1887

Abstract

The lymphotropic lentiviruses feline immunodeficiency virus (FIV) and human immunodeficiency virus (HIV) enter cells by sequential interaction with primary receptors CD134 or CD4, respectively, and subsequently with chemokine receptors. The host-cell range for FIV is broader than that for HIV, but whether this is a function of receptor expression is unknown. Lack of reagents specific to feline molecules has limited detection and analysis of receptors and their interaction with viral components. Here, the expression of CD134 and CXCR4 on feline T and B lymphocytes, dendritic cells (DCs) and macrophages was examined and the kinetics of FIV replication were assessed. Quantification of CD134 mRNA by real-time PCR indicated expression in all leukocytes, with significantly more transcripts in CD4 lymphocytes than in other leukocytes. Antibodies against human CD134 bound inconsistently to feline leukocytes. CXCR4 was detected with antibody clone 12G5 on the surface of monocyte-derived cells only, but gene transcripts were present in all cells, with the highest copy number in lymphocytes. CXCR4 expression decreased and CD134 expression increased with cell activation in lymphocytes. A subtype B biological isolate of FIV infected DCs, macrophages and lymphocytes, with the highest replication in CD4 lymphocytes, whilst cloned FIV P14 infected all cells, but replicated less efficiently. Although viral replication was lower in DCs and macrophages than in lymphocytes, DCs expressed specific receptors and were infected productively with FIV, as indicated by viral ultrastructure and DNA detection. These results may implicate altered function of DCs in the induction of specific immunity against FIV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83161-0
2008-01-01
2020-01-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/1/277.html?itemId=/content/journal/jgv/10.1099/vir.0.83161-0&mimeType=html&fmt=ahah

References

  1. al Shamkhani, A., Birkeland, M. L., Puklavec, M., Brown, M. H., James, W. & Barclay, A. N. ( 1996; ). OX40 is differentially expressed on activated rat and mouse T cells and is the sole receptor for the OX40 ligand. Eur J Immunol 26, 1695–1699.[CrossRef]
    [Google Scholar]
  2. Bachmann, M. H., Mathiason-Dubard, C., Learn, G. H., Rodrigo, A. G., Sodora, D. L., Mazzetti, P., Hoover, E. A. & Mullins, J. I. ( 1997; ). Genetic diversity of feline immunodeficiency virus: dual infection, recombination, and distinct evolutionary rates among envelope sequence clades. J Virol 71, 4241–4253.
    [Google Scholar]
  3. Baribaud, F., Edwards, T. G., Sharron, M., Brelot, A., Heveker, N., Price, K., Mortari, F., Alizon, M., Tsang, M. & Doms, R. W. ( 2001; ). Antigenically distinct conformations of CXCR4. J Virol 75, 8957–8967.[CrossRef]
    [Google Scholar]
  4. 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]
  5. Bendinelli, M., Pistello, M., Del Mauro, D., Cammarota, G., Maggi, F., Leonildi, A., Giannecchini, S., Bergamini, C. & Matteucci, D. ( 2001; ). During readaptation in vivo, a tissue culture-adapted strain of feline immunodeficiency virus reverts to broad neutralization resistance at different times in individual hosts but through changes at the same position of the surface glycoprotein. J Virol 75, 4584–4593.[CrossRef]
    [Google Scholar]
  6. 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]
  7. Brelot, A., Heveker, N., Pleskoff, O., Sol, N. & Alizon, M. ( 1997; ). Role of the first and third extracellular domains of CXCR-4 in human immunodeficiency virus coreceptor activity. J Virol 71, 4744–4751.
    [Google Scholar]
  8. Brelot, A., Heveker, N., Adema, K., Hosie, M. J., Willett, B. & Alizon, M. ( 1999; ). Effect of mutations in the second extracellular loop of CXCR4 on its utilization by human and feline immunodeficiency viruses. J Virol 73, 2576–2586.
    [Google Scholar]
  9. Brunner, D. & Pedersen, N. C. ( 1989; ). Infection of peritoneal macrophages in vitro and in vivo with feline immunodeficiency virus. J Virol 63, 5483–5488.
    [Google Scholar]
  10. Dean, G. A., Reubel, G. H., Moore, P. F. & Pedersen, N. C. ( 1996; ). Proviral burden and infection kinetics of feline immunodeficiency virus in lymphocyte subsets of blood and lymph node. J Virol 70, 5165–5169.
    [Google Scholar]
  11. Dean, G. A., Himathongkham, S. & Sparger, E. E. ( 1999; ). Differential cell tropism of feline immunodeficiency virus molecular clones in vivo. J Virol 73, 2596–2603.
    [Google Scholar]
  12. de Parseval, A., Chatterji, U., Sun, P. & Elder, J. H. ( 2004a; ). Feline immunodeficiency virus targets activated CD4+ T cells by using CD134 as a binding receptor. Proc Natl Acad Sci U S A 101, 13044–13049.[CrossRef]
    [Google Scholar]
  13. de Parseval, A., Ngo, S., Sun, P. & Elder, J. H. ( 2004b; ). Factors that increase the effective concentration of CXCR4 dictate feline immunodeficiency virus tropism and kinetics of replication. J Virol 78, 9132–9143.[CrossRef]
    [Google Scholar]
  14. de Parseval, A., Su, S. V., Elder, J. H. & Lee, B. ( 2004c; ). Specific interaction of feline immunodeficiency virus surface glycoprotein with human DC-SIGN. J Virol 78, 2597–2600.[CrossRef]
    [Google Scholar]
  15. de Parseval, A., Chatterji, U., Morris, G., Sun, P., Olson, A. J. & Elder, J. H. ( 2005; ). Structural mapping of CD134 residues critical for interaction with feline immunodeficiency virus. Nat Struct Mol Biol 12, 60–66.[CrossRef]
    [Google Scholar]
  16. de Parseval, A., Grant, C. K., Sastry, K. J. & Elder, J. H. ( 2006; ). Sequential CD134-CXCR4 interactions in feline immunodeficiency virus (FIV): soluble CD134 activates FIV Env for CXCR4-dependent entry and reveals a cryptic neutralization epitope. J Virol 80, 3088–3091.[CrossRef]
    [Google Scholar]
  17. Doms, R. W. ( 2000; ). Beyond receptor expression: the influence of receptor conformation, density, and affinity in HIV-1 infection. Virology 276, 229–237.[CrossRef]
    [Google Scholar]
  18. Dow, S. W., Mathiason, C. K. & Hoover, E. A. ( 1999; ). In vivo monocyte tropism of pathogenic feline immunodeficiency viruses. J Virol 73, 6852–6861.
    [Google Scholar]
  19. English, R. V., Johnson, C. M., Gebhard, D. H. & Tompkins, M. B. ( 1993; ). In vivo lymphocyte tropism of feline immunodeficiency virus. J Virol 67, 5175–5186.
    [Google Scholar]
  20. Everitt, B. S. ( 1995; ). The analysis of repeated measures: a practical review with examples. Statistician 44, 113–135.[CrossRef]
    [Google Scholar]
  21. Farzan, M., Babcock, G. J., Vasilieva, N., Wright, P. L., Kiprilov, E., Mirzabekov, T. & Choe, H. ( 2002; ). The role of post-translational modifications of the CXCR4 amino terminus in stromal-derived factor 1 α association and HIV-1 entry. J Biol Chem 277, 29484–29489.[CrossRef]
    [Google Scholar]
  22. Frank, I., Piatak, M., Jr, Stoessel, H., Romani, N., Bonnyay, D., Lifson, J. D. & Pope, M. ( 2002; ). Infectious and whole inactivated simian immunodeficiency viruses interact similarly with primate dendritic cells (DCs): differential intracellular fate of virions in mature and immature DCs. J Virol 76, 2936–2951.[CrossRef]
    [Google Scholar]
  23. Gramaglia, I., Weinberg, A. D., Lemon, M. & Croft, M. ( 1998; ). Ox-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. J Immunol 161, 6510–6517.
    [Google Scholar]
  24. Hernandez, L. D., Hoffman, L. R., Wolfsberg, T. G. & White, J. M. ( 1996; ). Virus-cell and cell-cell fusion. Annu Rev Cell Dev Biol 12, 627–661.[CrossRef]
    [Google Scholar]
  25. Hurtrel, B., Chakrabarti, L., Hurtrel, M., Bach, J. M., Ganiere, J. P. & Montagnier, L. ( 1994; ). Early events in lymph nodes during infection with SIV and FIV. Res Virol 145, 221–227.[CrossRef]
    [Google Scholar]
  26. Lane, J. R. ( 1999; ). Quantitative HIV culture. In HIV Protocols, pp. 11–15. Edited by N. Michael & J. H. Kim. Totowa, NJ: Humana Press.
  27. Lapham, C. K., Romantseva, T., Petricoin, E., King, L. R., Manischewitz, J., Zaitseva, M. B. & Golding, H. ( 2002; ). CXCR4 heterogeneity in primary cells: possible role of ubiquitination. J Leukoc Biol 72, 1206–1214.
    [Google Scholar]
  28. Lekkerkerker, A. N., van Kooyk, Y. & Geijtenbeek, T. B. ( 2006; ). Viral piracy: HIV-1 targets dendritic cells for transmission. Curr HIV Res 4, 169–176.[CrossRef]
    [Google Scholar]
  29. Olmsted, R. A., Barnes, A. K., Yamamoto, J. K., Hirsch, V. M., Purcell, R. H. & Johnson, P. R. ( 1989; ). Molecular cloning of feline immunodeficiency virus. Proc Natl Acad Sci U S A 86, 2448–2452.[CrossRef]
    [Google Scholar]
  30. Paterson, D. J., Jefferies, W. A., Green, J. R., Brandon, M. R., Corthesy, P., Puklavec, M. & Williams, A. F. ( 1987; ). Antigens of activated rat T lymphocytes including a molecule of 50,000 Mr detected only on CD4 positive T blasts. Mol Immunol 24, 1281–1290.[CrossRef]
    [Google Scholar]
  31. Patterson, S., Gross, J., English, N., Stackpoole, A., Bedford, P. & Knight, S. C. ( 1995; ). CD4 expression on dendritic cells and their infection by human immunodeficiency virus. J Gen Virol 76, 1155–1163.[CrossRef]
    [Google Scholar]
  32. Phillips, T. R., Talbott, R. L., Lamont, C., Muir, S., Lovelace, K. & Elder, J. H. ( 1990; ). Comparison of two host cell range variants of feline immunodeficiency virus. J Virol 64, 4605–4613.
    [Google Scholar]
  33. Pion, M., Arrighi, J. F., Jiang, J., Lundquist, C. A., Hartley, O., Aiken, C. & Piguet, V. ( 2007; ). Analysis of HIV-1-X4 fusion with immature dendritic cells identifies a specific restriction that is independent of CXCR4 levels. J Invest Dermatol 127, 319–323.[CrossRef]
    [Google Scholar]
  34. Reggeti, F. & Bienzle, D. ( 2004; ). Feline immunodeficiency virus subtypes A, B and C and intersubtype recombinants in Ontario, Canada. J Gen Virol 85, 1843–1852.[CrossRef]
    [Google Scholar]
  35. Shimojima, M., Miyazawa, T., Ikeda, Y., McMonagle, E. L., Haining, H., Akashi, H., Takeuchi, Y., Hosie, M. J. & Willett, B. J. ( 2004; ). Use of CD134 as a primary receptor by the feline immunodeficiency virus. Science 303, 1192–1195.[CrossRef]
    [Google Scholar]
  36. Sloane, A. J., Raso, V., Dimitrov, D. S., Xiao, X., Deo, S., Muljadi, N., Restuccia, D., Turville, S., Kearney, C. & other authors ( 2005; ). Marked structural and functional heterogeneity in CXCR4: separation of HIV-1 and SDF-1α responses. Immunol Cell Biol 83, 129–143.[CrossRef]
    [Google Scholar]
  37. Sodora, D. L., Shpaer, E. G., Kitchell, B. E., Dow, S. W., Hoover, E. A. & Mullins, J. I. ( 1994; ). Identification of three feline immunodeficiency virus (FIV) env gene subtypes and comparison of the FIV and human immunodeficiency virus type 1 evolutionary patterns. J Virol 68, 2230–2238.
    [Google Scholar]
  38. Steinman, R. M. & Hemmi, H. ( 2006; ). Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 311, 17–58.
    [Google Scholar]
  39. Talbott, R. L., Sparger, E. E., Lovelace, K. M., Fitch, W. M., Pedersen, N. C., Luciw, P. A. & Elder, J. H. ( 1989; ). Nucleotide sequence and genomic organization of feline immunodeficiency virus. Proc Natl Acad Sci U S A 86, 5743–5747.[CrossRef]
    [Google Scholar]
  40. 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]
  41. van der Meer, F. J. U. M., Schuurman, N. M. P. & Egberink, H. F. ( 2007; ). Feline immunodeficiency virus infection is enhanced by feline bone marrow-derived dendritic cells. J Gen Virol 88, 251–258.[CrossRef]
    [Google Scholar]
  42. Willett, B. J., Hosie, M. J., Neil, J. C., Turner, J. D. & Hoxie, J. A. ( 1997a; ). Common mechanism of infection by lentiviruses. Nature 385, 587
    [Google Scholar]
  43. Willett, B. J., Picard, L., Hosie, M. J., Turner, J. D., Adema, K. & Clapham, P. R. ( 1997b; ). Shared usage of the chemokine receptor CXCR4 by the feline and human immunodeficiency viruses. J Virol 71, 6407–6415.
    [Google Scholar]
  44. Willett, B. J., Cannon, C. A. & Hosie, M. J. ( 2003; ). Expression of CXCR4 on feline peripheral blood mononuclear cells: effect of feline immunodeficiency virus infection. J Virol 77, 709–712.[CrossRef]
    [Google Scholar]
  45. Willett, B. J., McMonagle, E. L., Bonci, F., Pistello, M. & Hosie, M. J. ( 2006; ). Mapping the domains of CD134 as a functional receptor for feline immunodeficiency virus. J Virol 80, 7744–7747.[CrossRef]
    [Google Scholar]
  46. Zaitseva, M., Romantseva, T., Manischewitz, J., Wang, J., Goucher, D. & Golding, H. ( 2005; ). Increased CXCR4-dependent HIV-1 fusion in activated T cells: role of CD4/CXCR4 association. J Leukoc Biol 78, 1306–1317.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83161-0
Loading
/content/journal/jgv/10.1099/vir.0.83161-0
Loading

Data & Media loading...

Most cited articles

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