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1887

Journal of General Virology header logo Journal of General Virology

Volume 87, Issue 2

Human immunodeficiency virus types 1 and 2 have different replication kinetics in human primary macrophage culture No Access

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
2025-04-26
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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 TRIM5 α 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- β 1. 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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Human immunodeficiency virus types 1 and 2 have different replication kinetics in human primary macrophage culture
J. Gen. Virol. 87, 411 (2006); https://doi.org/10.1099/vir.0.81391-0
/content/journal/jgv/10.1099/vir.0.81391-0
/content/journal/jgv/10.1099/vir.0.81391-0
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