1887

Abstract

The cell binding site of simian immunodeficiency virus (SIV) is believed to be the CD4 molecule. Several CD4 cell lines are, however, resistant to infection by SIV251 and additional cell membrane molecules have been implicated in SIV251 entry. We investigated the binding, envelope fusion and entry of the viral core proteins (p27) of SIV251 into two human CD4 cell lines (H9 and Sup-T1) which are infectible, and one CD4 (A3.01) and two CD4 cell lines (K562 and Raji) that are resistant to infection. The fusion of the viral and cellular membranes was monitored by a fluorescence assay for lipid mixing. Cell entry of the viral core was evaluated following virus-cell incubation and cell surface trypsinization. We found that SIV251 can bind to and fuse (membrane lipid mixing) in a temperature-dependent but pH-independent fashion with CD4 and CD4 human-derived cell lines. In contrast, lipid mixing with CD4 expressing EL-4 mouse T cells or Mv-1-lu mink lung fibroblasts was absent or limited, suggesting that certain components of human cell membranes in addition to CD4 are involved in SIV envelope-cell fusion. Lipid mixing with the human cells was inhibited partially by soluble CD4. Anti-CD4 antibodies inhibited the lipid inter-mixing with H9, but not with Raji cells, whereas neutralizing anti-SIV sera inhibited fusion with both CD4 and CD4 cells. Out of the five human cell lines tested, efficient entry of p27 and productive infection took place only with H9 and Sup-T1 cells. In these two cases, the amounts of p27 internalized during virus-cell fusion correlated with the extent of infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-74-6-1043
1993-06-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/74/6/JV0740061043.html?itemId=/content/journal/jgv/10.1099/0022-1317-74-6-1043&mimeType=html&fmt=ahah

References

  1. Agy M. B., Foy K., Gale M. J., Benveniste R. E., Clark E. A., Katze M. G. 1991; Viral and cellular gene expression in CD4+ human lymphoid cell lines infected by the simian immunodeficiency virus, SIV/Mne. Virology 183:170–180
    [Google Scholar]
  2. Allan J. S., Kanda P., Kennedy R. C., Cobb E. K., Anthony M., Eichberg J. W. 1990; Isolation and characterization of simian immunodeficiency viruses from two subspecies of African green monkeys. AIDS Research and Human Retroviruses 6:257–285
    [Google Scholar]
  3. Aloia R. C., Jensen F. C., Curtain C. C., Mobley P. W., Gordon L. M. 1988; Lipid composition and fluidity of the human immunodeficiency virus. Proceedings of the National Academy of Sciences, U.S.A. 85:900–904
    [Google Scholar]
  4. Benveniste R. E., Arthur L. O., Tsai C., Sowder R., Copeland T. D., Henderson L. E., Oroszlan S. 1986; Isolation of a lentivirus from a macaque with lymphoma: comparison with HTLV-III/LAV and other lentiviruses. Journal of Virology 60:483–490
    [Google Scholar]
  5. Benveniste R. E., Morton W. R., Clark E. A., Tsai C.-C., Ochs H. D., Ward J. M., Kuller L., Knott W. B., Hill R. W., Gale M. J., Thoulass M. E. 1988; Inoculation of baboons and macaques with simian immunodeficiency virus/Mne, a primate lentivirus closely related to human immunodeficiency virus type 2. Journal of Virology 62:2091–2101
    [Google Scholar]
  6. Centers for Disease Control 1988; 1988 Agent summary statement for human immunodeficiency virus and report on laboratory-acquired infection with human immunodeficiency virus. Morbidity and Mortality Weekly Report 37:supplement S-41–17
    [Google Scholar]
  7. Chakrabarti L., Guyader M., Alizon M., Daniel M. D., Desrosiers R. C., Tiollais P., Sonigo P. 1987; Sequence of simian immunodeficiency virus from macaque and its relationship to the other human and simian retroviruses. Nature, London 328:543–547
    [Google Scholar]
  8. Clapham P. R., Weber J. N., Whitby D., , McIntosh K., Dalgleish A. G., Maddon P. J., Deen K. C., Sweet R. W., Weiss R. A. 1989; Soluble CD4 blocks the infectivity of diverse strains of HIV and SIV for T cells and monocytes but not for brain and muscle cells. Nature, London 26:368–370
    [Google Scholar]
  9. Clapham P. R., Blanc D., Weiss R. A. 1991; Specific cell surface requirements for the infection of CD4-positive cells by human immunodeficiency virus types 1 and 2 and by simian immunodeficiency virus. Virology 181:703–715
    [Google Scholar]
  10. Dalgleish A. G., Beverly P. C. L., Clapham P. R., Crawford D. H., Greaves M. F., Weiss R. A. 1984; The CD4 (T-4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature, London 312:763–766
    [Google Scholar]
  11. Daniel M. D., Letvin N. L., King N. W., Kannagi M., Sehgal P. K., Hunt R. D., Kanki P. J., Essex M., Desrosiers R. C. 1985; Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science 228:1201–1204
    [Google Scholar]
  12. Dietrich U., Adamski M., Kreutz R., Seipp A., Kühnel H., Rübsamen-Waigmann H. 1989; A highly divergent HIV-2-related isolate. Nature, London 342:948–950
    [Google Scholar]
  13. Dimitrov D. S., Golding H., Blumenthal R. 1991; Initial stages of HIV-1 envelope glycoprotein-mediated cell fusion monitored by a new assay based on redistribution of fluorescent dyes. AIDS Research and Human Retroviruses 10:799–805
    [Google Scholar]
  14. Düzgüneş N. 1985; Membrane fusion. Subcellular Biochemistry 11:195–286
    [Google Scholar]
  15. Düzgüneş N., Bentz J. 1988; Fluorescence assays for membrane fusion. In Spectroscopic Membrane Probes vol. 1 pp. 117–159 Edited by Loew L. M. Boca Raton: CRC Press;
    [Google Scholar]
  16. Düzgüneş N., Pedroso de Lima M. C., Stamatatos L., Flasher D., Alford D., Friend D. S., Nir S. 1992; Fusion activity and inactivation of influenza virus: kinetics of low pH-induced fusion with cultured cells. Journal of General Virology 73:27–37
    [Google Scholar]
  17. Franchini G., Gurgo C., Guo C. H.-G., Gallo R. C., Collalti E., Fargnoli K. A., Hall L. F., Wong-Staal F., Reitz M. S. Jr 1987; Sequence of simian immunodeficiency virus and its relationship to the human immunodeficiency viruses. Nature, London 328:539–542
    [Google Scholar]
  18. Fults P. N., McClure H. M., Anderson D. C., Swenson R. B., Anand R., Srinivasan A. 1986; Isolation of a T-lymphotropic retrovirus from naturally infected sooty mangabeys (Cercocebus atys). Proceedings of the National Academy of Sciences, U.S.A. 83:5286–5290
    [Google Scholar]
  19. Gilbert M. J., Mason D., White J. M. 1990; Fusion of Rous sarcoma virus with host cells does not require exposure to low pH. Journal of Virology 64:5106–5113
    [Google Scholar]
  20. Grewe C., Beck A., Gelderblom H. R. 1990; HIV: early viruscell interactions. Journal of Acquired Immune Deficiency Syndromes 3:965–974
    [Google Scholar]
  21. Harouse J. M., Laughlin M. A., Pletcher C., Friedman H. M., Gonzalez-Scarano F. 1991a; Entry of human immunodeficiency virus-1 into glial cells proceeds via an alternate, efficient pathway. Journal of Leukocyte Biology 49:605–609
    [Google Scholar]
  22. Harouse J. M., Bhat S., Spitalnik S. L., Laughlin M., Stefano K., Silberberg D. H., Gonzalez-Scarano F. 1991b; Inhibition of entry of HIV-1 in neural cell lines by antibodies against galactosyl ceramide. Science 253:320–323
    [Google Scholar]
  23. Herrmann A., Clague M. J., Puri A., Morris S. J., Blumenthal R., Grimaldi S. 1990; Effect of erythrocyte transbilayer phospholipid distribution on fusion with vesicular stomatitis virus. Biochemistry 29:4054–4058
    [Google Scholar]
  24. Hoekstra D. 1990; Membrane fusion of enveloped viruses: especially a matter of proteins. Journal of Bioenergetics and Biomembranes 22:121–155
    [Google Scholar]
  25. Hoekstra D., Klappe K. 1986; Sendai virus-erythrocyte membrane interaction: quantitative and kinetic analysis of viral binding, dissociation, and fusion. Journal of Virology 58:87–95
    [Google Scholar]
  26. Hoekstra D., De Boer T., Klappe K., Wilschut J. 1984; Fluorescence method for measuring the kinetics of fusion between biological membranes. Biochemistry 23:5675–5681
    [Google Scholar]
  27. Hoekstra D., Klappe K., Hoff H., Nir S. 1989; Mechanism of fusion of Sendai virus: role of hydrophobic interactions and mobility constraints of viral membrane proteins. Journal of Biological Chemistry 264:6786–6792
    [Google Scholar]
  28. Hoxie J. A., Haggarty B. S., Bonser S. E., Rackowski J. L., Shan H., Kanki P. J. 1988; Biological characterization of a simian immunodeficiency virus-like retrovirus (HTLV-IV): evidence for CD4-associated molecules required for infection. Journal of Virology 62:2557–2568
    [Google Scholar]
  29. Kanki P. J., McLane M. F., King N. W. Jr, Letvin N. L., Hunt R. D., Sehgal P., Daniel M. D., Desrosiers R. C., Essex M. 1985; Serologic identification and characterization of a macaque T-lymphotropic retrovirus closely related to HTLV-III. Science 228:1199–1201
    [Google Scholar]
  30. Kannagi M., Yetz J. M., Letvin N. L. 1985; In vitro growth characteristics of simian T-lymphotropic virus type III. Proceedings of the National Academy of Sciences, U.S.A. 82:7053–7057
    [Google Scholar]
  31. Klatzmann D., Champagne E., Chamaret S., Gruest J., Guetard D., Hercend T., Gluckman J.-C., Montagnier L. 1984; T-lymphocyte T4 molecule behaves as the receptor for the human retrovirus LAV. Nature, London 312:767–768
    [Google Scholar]
  32. Koenig S., Hirsch V. M., Olmsted R. A., Powell D., Maury W., Rabson A., Fauci A. S., Purcell R. H., Johnson P. R. 1989; Selective infection of human CD4+ cells by simian immunodeficiency virus: productive infection associated with envelope glycoprotein-induced fusion. Proceedings of the National Academy of Sciences, U.S.A. 86:2443–2447
    [Google Scholar]
  33. Konopka K., Davis B. R., Larsen C. E., Alford D. R., Debs R. J., Düzgüneş N. 1990; Liposomes modulate human immunodeficiency virus infectivity. Journal of General Virology 71:2899–2907
    [Google Scholar]
  34. Kunsch C., Wigdahl B. 1991; Maintenance of human immunodeficiency virus type-1 proviral DNA in human fetal dorsal root ganglia neural cells following a nonproductive infection. Journal of Leukocyte Biology 49:505–510
    [Google Scholar]
  35. Lackner A. A., Smith M. O., Munn R. J., Martfeld D. J., Gardner M. B., Marx P. A., Dandekar S. 1991; Localization of simian immunodeficiency virus in the central nervous system of rhesus monkeys. American Journal of Pathology 139:609–621
    [Google Scholar]
  36. Langhoff E., Terwilliger E. F., Bos H. J., Kalland K. H., Poznansky M. C., Bacon O. M. L., Haseltine W. A. 1991; Replication of human immunodeficiency virus type 1 in primary dendritic cell cultures. Proceedings of the National Academy of Sciences, U.S.A. 88:7998–8002
    [Google Scholar]
  37. Larsen C. E., Alford D. R., Young L. J. T., McGraw T. P., Düzgüneş N. 1990; Fusion of simian immunodeficiency virus with liposomes and erythrocyte ghost membranes: effects of lipid composition, pH and calcium. Journal of General Virology 71:1947–1955
    [Google Scholar]
  38. Lima M. C. P., Nir S., Flasher D., Klappe K., Hoekstra D., Düzgüneş N. 1991; Kinetics of fusion of Sendai virus with human HL-60 and CEM cells. Biochimica et biophysica acta 1070:446–454
    [Google Scholar]
  39. Lowenstine L. J., Pedersen N. C., Higgins J., Pallis K. C., Uyeda A., Marx P. A., Lerche N. W., Munn R. J., Gardner M. B. 1986; Seroepidemiologic survey of captive Old World primates for antibodies to human and simian retroviruses. Isolation of lentivirus from sooty mangabeys (Cercocebus atys). International Journal of Cancer 38:563–575
    [Google Scholar]
  40. Lowy R. J., Sarkar D. P., Blumenthal R. 1992; Influenza viruscell fusion: observations of protein and lipid movements using low-light-level fluorescent video microscopy. Journal of Cellular Biochemistry supplement 16C:131
    [Google Scholar]
  41. Maddon P. J., McDougal J. S., Clapham P. R., Dalgleish A. G., Jamal S., Weiss R. A., Axel R. 1988; HIV infection does not require endocytosis of its receptor. Cell 54:865–874
    [Google Scholar]
  42. Marsh M., Helenius A. 1989; Virus entry into animal cells. Advances in Virus Research 36:107–151
    [Google Scholar]
  43. Matlin K., Reggio H., Helenius A., Simons K. 1981; The infective entry of influenza virus into MDCK cells. Journal of Cell Biology 91:601–613
    [Google Scholar]
  44. McClure M. O., Marsh M., Weiss R. A. 1988; Human immunodeficiency virus infection of CD4-bearing cells occurs by a pH-independent mechanism. EM BO Journal 1:513–518
    [Google Scholar]
  45. McDougal J. S., Mawle A., Cort S. P., Nicholson J. K. A., Gross G. D., Scheppler-Campbell J. A., Hicks D., Sligh J. 1985; Cellular tropism of the human retrovirus HTLV-III/LAV. Journal of Immunology 135:3151–3161
    [Google Scholar]
  46. Moore J. P., McKeating J. A., Weiss R. A., Sattentau Q. J. 1990; Dissociation of gpl20 from HIV-1 virions induced by soluble CD4. Science 250:1139–1142
    [Google Scholar]
  47. Moyer M. P., Gendelman H. E. 1991; HIV replication and persistence in human gastrointestinal cells cultured in vitro. Journal of Leukocyte Biology 49:499–504
    [Google Scholar]
  48. Murphey-Corb M., Martin L. N., Rangan S. R. S., Baskin G. B., Gormus B. J., Wolf R. H., Andes W. A., West M. 1986; Isolation of an HTLV-III related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature, London 321:435–137
    [Google Scholar]
  49. Nir S., Klappe K., Hoekstra D. 1986; Kinetics and extent of fusion between Sendai virus and erythrocyte ghosts: application of a mass action kinetic model. Biochemistry 25:2155–2161
    [Google Scholar]
  50. 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]
  51. Sinangil F., Loyter A., Volsky D. J. 1988; Quantitative measurement of fusion between human immunodeficiency virus and cultured cells using membrane fluorescence dequenching. FEBS Letters 239:88–92
    [Google Scholar]
  52. Srinivasakumar N., Ogra P. L., Flanagan T. D. 1991; Characteristics of fusion of respiratory syncytial virus with HEp-2 cells as measured by R18 fluorescence dequenching assay. Journal of Virology 65:4063–4069
    [Google Scholar]
  53. Stamatatos L., Düzgüneş N. 1992; Interaction of simian immunodeficiency virus with CD4+ and CD4- cells: envelope fusion, p27 entry and infectivity. Journal of Cellular Biochemistry supplement 16C:125
    [Google Scholar]
  54. Stegmann T., Booy F. P., Wilschut J. 1987; Effects of low pH on influenza virus. Activation and inactivation of the membrane fusion capacity of the hemagglutinin. Journal of Biological Chemistry 262:17744–17749
    [Google Scholar]
  55. Stegmann T., Doms R. W., Helenius A. 1989; Protein-mediated membrane fusion. Annual Review of Biophysics and Biophysical Chemistry 18:187–211
    [Google Scholar]
  56. Stein B. S., Gowda S. D., Lifson J. D., Penhallow R. C., Bensch K. G., Engleman E. G. 1987; pH-independent HIV entry into CD4-positive cells via virus envelope fusion to the plasma membrane. Cell 49:659–668
    [Google Scholar]
  57. Tang S., Levy J. 1991; Inactivation of HIV-1 by trypsin and its use in demonstrating specific virus infection of cells. Journal of Virological Methods 33:39–46
    [Google Scholar]
  58. Tateno M., Gonzalez-Scarano F., Levy J. A. 1989; Human immunodeficiency virus can infect CD4-negative human fibro-blastoid cells. Proceedings of the National Academy of Sciences, U.S.A. 86:4287–4290
    [Google Scholar]
  59. Volsky D. J. 1990; Fusion of human immunodeficiency virus type (HIV-1) with human cells as measured by membrane fluorescence dequenching (DQ) method: roles of HIV-1 cell fusion in AIDS pathogenesis. In Horizons in Membrane Biotechnology pp. 179–198 Edited by Nicolau C., Chapman D. New York: Wiley-Liss;
    [Google Scholar]
  60. Yahi N., Baghdiguian S., Moreau H., Fantini J. 1992; Galactosyl ceramide (or a closely related molecule) is the receptor for human immunodeficiency virus type 1 on human colon epithelial HT29 cells. Journal of Virology 66:4848–1854
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-74-6-1043
Loading
/content/journal/jgv/10.1099/0022-1317-74-6-1043
Loading

Data & Media loading...

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