1887

Abstract

In the pathogenesis of feline immunodeficiency virus (FIV) infection, feline dendritic cells (feDCs) are thought to play an important role. As with DCs in other species, feDCs are believed to transport virus particles to lymph nodes and transfer them to lymphocytes. Our investigation has focused on the ability of feDCs to influence the infection of syngeneic peripheral blood mononuclear cells (PBMCs) and allogeneic thymocytes. feDCs were derived from bone marrow mononuclear cells that were cultured under the influence of feline interleukin-4 and feline granulocyte–macrophage colony-stimulating factor. By using these feDCs in co-culture with resting PBMCs, an upregulation of FIV replication was shown. An enhancement of FIV infection was also detected when co-cultures of feDCs/feline thymocytes were infected. To obtain this enhancement, direct contact of the cells in the co-culture was necessary; transwell cultures showed that the involvement of only soluble factors produced by feDCs in this process is not likely. These feDCs were also able to induce the proliferation of resting thymocytes, which might explain the enhanced FIV replication observed. Together, these data suggest that feDCs have abilities similar to those shown for simian and human DCs in the interaction with leukocytes. This system is suitable for further investigations of the interplay of DC and T cells during FIV infection .

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2007-01-01
2019-10-21
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References

  1. Banchereau, J. & Steinman, R. M. ( 1998; ). Dendritic cells and the control of immunity. Nature 392, 245–252.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  3. Bendinelli, M., Pistello, M., Lombardi, S., Poli, A., Garzelli, C., Matteucci, D., Ceccherini-Nelli, L., Malvaldi, G. & Tozzini, F. ( 1995; ). Feline immunodeficiency virus: an interesting model for AIDS studies and an important cat pathogen. Clin Microbiol Rev 8, 87–112.
    [Google Scholar]
  4. Bienzle, D., Reggeti, F., Clark, M. E. & Chow, C. ( 2003; ). Immunophenotype and functional properties of feline dendritic cells derived from blood and bone marrow. Vet Immunol Immunopathol 96, 19–30.[CrossRef]
    [Google Scholar]
  5. Bingen, A., Nonnenmacher, H., Bastien-Valle, M. & Martin, J. P. ( 2002; ). Tissues rich in macrophagic cells are the major sites of feline immunodeficiency virus uptake after intravenous inoculation into cats. Microbes Infect 4, 795–803.[CrossRef]
    [Google Scholar]
  6. Brown, W. C., Bissey, L., Logan, K. S., Pedersen, N. C., Elder, J. H. & Collisson, E. W. ( 1991; ). Feline immunodeficiency virus infects both CD4+ and CD8+ T lymphocytes. J Virol 65, 3359–3364.
    [Google Scholar]
  7. Burkhard, M. J. & Dean, G. A. ( 2003; ). Transmission and immunopathogenesis of FIV in cats as a model for HIV. Curr HIV Res 1, 15–29.[CrossRef]
    [Google Scholar]
  8. Cameron, P. U., Freudenthal, P. S., Barker, J. M., Gezelter, S., Inaba, K. & Steinman, R. M. ( 1992; ). Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257, 383–387.[CrossRef]
    [Google Scholar]
  9. Cameron, P., Pope, M., Granelli-Piperno, A. & Steinman, R. M. ( 1996; ). Dendritic cells and the replication of HIV-1. J Leukoc Biol 59, 158–171.
    [Google Scholar]
  10. Cody, V., Shen, H., Shlyankevich, M., Tigelaar, R. E., Brandsma, J. L. & Hanlon, D. J. ( 2005; ). Generation of dendritic cells from rabbit bone marrow mononuclear cell cultures supplemented with hGM-CSF and hIL-4. Vet Immunol Immunopathol 103, 163–172.[CrossRef]
    [Google Scholar]
  11. de Parseval, A., Su, S. V., Elder, J. H. & Lee, B. ( 2004; ). Specific interaction of feline immunodeficiency virus surface glycoprotein with human DC-SIGN. J Virol 78, 2597–2600.[CrossRef]
    [Google Scholar]
  12. Egberink, H. F., Ederveen, J., Montelaro, R. C., Pedersen, N. C., Horzinek, M. C. & Koolen, M. J. ( 1990; ). Intracellular proteins of feline immunodeficiency virus and their antigenic relationship with equine infectious anaemia virus proteins. J Gen Virol 71, 739–743.[CrossRef]
    [Google Scholar]
  13. Egberink, H. F., Keldermans, C. E., Koolen, M. J. & Horzinek, M. C. ( 1992; ). Humoral immune response to feline immunodeficiency virus in cats with experimentally induced and naturally acquired infections. Am J Vet Res 53, 1133–1138.
    [Google Scholar]
  14. Freer, G., Matteucci, D., Mazzetti, P., Bozzacco, L. & Bendinelli, M. ( 2005; ). Generation of feline dendritic cells derived from peripheral blood monocytes for in vivo use. Clin Diagn Lab Immunol 12, 1202–1208.
    [Google Scholar]
  15. Gemeniano, M. C., Sawai, E. T., Leutenegger, C. M. & Sparger, E. E. ( 2003; ). Feline immunodeficiency virus ORF-A is required for virus particle formation and virus infectivity. J Virol 77, 8819–8830.[CrossRef]
    [Google Scholar]
  16. Granelli-Piperno, A., Delgado, E., Finkel, V., Paxton, W. & Steinman, R. M. ( 1998; ). Immature dendritic cells selectively replicate macrophagetropic (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J Virol 72, 2733–2737.
    [Google Scholar]
  17. Gummuluru, S., KewalRamani, V. N. & Emerman, M. ( 2002; ). Dendritic cell-mediated viral transfer to T cells is required for human immunodeficiency virus type 1 persistence in the face of rapid cell turnover. J Virol 76, 10692–10701.[CrossRef]
    [Google Scholar]
  18. Gummuluru, S., Rogel, M., Stamatatos, L. & Emerman, M. ( 2003; ). Binding of human immunodeficiency virus type 1 to immature dendritic cells can occur independently of DC-SIGN and mannose binding C-type lectin receptors via a cholesterol-dependent pathway. J Virol 77, 12865–12874.[CrossRef]
    [Google Scholar]
  19. Ibisch, C., Pradal, G., Bach, J. M. & Lieubeau, B. ( 2005; ). Functional canine dendritic cells can be generated in vitro from peripheral blood mononuclear cells and contain a cytoplasmic ultrastructural marker. J Immunol Methods 298, 175–182.[CrossRef]
    [Google Scholar]
  20. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S. & Steinman, R. M. ( 1992; ). Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176, 1693–1702.[CrossRef]
    [Google Scholar]
  21. Kimata, J. T., Wilson, J. M. & Patel, P. G. ( 2004; ). The increased replicative capacity of a late-stage simian immunodeficiency virus mne variant is evident in macrophage- or dendritic cell-T-cell cocultures. Virology 327, 307–317.[CrossRef]
    [Google Scholar]
  22. Langenkamp, A., Casorati, G., Garavaglia, C., Dellabona, P., Lanzavecchia, A. & Sallusto, F. ( 2002; ). T cell priming by dendritic cells: thresholds for proliferation, differentiation and death and intraclonal functional diversification. Eur J Immunol 32, 2046–2054.[CrossRef]
    [Google Scholar]
  23. Lichtner, M., Maranon, C., Vidalain, P. O., Azocar, O., Hanau, D., Lebon, P., Burgard, M., Rouzioux, C., Vullo, V. & other authors ( 2004; ). HIV type 1-infected dendritic cells induce apoptotic death in infected and uninfected primary CD4 T lymphocytes. AIDS Res Hum Retroviruses 20, 175–182.[CrossRef]
    [Google Scholar]
  24. Lore, K. & Larsson, M. ( 2003; ). The role of dendritic cells in the pathogenesis of HIV-1 infection. APMIS 111, 776–788.[CrossRef]
    [Google Scholar]
  25. Messmer, D., Ignatius, R., Santisteban, C., Steinman, R. M. & Pope, M. ( 2000; ). The decreased replicative capacity of simian immunodeficiency virus SIVmac239Delta(nef) is manifest in cultures of immature dendritic cells and T cells. J Virol 74, 2406–2413.[CrossRef]
    [Google Scholar]
  26. Obert, L. A. & Hoover, E. A. ( 2002; ). Early pathogenesis of transmucosal feline immunodeficiency virus infection. J Virol 76, 6311–6322.[CrossRef]
    [Google Scholar]
  27. O'Doherty, U., Ignatius, R., Bhardwaj, N. & Pope, M. ( 1997; ). Generation of monocyte-derived dendritic cells from precursors in rhesus macaque blood. J Immunol Methods 207, 185–194.[CrossRef]
    [Google Scholar]
  28. Pedersen, N. C., Ho, E. W., Brown, M. L. & Yamamoto, J. K. ( 1987; ). Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 235, 790–793.[CrossRef]
    [Google Scholar]
  29. Petit, C., Buseyne, F., Boccaccio, C., Abastado, J. P., Heard, J. M. & Schwartz, O. ( 2001; ). Nef is required for efficient HIV-1 replication in cocultures of dendritic cells and lymphocytes. Virology 286, 225–236.[CrossRef]
    [Google Scholar]
  30. Pinchuk, L. M., Grouard-Vogel, G., Magaletti, D. M., Doty, R. T., Andrews, R. G. & Clark, E. A. ( 1999; ). Isolation and characterization of macaque dendritic cells from CD34(+) bone marrow progenitors. Cell Immunol 196, 34–40.[CrossRef]
    [Google Scholar]
  31. Pope, M., Betjes, M. G., Romani, N., Hirmand, H., Cameron, P. U., Hoffman, L., Gezelter, S., Schuler, G. & Steinman, R. M. ( 1994; ). Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1. Cell 78, 389–398.[CrossRef]
    [Google Scholar]
  32. Pope, M., Gezelter, S., Gallo, N., Hoffman, L. & Steinman, R. M. ( 1995; ). Low levels of HIV-1 infection in cutaneous dendritic cells promote extensive viral replication upon binding to memory CD4+ T cells. J Exp Med 182, 2045–2056.[CrossRef]
    [Google Scholar]
  33. Pope, M., Elmore, D., Ho, D. & Marx, P. ( 1997; ). Dendritic cell-T cell mixtures, isolated from the skin and mucosae of macaques, support the replication of SIV. AIDS Res Hum Retroviruses 13, 819–827.[CrossRef]
    [Google Scholar]
  34. Sprague, W. S., Pope, M. & Hoover, E. A. ( 2005; ). Culture and comparison of feline myeloid dendritic cells vs macrophages. J Comp Pathol 133, 136–145.[CrossRef]
    [Google Scholar]
  35. Talmor, M., Mirza, A., Turley, S., Mellman, I., Hoffman, L. A. & Steinman, R. M. ( 1998; ). Generation or large numbers of immature and mature dendritic cells from rat bone marrow cultures. Eur J Immunol 28, 811–817.[CrossRef]
    [Google Scholar]
  36. Torres, B. A., Tanabe, T. & Johnson, H. M. ( 1996a; ). Characterization of Nef-induced CD4 T cell proliferation. Biochem Biophys Res Commun 225, 54–61.[CrossRef]
    [Google Scholar]
  37. Torres, B. A., Tanabe, T., Yamamoto, J. K. & Johnson, H. M. ( 1996b; ). HIV encodes for its own CD4 T-cell superantigen mitogen. Biochem Biophys Res Commun 225, 672–678.[CrossRef]
    [Google Scholar]
  38. Toyosaki, T., Miyazawa, T., Furuya, T., Tomonaga, K., Shin, Y. S., Okita, M., Kawaguchi, Y., Kai, C., Mori, S. & Mikami, T. ( 1993; ). Localization of the viral antigen of feline immunodeficiency virus in the lymph nodes of cats at the early stage of infection. Arch Virol 131, 335–347.[CrossRef]
    [Google Scholar]
  39. Wilflingseder, D., Banki, Z., Dierich, M. P. & Stoiber, H. ( 2005; ). Mechanisms promoting dendritic cell-mediated transmission of HIV. Mol Immunol 42, 229–237.[CrossRef]
    [Google Scholar]
  40. Wu, L., Bashirova, A. A., Martin, T. D., Villamide, L., Mehlhop, E., Chertov, A. O., Unutmaz, D., Pope, M., Carrington, M. & KewalRamani, V. N. ( 2002; ). Rhesus macaque dendritic cells efficiently transmit primate lentiviruses independently of DC-SIGN. Proc Natl Acad Sci U S A 99, 1568–1573.[CrossRef]
    [Google Scholar]
  41. Yamamoto, J. K., Hansen, H., Ho, E. W., Morishita, T. Y., Okuda, T., Sawa, T. R., Nakamura, R. M. & Pedersen, N. C. ( 1989; ). Epidemiologic and clinical aspects of feline immunodeficiency virus infection in cats from the continental United States and Canada and possible mode of transmission. J Am Vet Med Assoc 194, 213–220.
    [Google Scholar]
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