1887

Abstract

The parapoxvirus orf virus causes pustular dermatitis in sheep and is transmissible to humans. The virus encodes a secreted chemokine-binding protein (CBP). We examined the ability of this protein to inhibit migration of murine monocytes in response to CC inflammatory chemokines, using chemotaxis assays, and its effects on monocyte recruitment into the skin, using a mouse model in which inflammation was induced with bacterial lipopolysaccharide. CBP was shown to bind murine chemokines CCL2, CCL3 and CCL5 with high affinity by surface plasmon resonance and it completely inhibited chemokine-induced migration of monocytes at a CBP : chemokine molar ratio of 4 : 1. In the mouse, low levels of CBP potently inhibited the recruitment of Gr-1/CD11b monocytes to the site of inflammation in the skin but had little effect on neutrophil recruitment, suggesting that this factor plays a role in disrupting chemokine-induced recruitment of specific immune cell types to infection sites.

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2009-06-01
2019-11-19
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References

  1. Anderson, I. E., Reid, H. W., Nettleton, P. F., McInnes, C. J. & Haig, D. M. ( 2001; ). Detection of cellular cytokine mRNA expression during orf virus infection in sheep: differential interferon-gamma mRNA expression by cells in primary versus reinfection skin lesions. Vet Immunol Immunopathol 83, 161–176.[CrossRef]
    [Google Scholar]
  2. Baggiolini, M. ( 1998; ). Chemokines and leukocyte traffic. Nature 392, 565–568.[CrossRef]
    [Google Scholar]
  3. Charo, I. F. & Ransohoff, R. M. ( 2006; ). The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354, 610–621.[CrossRef]
    [Google Scholar]
  4. Conti, P., Pang, X., Boucher, W., Letourneau, R., Reale, M., Barbacane, R. C., Thibault, J. & Theoharides, T. C. ( 1997; ). Impact of Rantes and MCP-1 chemokines on in vivo basophilic cell recruitment in rat skin injection model and their role in modifying the protein and mRNA levels for histidine decarboxylase. Blood 89, 4120–4127.
    [Google Scholar]
  5. Cyster, J. G. ( 1999; ). Chemokines and cell migration in secondary lymphoid organs. Science 286, 2098–2102.[CrossRef]
    [Google Scholar]
  6. Dabbagh, K., Xiao, Y., Smith, C., Stepick-Biek, P., Kim, S. G., Lamm, W. J. E., Liggitt, D. H. & Lewis, D. B. ( 2000; ). Local blockade of allergic airway hyperreactivity and inflammation by the poxvirus-derived pan-CC-chemokine inhibitor vCCI. J Immunol 165, 3418–3422.[CrossRef]
    [Google Scholar]
  7. Deane, D., McInnes, C. J., Percival, A., Wood, A., Thomson, J., Lear, A., Gilray, J., Fleming, S., Mercer, A. & Haig, D. ( 2000; ). Orf virus encodes a novel secreted protein inhibitor of granulocyte-macrophage colony-stimulating factor and interleukin-2. J Virol 74, 1313–1320.[CrossRef]
    [Google Scholar]
  8. Dieu-Nosjean, M. C., Vicari, A., Lebecque, S. & Caux, C. ( 1999; ). Regulation of dendritic cell trafficking: a process that involves the participation of selective chemokines. J Leukoc Biol 66, 252–262.
    [Google Scholar]
  9. Fahey, J. V., Schaefer, T. M., Channon, J. Y. & Wira, C. R. ( 2005; ). Secretion of cytokines and chemokines by polarized human epithelial cells from the female reproductive tract. Hum Reprod 20, 1439–1446.[CrossRef]
    [Google Scholar]
  10. Fleming, S. B. & Mercer, A. A. ( 2007; ). Genus Parapoxvirus. In Poxviruses (in the series Birkhäuser Advances in Infectious Diseases, series Editors A. Schmidt, M. H. Wolff & S. H. E. Kaufmann), pp. 127–165. Edited by A. A. Mercer, A. Schmidt & O. Weber. Basel: Birkhäuser.
  11. Fleming, S. B., McCaughan, C. A., Andrews, A. E., Nash, A. D. & Mercer, A. A. ( 1997; ). A homologue of interleukin-10 is encoded by the poxvirus orf virus. J Virol 71, 4857–4861.
    [Google Scholar]
  12. Geissmann, F., Jung, S. & Littman, D. R. ( 2003; ). Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71–82.[CrossRef]
    [Google Scholar]
  13. González, L., Anderson, I., Deane, D., Summers, C. & Buxton, D. ( 2001; ). Detection of immune system cells in paraffin wax-embedded ovine tissues. J Comp Pathol 125, 41–47.[CrossRef]
    [Google Scholar]
  14. Haberstroh, U., Pocock, J., Gómez-Guerrero, C., Helmchen, U., Hamann, A., Gutierrez-Ramos, J. C., Stahl, R. A. & Thaiss, F. ( 2002; ). Expression of the chemokines MCP-1/CCL2 and RANTES/CCL5 is differentially regulated by infiltrating inflammatory cells. Kidney Int 62, 1264–1276.[CrossRef]
    [Google Scholar]
  15. Haig, D. M. & Mercer, A. A. ( 1998; ). Ovine diseases. Orf. Vet Res 29, 311–326.
    [Google Scholar]
  16. Haig, D. M., Thomson, J., McInnes, C. J., Deane, D. L., Anderson, I. E., McCaughan, C. A., Imlach, W., Mercer, A. A., Howard, C. J. & Fleming, S. B. ( 2002; ). A comparison of the anti-inflammatory and immunostimulatory activities of orf virus and ovine interleukin-10. Virus Res 90, 303–316.[CrossRef]
    [Google Scholar]
  17. Huang, H., Li, F., Cairns, C. M., Gordon, J. R. & Xiang, J. ( 2001; ). Neutrophils and B cells express XCR1 receptor and chemotactically respond to lymphotactin. Biochem Biophys Res Commun 281, 378–382.[CrossRef]
    [Google Scholar]
  18. Imhof, B. A. & Aurrand-Lions, M. ( 2004; ). Adhesion mechanisms regulating the migration of monocytes. Nat Rev Immunol 4, 432–444.[CrossRef]
    [Google Scholar]
  19. Ishikawa, F. & Miyazaki, S. ( 2005; ). New biodefense strategies by neutrophils. Arch Immunol Ther Exp (Warsz) 53, 226–233.
    [Google Scholar]
  20. Kopydlowski, K. M., Salkowski, C. A., Cody, M. J., van Rooijen, N., Major, J., Hamilton, T. A. & Vogel, S. N. ( 1999; ). Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. J Immunol 163, 1537–1544.
    [Google Scholar]
  21. Larsen, C. G., Anderson, A. O., Appella, E., Oppenheim, J. J. & Matsushima, K. ( 1989; ). The neutrophil-activating protein (NAP-1) is also chemotactic for T lymphocytes. Science 243, 1464–1466.[CrossRef]
    [Google Scholar]
  22. Liu, L., Dai, E., Miller, L., Seet, B., Alshad, L., Macauley, C., Li, X., Virgin, H. W., Bunce, C. & other authors ( 2004; ). Viral chemokine-binding proteins inhibit inflammatory responses and aortic allograft transplant vasculopathy in rat models. Transplantation 77, 1652–1660.[CrossRef]
    [Google Scholar]
  23. Lyttle, D. J., Fraser, K. M., Fleming, S. B., Mercer, A. A. & Robinson, A. J. ( 1994; ). Homologs of vascular endothelial growth factor are encoded by the poxvirus orf virus. J Virol 68, 84–92.
    [Google Scholar]
  24. Reading, P. C., Symons, J. A. & Smith, G. L. ( 2003; ). A soluble chemokine-binding protein from vaccinia virus reduces virulence and the inflammatory response to infection. J Immunol 170, 1435–1442.[CrossRef]
    [Google Scholar]
  25. Reiner, S. L. & Locksley, R. M. ( 1993; ). Cytokines in the differentiation of Th1/Th2 CD4+ subsets in leishmaniasis. J Cell Biochem 53, 323–328.
    [Google Scholar]
  26. Rollins, B. J. ( 1997; ). Chemokines. Blood 90, 909–928.
    [Google Scholar]
  27. Rossi, D. & Zlotnik, A. ( 2000; ). The biology of chemokines and their receptors. Annu Rev Immunol 18, 217–242.[CrossRef]
    [Google Scholar]
  28. Schuetze, N., Schoeneberger, S., Mueller, U., Freudenberg, M. A., Alber, G. & Straubinger, R. K. ( 2005; ). IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella Enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int Immunol 17, 649–659.[CrossRef]
    [Google Scholar]
  29. Seet, B. T., McCaughan, C. A., Handel, T. M., Mercer, A. A., Brunetti, C., McFadden, G. & Fleming, S. B. ( 2003; ). Analysis of an orf virus chemokine-binding protein: shifting ligand specificities among a family of poxvirus viroceptors. Proc Natl Acad Sci U S A 100, 15137–15142.[CrossRef]
    [Google Scholar]
  30. Sozzani, S., Luini, W., Borsatti, A., Polentarutti, N., Zhou, D., Piemonti, L., D'Amico, G., Power, C. A., Wells, T. N. & other authors ( 1997; ). Receptor expression and responsiveness of human dendritic cells to a defined set of CC and CXC chemokines. J Immunol 159, 1993–2000.
    [Google Scholar]
  31. Takeda, K., Kaisho, T. & Akira, S. ( 2003; ). Toll-like receptors. Annu Rev Immunol 21, 355–376.
    [Google Scholar]
  32. Uguccioni, M., D'Apuzzo, M., Loetscher, M., Dewald, B. & Baggiolini, M. ( 1995; ). Actions of the chemotactic cytokines MCP-1, MCP-2, MCP-3, RANTES, MIP-1α and MIP-1β on human monocytes. Eur J Immunol 25, 64–68.[CrossRef]
    [Google Scholar]
  33. Wang, J. M., McVicar, D. W., Oppenheim, J. J. & Kelvin, D. J. ( 1993; ). Identification of RANTES receptors on human monocytic cells: competition for binding and desensitization by homologous chemotactic cytokines. J Exp Med 177, 699–705.[CrossRef]
    [Google Scholar]
  34. Wetzler, C., Kampfer, H., Pfeilschifter, J. & Frank, S. ( 2000; ). Keratinocyte-derived chemotactic cytokines: expressional modulation by nitric oxide in vitro and during cutaneous wound repair in vivo. Biochem Biophys Res Commun 274, 689–696.[CrossRef]
    [Google Scholar]
  35. Yu, Y., Sweeney, M. D., Saad, O. M., Crown, S. E., Hsu, A. R., Handel, T. M. & Leary, J. A. ( 2005; ). Chemokine-glycosaminoglycan binding: specificity for CCR2 ligand binding to highly sulfated oligosaccharides using FTICR mass spectrometry. J Biol Chem 280, 32200–32208.[CrossRef]
    [Google Scholar]
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