Skip to content
1887

Journal of General Virology header logo Journal of General Virology

Volume 75, Issue 7

Definition of the range and distribution of human immunodeficiency virus macrophage tropism using PCR-based infectivity measurements No Access

Abstract

The tropism of human immunodeficiency virus (HIV) for macrophages (mø)is a well recognized phenomenon, but the range and distribution of m𝜙-tropic phenotypes have not been defined by quantitative means. This study uses a PCR-based infectivity assay to derive an index of m𝜙 tropism for several common strains of HIV. The results show that m𝜙 tropism varies over about six orders of magnitude and that the most m𝜙-tropic strains have a higher infectivity for m𝜙 than for peripheral blood lymphocytes. Strains were distributed throughout this range, suggesting that m𝜙 tropism is a continuously variable phenotypic property. Although the degree of tropism was strongly influenced by the mode of isolation and propagation of virus strains, there was no evidence for the existence of distinct m𝜙-tropic or non-m𝜙-tropic phenotypes. Finally, the tropism of two selected strains was found to be determined by an early step in replication, probably virus entry.

  • Received:
  • Accepted:
  • Published Online:
© The Journal of General Virology 1994
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-75-7-1597
1994-07-01
2025-05-24
Loading full text...

Full text loading...

References

  1. Asjo B., Morfelt-Manson L., Albert J., Biberfeld G., Karlsson A., Lidman K., Fenyo E. M. 1986; Replicative capacity of human immunodeficiency virus from patients with varying severity of HIV infection. Lancet ii:660–662
     [Google Scholar]
  2. Brighty D. W., Rosenberg M., Chen I. S. Y., Ivey-Hoyle M. 1991; Envelope proteins from clinical isolates of HIV-1 which are refractory to neutralisation by sCD4 possess high affinity for the CD4 receptor. Proceedings of the National Academy of Sciences, U.S.A 88:7802–7805
     [Google Scholar]
  3. Cann A. J., Zack J. A., Go A. S., Arrigo S. J., Koyanagi Y., Green P. L., Koyanagi Y., Pang S., Chen I. S. Y. 1990; Human immunodeficiency virus type 1 T-cell tropism is determined by events prior to provirus formation. Journal of Virology 64:4735–4742
     [Google Scholar]
  4. Cheng-Mayer C., Weiss C., Seto D., Levy J. A. 1989; Isolates of human immunodeficiency virus type 1 from the brain may constitute a special group of the AIDS virus. Proceedings of the National Academy of Sciences, U.S.A 86:8575–8579
     [Google Scholar]
  5. Cheng-Mayer C., Quiroga M., Tung J. W., Dina D., Levy J. A. 1990; Viral determinants of human immunodeficiency virus type 1 T-cell or macrophage tropism, cytopathogenicity and CD4 antigen modulation. Journal of Virology 64:4390–4398
     [Google Scholar]
  6. Chesebro B., Nishno J., Perryman S., Cann A., O’Brien W., Chen I. S. Y., Wehrly K. 1991; Identification of human immunodeficiency virus envelope gene sequences influencing viral entry into CD4-positive HeLa cells, T-leukemia cells and macrophages. Journal of Virology 65:5782–5789
     [Google Scholar]
  7. Collin M., James W. S., Gordon S. 1991; Development of techniques to analyse the formation of HIV provirus in primary human macrophages. Research in Virology 142:105–112
     [Google Scholar]
  8. Collin M., Herbein G., Montaner L., Gordon S. 1993; PCR analysis of HIV-1 infection of macrophages: virus entry is CD4-dependent. Research in Virology 144:13–16
     [Google Scholar]
  9. Collman R., Hassan N. F., Walker R., Godfrey B., Cutilli J., Hastings J. C., Friedman H., Douglas S. D., Nathanson N. 1989; Infection of monocyte-derived macrophages with human immunodeficiency virus type 1 (HIV-1). Monocyte-tropic and lymphocyte-tropic strains of HIV-1 show distinctive patterns of replication in a panel of cell types. Journal of Experimental Medicine 170:1149–1163
     [Google Scholar]
  10. de Jong J.-J., Goudsmit J., Keulen W., Klaver B., Krone W., Tersmette M., de Ronde A. 1992; Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium formation and replication capacity. Journal of Virology 66:757–765
     [Google Scholar]
  11. Fenyo E. M., Morfeldt-Manson L., Chiodi F., Lind B., von Gegerfelt A., Olausson E., Asjo B. 1988; Distinct replication and cytopathic characteristics of human immunodeficiency virus isolates. Journal of Virology 62:4414–4419
     [Google Scholar]
  12. 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
     [Google Scholar]
  13. Gendelman H. E., Orenstein J. M., Martin M. A., Ferrua C., Mitra R., Phipps T., Wahl L. A., Lane H. C., Fauci A. S., Burke D. S., Skillman D., Meltzer M. S. 1988; Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes. Journal of Experimental Medicine 167:1428–1441
     [Google Scholar]
  14. Gendelman H. E., Baca L. M., Husayni H., Turpin J. A., Skillman D., Kalter D. C., Orenstein J. M., Hoover D. L., Meltzer M. S. 1990; Macrophage-HIV interaction: viral isolation and target cell tropism. AIDS 4:221–228
     [Google Scholar]
  15. Grimaila R. J., Fuller B. A., Rennert P. D., Nelson M.B, Potts B., Murray M., Putney S. D., Gray G. 1992; Mutations in the principal neutralization determinant of human immunodeficiency virus type 1 affect syncytium formation, virus infectivity, growth kinetics and neutralization. Journal of Virology 66:1875–1883
     [Google Scholar]
  16. Hattori T., Michaels F., Fargnoli K., Marcon L., Gallo R. C., Franchini G. 1990; The human immunodeficiency virus type 2 vpr gene is essential for productive infection of human macrophages. Proceedings of the National Academy of Sciences, U.S.A 87:8080–8084
     [Google Scholar]
  17. Hwang S. S., Boyle T. J., Lyerly H. K., Cullen B. R. 1991; Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 253:71–73
     [Google Scholar]
  18. Ivey-Hoyle M., Culp J. S., Chaikin M. A., Hellmig B. D., Matthews T. J., Sweet R. W., Rosenberg M. 1991; Envelope glycoproteins from biologically diverse isolates of human immunodeficiency viruses have widely different affinities for CD4. Proceedings of the National Academy of Sciences, U.S.A 88:512–516
     [Google Scholar]
  19. Koyanagi Y., Miles S., Mitsuyasu R. T., Merrill J. E., Vinters H. V., Chen I. S. Y. 1987; Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236:819–822
     [Google Scholar]
  20. Kusumi K., Conway B., Cunningham S., Berson A., Evans C., Iversen A. K. N., Colvin D., Gallo M. V., Coutre S., Shpaer E. G., Fulkener D. V., de Ronde A., Volkman S., Williams C., Hirsch M. S., Mullins J. I. 1992; Human immunodeficiency virus type 1 envelope gene structure and diversity in vivo and after cocultivation in vitro. Journal of Virology 66:875–885
     [Google Scholar]
  21. Liu Z.-Q., Wood C., Levy J. A., Cheng-Mayer C. 1990; The viral envelope gene is involved in macrophage tropism of a human immunodeficiency virus type 1 strain isolated from brain tissue. Journal of Virology 64:6148–6153
     [Google Scholar]
  22. Mcdougal J. S., Cort S. P., Kennedy M. S., Cabradilla C. D., Feorini P. M., Francis D. P., Hicks D., Kalyanaraman V. S., Martin L. S. 1985; Immunoassay for the detection and quantification of infectious human retrovirus, lymphadenopathy-associated virus (LAV). Journal of Immunological Methods 16:171–183
     [Google Scholar]
  23. Massari F. E., Poli G., Schnittman S. M., Psallidopolous M. C., Davey V., Fauci A. S. 1990; In vivo T lymphocyte origin of macrophage tropic strains of HIV. Role of monocytes during in vitro isolation and in vivo infection. Journal of Immunology 144:4628–4632
     [Google Scholar]
  24. Meyerhans A., Cheynier R., Albert J., Seth M., Kwok S., Sninsky J., Morfeldt-Manson L., Asjo B., Wain-Hobson S. 1989; Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell 58:901–910
     [Google Scholar]
  25. Moore J. P., Mckeating J. A., Weiss R. A., Sattentau Q. J. 1990; Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 250:1139–1142
     [Google Scholar]
  26. Moore J. P., Mckeating J. A., Huang Y., Ashkenazi A., Ho D. D. 1992; Virions of primary human immunodeficiency virus type 1 isolates resistant to soluble CD4 (sCD4) neutralization differ in sCD4 binding and glycoprotein gp120 retention from sCD4-sensitive isolates. Journal of Virology 66:235–243
     [Google Scholar]
  27. O’Brien W. A., Koyanagi Y., Namazie A., Zhao J.-Q., Diagne A., Idler K., Zack J. A., Chen I. S. Y. 1990; HIV-1 tropism for mononuclear phagocytes can be determined by regions of gpl20 outside the CD4-binding domain. Nature; London: 34869–73
     [Google Scholar]
  28. Orenstein J. M., Meltzer M. S., Phipps T., Gendelman H. E. 1988; Cytoplasmic assembly and accumulation of human immunodeficiency virus types 1 and 2 in recombinant human colony- stimulating factor-1 treated human monocytes: an ultrastructural study. Journal of Virology 62:2578–2586
     [Google Scholar]
  29. Pang S., Koyanagi Y., Miles S., Wiley C., Vinters H. V., Chen I. S. Y. 1990; High levels of unintegrated HIV-1 DNA in brain tissue of AIDS dementia patients. Nature; London: 34385–89
     [Google Scholar]
  30. Potash M. J., Zeira M., Huang Z.-B., Pearce T. E., Eden E., Gendelman H. E., Volsky D. J. 1992; Virus-cell membrane fusion does not predict efficient infection of alveolar macrophages by human immunodeficiency virus type 1 (HIV-1). Virology 188:864–868
     [Google Scholar]
  31. Reed L. J., Muench H. 1938; A simple method of estimating fifty percent endpoints. American Journal of Hygiene 27:493–497
     [Google Scholar]
  32. Salahuddin S. Z., Markham P. D., Wong-Staal F., Franchini G., Kalyanaraman V. S., Gallo R. C. 1983; Restricted expression of human T cell leukemia lymphoma virus (HTLV) in transformed human umbilical cord blood lymphocytes. Virology 129:51–64
     [Google Scholar]
  33. Schuitemaker H., Kootstra N. A., de Goede R. E. Y., de Wolf F., Meidema F., Tersmette M. 1991; Monocytotropic human immunodeficiency virus type 1 (HIV-1) variants detectable at all stages of HIV-1 infection lack T-cell line tropism and syncytium- inducing ability in primary T cell culture. Journal of Virology 65:356–363
     [Google Scholar]
  34. Schuitemaker H., Koot M., Koostra N. A., Derckson M. W., de Goede R. Y., Van Steenwijk R. P., Lange J. M. A., Schattenkerk J. K. M. E., Miedema F., Tersmette M. 1992; Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-tropic virus populations. Journal of Virology 66:1354–1360
     [Google Scholar]
  35. Shaw G. M., Hahn B. H., Arya S. K., Groopman J. E., Gallo R. C., Wong-Staal F. 1984; Molecular characterization of human T-cell leukemia (lymphotropic) virus type III B in the acquired immune deficiency syndrome. Science 226:1165–1171
     [Google Scholar]
  36. Shioda T., Levy J. A., Cheng-Mayer C. 1991; Macrophage and T-cell line tropisms of HIV-1 are determined by specific regions of the envelope gp120 gene. Nature; London: 349167–169
     [Google Scholar]
  37. Simon J. H. M., Somoza C., Schockmel G., Collin M., Williams A. F., James W. 1993; A rat CD4 mutant containing the gpl20- binding site mediates human immunodeficiency virus type 1 infection. Journal of Experimental Medicine 177:949–954
     [Google Scholar]
  38. Tersmette M., Gruters R. A., de Wolf F., de Goede R. Y., Lange J. M. A., Schellens P. T. A., Goudsmit J., Huisman H. G., Meidema F. 1989; Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential isolates. Journal of Virology 63:2118–2125
     [Google Scholar]
  39. Westervelt P., Gendelman H. E., Ratner L. 1991; Identification of a determinant within the human immunodeficiency virus 1 surface envelope glycoprotein critical for productive infection of primary monocytes. Proceedings of the National Academy of Sciences, U.S.A 88:3097–3101
     [Google Scholar]
  40. Westervelt P., Henkel T., Trowbridge D. B., Orenstein J., Gendelman H. E., Ratner L. 1992; Dual regulation of silent and productive infection in monocytes by distinct human immunodeficiency virus type 1 determinants. Journal of Virology 66:3925–3931
     [Google Scholar]
/content/journal/jgv/10.1099/0022-1317-75-7-1597
Loading
Definition of the range and distribution of human immunodeficiency virus macrophage tropism using PCR-based infectivity measurements
J. Gen. Virol. 75, 1597 (1994); https://doi.org/10.1099/0022-1317-75-7-1597
/content/journal/jgv/10.1099/0022-1317-75-7-1597
/content/journal/jgv/10.1099/0022-1317-75-7-1597
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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