1887

Abstract

This study compares the replication of primary isolates of human immunodeficiency virus type 2 (HIV-2) and type 1 (HIV-1) in monocyte-derived macrophages (MDMs). Eleven HIV-2 and five HIV-1 primary isolates that use CCR5, CXCR4 or both coreceptors to enter cells were included. Regardless of coreceptor preference, 10 of 11 HIV-2 viruses could enter, reverse transcribe and produce fully infectious virus in MDMs with efficiency equal to that in peripheral blood mononuclear cells. However, the kinetics of replication of HIV-2 compared with HIV-1 over time were distinct. HIV-2 had a burst of virus replication 2 days after infection that resolved into an apparent ‘latent state’ at day 3. HIV-1, however, continued to produce infectious virions at a lower, but steady, rate throughout the course of infection. These results may have implications for the lower pathogenesis and viral-load characteristics of HIV-2 infection.

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2006-02-01
2019-11-12
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References

  1. Alimonti, J. B., Ball, T. B. & Fowke, K. R. ( 2003; ). Mechanisms of CD4+ T lymphocyte cell death in human immunodeficiency virus infection and AIDS. J Gen Virol 84, 1649–1661.[CrossRef]
    [Google Scholar]
  2. Ariyoshi, K., Berry, N., Wilkins, A. & 9 other authors ( 1996; ). A community-based study of human immunodeficiency virus type 2 provirus load in rural village in West Africa. J Infect Dis 173, 245–248.[CrossRef]
    [Google Scholar]
  3. Berry, N., Jaffar, S., van der Loeff, M. S. & 9 other authors ( 2002; ). Low level viremia and high CD4% predict normal survival in a cohort of HIV type-2-infected villagers. AIDS Res Hum Retroviruses 18, 1167–1173.[CrossRef]
    [Google Scholar]
  4. Blaak, H., Boers, P. H. M., Gruters, R. A., Schuitemaker, H., van der Ende, M. E. & Osterhaus, A. D. M. E. ( 2005; ). CCR5, GPR15, and CXCR6 are major coreceptors of human immunodeficiency virus type 2 variants isolated from individuals with and without plasma viremia. J Virol 79, 1686–1700.[CrossRef]
    [Google Scholar]
  5. Clapham, P. R. & McKnight, Á. ( 2002; ). Cell surface receptors, virus entry and tropism of primate lentiviruses. J Gen Virol 83, 1809–1829.
    [Google Scholar]
  6. Clavel, F., Mansinho, K., Chamaret, S., Guetard, D., Favier, V., Nina, J., Santos-Ferreira, M. O., Champalimaud, J. L. & Montagnier, L. ( 1987; ). Human immunodeficiency virus type 2 infection associated with AIDS in West Africa. N Engl J Med 316, 1180–1185.[CrossRef]
    [Google Scholar]
  7. Connor, R. I., Sheridan, K. E., Ceradini, D., Choe, S. & Landau, N. R. ( 1997; ). Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 185, 621–628.[CrossRef]
    [Google Scholar]
  8. Damond, F., Descamps, D., Farfara, I. & 7 other authors ( 2001; ). Quantification of proviral load of human immunodeficiency virus type 2 subtypes A and B using real-time PCR. J Clin Microbiol 39, 4264–4268.[CrossRef]
    [Google Scholar]
  9. Damond, F., Gueudin, M., Pueyo, S. & 8 other authors ( 2002; ). Plasma RNA viral load in human immunodeficiency virus type 2 subtype A and subtype B infections. J Clin Microbiol 40, 3654–3659.[CrossRef]
    [Google Scholar]
  10. Dawson, M. ( 1987; ). Pathogenesis of maedi-visna. Vet Rec 120, 451–454.[CrossRef]
    [Google Scholar]
  11. Deng, H., Liu, R., Ellmeier, W. & 12 other authors ( 1996; ). Identification of a major co-receptor for primary isolates of HIV-1. Nature 381, 661–666.[CrossRef]
    [Google Scholar]
  12. Eisert, V., Kreutz, M., Becker, K., Königs, C., Alex, U., Rübsamen-Waigmann, H., Andreesen, R. & von Briesen, H. ( 2001; ). Analysis of cellular factors influencing the replication of human immunodeficiency virus type I in human macrophages derived from blood of different healthy donors. Virology 286, 31–44.[CrossRef]
    [Google Scholar]
  13. Feng, Y., Broder, C. C., Kennedy, P. E. & Berger, E. A. ( 1996; ). HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272, 872–877.[CrossRef]
    [Google Scholar]
  14. Garaci, E., Caroleo, M. C., Aloe, L. & 8 other authors ( 1999; ). Nerve growth factor is an autocrine factor essential for the survival of macrophages infected with HIV. Proc Natl Acad Sci U S A 96, 14013–14018.[CrossRef]
    [Google Scholar]
  15. Gartner, S., Markovits, P., Markovitz, D. M., Kaplan, M. H., Gallo, R. C. & Popovic, M. ( 1986; ). The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233, 215–219.[CrossRef]
    [Google Scholar]
  16. Gomes, P., Taveira, N. C., Pereira, J. M., Antunes, F., Ferreira, M. O. S. & Lourenço, M. H. ( 1999; ). Quantitation of human immunodeficiency virus type 2 DNA in peripheral blood mononuclear cells by using a quantitative-competitive PCR assay. J Clin Microbiol 37, 453–456.
    [Google Scholar]
  17. Gorry, P. R., Churchill, M., Crowe, S. M., Cunningham, A. L. & Gabuzda, D. ( 2005; ). Pathogenesis of macrophage tropic HIV-1. Curr HIV Res 3, 53–60.[CrossRef]
    [Google Scholar]
  18. Kanki, P. J., Travers, K. U., Mboup, S. & 9 other authors ( 1994; ). Slower heterosexual spread of HIV-2 than HIV-1. Lancet 343, 943–946.[CrossRef]
    [Google Scholar]
  19. Kulkarni, S., Tripathy, S., Agnihotri, K. & 7 other authors ( 2005; ). Indian primary HIV-2 isolates and relationship between V3 genotype, biological phenotype and coreceptor usage. Virology 337, 68–75.[CrossRef]
    [Google Scholar]
  20. Li, S., Juarez, J., Alali, M., Dwyer, D., Collman, R., Cunningham, A. & Naif, H. M. ( 1999; ). Persistent CCR5 utilization and enhanced macrophage tropism by primary blood human immunodeficiency virus type 1 isolates from advanced stages of disease and comparison to tissue-derived isolates. J Virol 73, 9741–9755.
    [Google Scholar]
  21. Lizeng, Q., Skott, P., Sourial, S., Nilsson, C., Andersson, S., Ehnlund, M., Taveira, N. & Björling, E. ( 2003; ). Serum immunoglobulin A (IgA)-mediated immunity in human immunodeficiency virus type 2 (HIV-2) infection. Virology 308, 225–232.[CrossRef]
    [Google Scholar]
  22. Loussert-Ajaka, I., Simon, F., Farfara, I., Descamps, D., Collin, G. & Brun-Vezinet, F. ( 1995; ). Detection of circulating human immunodeficiency virus type 2 in plasma by reverse transcription polymerase chain reaction. Res Virol 146, 409–414.[CrossRef]
    [Google Scholar]
  23. Maddon, P. J., Dalgleish, A. G., McDougal, J. S., Clapham, P. R., Weiss, R. A. & Axel, R. ( 1986; ). The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47, 333–348.[CrossRef]
    [Google Scholar]
  24. Marlink, R., Kanki, P., Thior, I. & 13 other authors ( 1994; ). Reduced rate of disease development after HIV-2 infection as compared to HIV-1. Science 265, 1587–1590.[CrossRef]
    [Google Scholar]
  25. McKnight, Á., Dittmar, M. T., Moniz-Periera, J. & 8 other authors ( 1998; ). A broad range of chemokine receptors are used by primary isolates of human immunodeficiency virus type 2 as coreceptors with CD4. J Virol 72, 4065–4071.
    [Google Scholar]
  26. McKnight, Á., Griffiths, D. J., Dittmar, M., Clapham, P. & Thomas, E. ( 2001; ). Characterization of a late entry event in the replication cycle of human immunodeficiency virus type 2. J Virol 75, 6914–6922.[CrossRef]
    [Google Scholar]
  27. Meylan, P. R., Baumgartner, M., Ciuffi, A., Munoz, M. & Sahli, R. ( 1998; ). The nef gene controls syncytium formation in primary human lymphocytes and macrophages infected by HIV type 1. AIDS Res Hum Retroviruses 14, 1531–1542.[CrossRef]
    [Google Scholar]
  28. Mörner, A., Björndal, Å., Albert, J., KewalRamani, V. N., Littman, D. R., Inoue, R., Thorstensson, R., Fenyö, E. M. & Björling, E. ( 1999; ). Primary human immunodeficiency virus type 2 (HIV-2) isolates, like HIV-1 isolates, frequently use CCR5 but show promiscuity in coreceptor usage. J Virol 73, 2343–2349.
    [Google Scholar]
  29. Mörner, A., Björndal, Å., Leandersson, A.-C., Albert, J., Björling, E. & Jansson, M. ( 2002; ). CCR5 or CXCR4 is required for efficient infection of peripheral blood mononuclear cells by promiscuous human immunodeficiency virus type 2 primary isolates. AIDS Res Hum Retroviruses 18, 193–200.[CrossRef]
    [Google Scholar]
  30. Mörner, A., Thomas, J. A., Björling, E., Munson, P. J., Lucas, S. B. & McKnight, Á. ( 2003; ). Productive HIV-2 infection in the brain is restricted to macrophages/microglia. AIDS 17, 1451–1455.[CrossRef]
    [Google Scholar]
  31. Muller, J. M., Ziegler-Heitbrock, H. W. & Baeuerle, P. A. ( 1993; ). Nuclear factor kappa B, a mediator of lipopolysaccharide effects. Immunobiology 187, 233–256.[CrossRef]
    [Google Scholar]
  32. Neil, S., Martin, F., Ikeda, Y. & Collins, M. ( 2001; ). Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J Virol 75, 5448–5456.[CrossRef]
    [Google Scholar]
  33. Neil, S. J. D., Aasa-Chapman, M. M. I., Clapham, P. R., Nibbs, R. J., McKnight, Á. & Weiss, R. A. ( 2005; ). The promiscuous CC chemokine receptor D6 is a functional coreceptor for primary isolates of human immunodeficiency virus type 1 (HIV-1) and HIV-2 on astrocytes. J Virol 79, 9618–9624.[CrossRef]
    [Google Scholar]
  34. Norrgren, H., Cardoso, A. N., da Silva, Z. J., Andersson, S., Dias, F., Biberfeld, G. & Naucler, A. ( 1997; ). Increased prevalence of HIV-2 infection in hospitalized patients with severe bacterial diseases in Guinea-Bissau. Scand J Infect Dis 29, 453–459.[CrossRef]
    [Google Scholar]
  35. Popper, S. J., Sarr, A. D., Travers, K. U., Guèye-Ndiaye, A., Mboup, S., Essex, M. E. & Kanki, P. J. ( 1999; ). Lower human immunodeficiency virus (HIV) type 2 viral load reflects the difference in pathogenicity of HIV-1 and HIV-2. J Infect Dis 180, 1116–1121.[CrossRef]
    [Google Scholar]
  36. Popper, S. J., Sarr, A. D., Guèye-Ndiaye, A., Mboup, S., Essex, M. E. & Kanki, P. J. ( 2000; ). Low plasma human immunodeficiency virus type 2 viral load is independent of proviral load: low virus production in vivo. J Virol 74, 1554–1557.[CrossRef]
    [Google Scholar]
  37. Reeves, J. D., Hibbitts, S., Simmons, G., McKnight, Á., Azevedo-Pereira, J. M., Moniz-Pereira, J. & Clapham, P. R. ( 1999; ). Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4-negative cells via CCR5 and CXCR4: comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism in vivo. J Virol 73, 7795–7804.
    [Google Scholar]
  38. Sattentau, Q. J., Clapham, P. R., Weiss, R. A., Beverley, P. C., Montagnier, L., Alhalabi, M. F., Gluckmann, J. C. & Klatzmann, D. ( 1988; ). The human and simian immunodeficiency viruses HIV-1, HIV-2 and SIV interact with similar epitopes on their cellular receptor, the CD4 molecule. AIDS 2, 101–105.[CrossRef]
    [Google Scholar]
  39. Schmitz, C., Marchant, D., Neil, S. J. D., Aubin, K., Reuter, S., Dittmar, M. T. & McKnight, Á. ( 2004; ). Lv2, a novel postentry restriction, is mediated by both capsid and envelope. J Virol 78, 2006–2016.[CrossRef]
    [Google Scholar]
  40. Schuitemaker, H. ( 1994; ). Macrophage-tropic HIV-1 variants: initiators of infection and AIDS pathogenesis? J Leukoc Biol 56, 218–224.
    [Google Scholar]
  41. Schuitemaker, H., Kootstra, N. A., Fouchier, R. A. M., Hooibrink, B. & Miedema, F. ( 1994; ). Productive HIV-1 infection of macrophages restricted to the cell fraction with proliferative capacity. EMBO J 13, 5929–5936.
    [Google Scholar]
  42. Schutten, M., van Baalen, C. A., Guillon, C., Huisman, R. C., Boers, P. H. M., Sintnicolaas, K., Gruters, R. A. & Osterhaus, A. D. M. E. ( 2001; ). Macrophage tropism of human immunodeficiency virus type 1 facilitates in vivo escape from cytotoxic T-lymphocyte pressure. J Virol 75, 2706–2709.[CrossRef]
    [Google Scholar]
  43. Sellon, D. C., Perry, S. T., Coggins, L. & Fuller, F. J. ( 1992; ). Wild-type equine infectious anemia virus replicates in vivo predominantly in tissue macrophages, not in peripheral blood monocytes. J Virol 66, 5906–5913.
    [Google Scholar]
  44. Simmons, G., McKnight, Á., Takeuchi, Y., Hoshino, H. & Clapham, P. R. ( 1995; ). Cell-to-cell fusion, but not virus entry in macrophages by T-cell line tropic HIV-1 strains: a V3 loop-determined restriction. Virology 209, 696–700.[CrossRef]
    [Google Scholar]
  45. Simmons, G., Wilkinson, D., Reeves, J. D. & 8 other authors ( 1996; ). Primary, syncytium-inducing human immunodeficiency virus type 1 isolates are dual-tropic and most can use either Lestr or CCR5 as coreceptors for virus entry. J Virol 70, 8355–8360.
    [Google Scholar]
  46. Simmons, G., Reeves, J. D., McKnight, Á. & 8 other authors ( 1998; ). CXCR4 as a functional coreceptor for human immunodeficiency virus type 1 infection of primary macrophages. J Virol 72, 8453–8457.
    [Google Scholar]
  47. Soda, Y., Shimizu, N., Jinno, A., Liu, H.-Y., Kanbe, K., Kitamura, T. & Hoshino, H. ( 1999; ). Establishment of a new system for determination of coreceptor usages of HIV based on the human glioma NP-2 cell line. Biochem Biophys Res Commun 258, 313–321.[CrossRef]
    [Google Scholar]
  48. Sol, N., Ferchal, F., Braun, J., Pleskoff, O., Tréboute, C., Ansart, I. & Alizon, M. ( 1997; ). Usage of the coreceptors CCR-5, CCR-3, and CXCR-4 by primary and cell line-adapted human immunodeficiency virus type 2. J Virol 71, 8237–8244.
    [Google Scholar]
  49. Sonza, S., Maerz, A., Deacon, N., Meanger, J., Mills, J. & Crowe, S. ( 1996; ). Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes. J Virol 70, 3863–3869.
    [Google Scholar]
  50. Sousa, A. E., Carneiro, J., Meier-Schellersheim, M., Grossman, Z. & Victorino, R. M. M. ( 2002; ). CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J Immunol 169, 3400–3406.[CrossRef]
    [Google Scholar]
  51. Stremlau, M., Owens, C. M., Perron, M. J., Kiessling, M., Autissier, P. & Sodroski, J. ( 2004; ). The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427, 848–853.[CrossRef]
    [Google Scholar]
  52. Thomas, E. R., Shotton, C., Weiss, R. A., Clapham, P. R. & McKnight, Á. ( 2003; ). CD4-dependent and CD4-independent HIV-2: consequences for neutralization. AIDS 17, 291–300.[CrossRef]
    [Google Scholar]
  53. Triques, K. & Stevenson, M. ( 2004; ). Characterization of restrictions to human immunodeficiency virus type 1 infection of monocytes. J Virol 78, 5523–5527.[CrossRef]
    [Google Scholar]
  54. Tuttle, D. L., Anders, C. B., Aquino-De Jesus, M. J. & 9 other authors ( 2002; ). Increased replication of non-syncytium-inducing HIV type 1 isolates in monocyte-derived macrophages is linked to advanced disease in infected children. AIDS Res Hum Retroviruses 18, 353–362.[CrossRef]
    [Google Scholar]
  55. Wang, J., Guan, E., Roderiquez, G. & Norcross, M. A. ( 2001; ). Synergistic induction of apoptosis in primary CD4+ T cells by macrophage-tropic HIV-1 and TGF-β1. J Immunol 167, 3360–3366.[CrossRef]
    [Google Scholar]
  56. Weiss, R. A., Clapham, P. R., Weber, J. N., Whitby, D., Tedder, R. S., O'Connor, T., Chamaret, S. & Montagnier, L. ( 1988; ). HIV-2 antisera cross-neutralize HIV-1. AIDS 2, 95–100.[CrossRef]
    [Google Scholar]
  57. Zhang, M., Li, X., Pang, X., Ding, L., Wood, O., Clouse, K., Hewlett, I. & Dayton, A. I. ( 2001; ). Identification of a potential HIV-induced source of bystander-mediated apoptosis in T cells: upregulation of TRAIL in primary human macrophages by HIV-1 Tat. J Biomed Sci 8, 290–296.[CrossRef]
    [Google Scholar]
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