google Scholar]
  19. Josephson K., Logsdon N. J., Walter M. R. 2001; Crystal structure of the IL-10/IL-10R1 complex reveals a shared receptor binding site. Immunity 15:35–46 [CrossRef]
    [Google Scholar]
  20. Lateef Z., Fleming S., Halliday G., Faulkner L., Mercer A., Baird M. 2003; Orf virus-encoded interleukin-10 inhibits maturation, antigen presentation and migration of murine dendritic cells. J Gen Virol 84:1101–1109 [CrossRef]
    [Google Scholar]
  21. Lear A., Hutchison G., Reid H. W., Norval M., Haig D. M. 1996; Phenotypic characterisation of the dendritic cells accumulating in ovine dermis following primary and secondary orf virus infections. Eur J Dermatol 6:135–140 [CrossRef]
    [Google Scholar]
  22. Lutz M. B., Schuler G. 2002; Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity?. Trends Immunol 23:445–449 [CrossRef]
    [Google Scholar]
  23. Mercer A. A., Ueda N., Friederichs S.-M., Hofmann K., Fraser K. M., Bateman T., Fleming S. B. 2006; Comparative analysis of genome sequences of three isolates of Orf virus reveals unexpected sequence variation. Virus Res 116:146–158 [CrossRef]
    [Google Scholar]
  24. Moore K. W., de Waal Malefyt R., Coffman R. L., O'Garra A. 2001; Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765 [CrossRef]
    [Google Scholar]
  25. Morel A. S., Quaratino S., Douek D. C., Londei M. 1997; Split activity of interleukin-10 on antigen capture and antigen presentation by human dendritic cells: definition of a maturative step. Eur J Immunol 27:26–34 [CrossRef]
    [Google Scholar]
  26. Mourtada I., Le Tourneur M., Chevrant-Breton J., Le Gall F. 2000; Human orf and erythema multiforme. Ann Dermatol Venereol 127:397–399 (in French
    [Google Scholar]
  27. Pether J. V., Guerrier C. J., Jones S. M., Adam A. E., Kingsbury W. N. 1986; Giant orf in a normal individual. Br J Dermatol 115:497–499 [CrossRef]
    [Google Scholar]
  28. Raftery M. J., Wieland D., Gronewald S., Kraus A. A., Giese T., Schönrich G. 2004; Shaping phenotype, function, and survival of dendritic cells by cytomegalovirus-encoded IL-10. J Immunol 173:3383–3391 [CrossRef]
    [Google Scholar]
  29. Robinson A. J., Lyttle D. J. 1992; Parapoxviruses: their biology and potential as recombinant vaccines. In Recombinant Poxviruses pp  285–327 Edited by Binns M. M., Smith G. L. Boca Raton, FL: CRC Press;
    [Google Scholar]
  30. Rogers M., Bale P., De Silva L. M., Glasson M. J., Collins E. 1989; Giant parapox infection in a two year old child. Australas J Dermatol 30:87–91 [CrossRef]
    [Google Scholar]
  31. Sanchez R. L., Hebert A., Lucia H., Swedo J. 1985; Orf. A case report with histologic, electron microscopic, and immunoperoxidase studies. Arch Pathol Lab Med 109:166–170
    [Google Scholar]
  32. Savage J., Black M. M. 1972; ‘Giant’ orf of finger in a patient with a lymphoma. Proc R Soc Med 65:766–768
    [Google Scholar]
  33. Shortman K., Liu Y.-J. 2002; Mouse and human dendritic cell subtypes. Nat Rev Immunol 2:151–161 [CrossRef]
    [Google Scholar]
  34. Tan S. T., Blake G. B., Chambers S. 1991; Recurrent orf in an immunocompromised host. Br J Plast Surg 44:465–467 [CrossRef]
    [Google Scholar]
  35. Thoeni G., Stoitzner P., Brandacher G., Romani N., Heufler C., Werner-Felmayer G., Werner E. R. 2005; Tetrahydro-4-aminobiopterin attenuates dendritic cell-induced T cell priming independently from inducible nitric oxide synthase. J Immunol 174:7584–7591 [CrossRef]
    [Google Scholar]
  36. Villadangos J. A., Heath W. R. 2005; Life cycle, migration and antigen presenting functions of spleen and lymph node dendritic cells: limitations of the Langerhans cells paradigm. Semin Immunol 17:262–272 [CrossRef]
    [Google Scholar]
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