1887

Abstract

In order to test the hypothesis that macrophages and dendritic cells (DCs) in mucosal tissue play an important role in heterosexual transmission of human immunodeficiency virus, the replication capacities of two simian immunodeficiency viruses (SIVs) were examined in cultured macrophages and DCs as well as in cultured PBMCs . The virus strains were a T cell-tropic SIV, SIVmac239, and a T cell- and macrophage-tropic (dual-tropic) SIV, SIVmac239/316E. The infectivities of these viruses to cynomolgus macaques by intravaginal inoculation were also compared. Although both virus strains replicated well in cultured PBMCs, SIVmac239 did not replicate in cultured macrophages, whereas SIVmac239/316E did. Both strains showed little replication in cultured DCs, but a high virus yield could be obtained when SIVmac239/316E-infected DCs were co-cultured with uninfected PBMCs. A mixture of these SIVs was inoculated intravaginally to three monkeys and the virus strain that first appeared through the vaginal mucosa was determined. The virus clones detected first in PBMCs, inguinal lymph nodes and vaginal wash cells (VWCs) after the virus inoculation were of SIVmac239 in all cases, except for one clone of SIVmac239/316E in VWCs of one monkey at one time-point. These results show that the infectivity of the virus in intravaginal transmission did not depend on the cell tropism in vitro of the virus.

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1999-04-01
2024-03-29
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References

  1. Barratt-Boyes S. M., Henderson R. A., Finn O. J. 1996; Chimpanzee dendritic cells with potent immunostimulatory function can be propagated from peripheral blood. Immunology 87:528–534
    [Google Scholar]
  2. Berger E. A., Doms R. W., Fenyo E. M., Korber B. T., Littman D. R., Moore J. P., Sattentau Q. J., Schuitemaker H., Sodroski J., Weiss R. A. 1998; A new classification for HIV-1. Nature 391:240
    [Google Scholar]
  3. Blauvelt A., Asada H., Saville M. W., Klaus-Kovtun V., Altman D. J., Yarchoan R., Katz S. I. 1997; Productive infection of dendritic cells by HIV-1 and their ability to capture virus are mediated through separate pathways. Journal of Clinical Investigation 100:2043–2053
    [Google Scholar]
  4. Bomsel M. 1997; Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nature Medicine 3:42–47
    [Google Scholar]
  5. Chen Z., Zhou P., Ho D. D., Landau N. R., Marx P. A. 1997; Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. Journal of Virology 71:2705–2714
    [Google Scholar]
  6. Chen J., Ido E., Jin M., Kuwata T., Igarashi T., Mizuno A., Koyanagi Y., Hayami M. 1998; Replication of human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus strain mac (SIVmac) and chimeric HIV-l/SIVmac viruses having env genes derived from macrophage-tropic viruses: an indication of different mechanisms of macro- phage-tropism in human and monkey cells. Journal of General Virology 79:741–745
    [Google Scholar]
  7. Choe H., Farzan M., Sun Y., Sullivan N., Rollins B., Ponath P. D., Wu L., Mackay C. R., LaRosa G., Newman W., Gerard N., Gerard C., Sodroski J. 1996; The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135–1148
    [Google Scholar]
  8. Deng H., Liu R., Ellmeir W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R. E., Hill C. M., Davis C. B., Peiper S. C., Schall T. J., Littman D. R., Landau N. R. 1996; Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661–666
    [Google Scholar]
  9. Dittmar M. T., Simmons G., Hibbitts S., O’Hare M., Louisirirotchan- akul S., Beddows S., Weber J., Clapham P. R., Weiss R. A. 1997; Langerhans cell tropism of human immunodeficiency virus type 1 subtype A through F isolates derived from different transmission groups. Journal of Virology 71:8008–8013
    [Google Scholar]
  10. Doranz B. J., Rucker J., Yi Y., Smyth R. J., Samson M., Peiper S. C., Parmentier M., Collman R. G., Doms R. W. 1996; A dual-tropic HIV-1 isolate that uses fusin and the β-chemokine receptors CKR-5, CKR- 3 and CKR-2b as fusion cofactors. Cell 85:1149–1158
    [Google Scholar]
  11. Dragic T., Litwin V., Allaway G., Martin S. R., Huang Y., Nagashima K. A., Cayanan C., Maddon P. J., Koup R. A., Moore J. P., Paxton W. A. 1996; HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667–673
    [Google Scholar]
  12. Edinger A. L., Amedee A., Miller K., Doranz B. J., Endres M., Sharron M., Samson M., Lu Z. H., Clements J. E., Murphey-Corb M., Peiper S. C., Parmentier M., Broder C. C., Doms R. W. 1997; Differential utilization of CCR5 by macrophage and T cell tropic simian immunodeficiency virus strains. Proceedings of the National Academy of Sciences, USA 94:4005–4010
    [Google Scholar]
  13. Edinger A. L., Hoffman T. L., Sharron M., Lee B., O’Dowd B., Doms R. W. 1998; Use of GPR1, GPR15, and STRL33 as coreceptors by diverse human immunodeficiency virus type 1 and simian immunodeficiency virus envelope proteins. Virology 249:367–378
    [Google Scholar]
  14. Enose Y., Okada M., Sata T., Ma W., Igarashi T., Ibuki K., Ido E., Hayami M. 1997; Restriction of viral population by intravaginal infection of simian immunodeficiency viruses in macaque monkeys. Archives of Virology 142:37–51
    [Google Scholar]
  15. 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 272:872–876
    [Google Scholar]
  16. Frankel S. S., Wenig B. M., Burke A. P., Mannan P., Thompson L. D., Abbondanzo S. L., Nelson A. M., Pope M., Steinman R. M. 1996; Replication of HIV-1 in dendritic cell-derived syncytia at the mucosal surface of the adenoid. Science 272:115–117
    [Google Scholar]
  17. Granelli-Piperno A., Moser B., Pope M., Chen D., Wei Y., Isdell F., O’Doherty U., Paxton W., Koup R., Mojsov S., Bhardwaj N., Clark- Lewis I., Baggiolini M., Steinman R. M. 1996; Efficient interaction of HIV-1 with purified dendritic cells via multiple chemokine coreceptors. Journal of Experimental Medicine 184:2433–2438
    [Google Scholar]
  18. Harouse J. M., Tan R. C. H., Gettie A., Dailey P., Marx P. A., Luciw P. A., Cheng-Mayer C. 1998; Mucosal transmission of pathogenic CXCR4-utilizing SHIVSF33A variants in rhesus macaques. Virology 248:95–107
    [Google Scholar]
  19. Kestler H., Kodama T., Ringler D., Marthas M., Pedersen N., Lackner A., Regier D., Sehgal P., Daniel M., King N., Desrosiers R. 1990; Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 248:1109–1111
    [Google Scholar]
  20. Kirchhoff F., Pöhlmann S., Hamacher M., Means R. E., Kraus T., Uberla K., Di Marzio P. 1997; Simian immunodeficiency virus variants with differential T-cell and macrophage tropism use CCR5 and an unidentified cofactor expressed in CEMx174 cells for efficient entry. Journal of Virology 71:6509–6516
    [Google Scholar]
  21. Lehner T., Wang Y., Cranage M., Bergmeier L. A., Mitchell E., Tao L., Hall G., Dennis M., Cook N., Brookes R., Klavinskis L., Jones I., Doyle C., Ward R. 1996; Protective mucosal immunity elicited by targeted iliac lymph node immunization with a subunit SIV envelope and core vaccine in macaques. Nature Medicine 2:767–775
    [Google Scholar]
  22. Lohman B. L., Miller C. J., McChesney M. B. 1995; Antiviral cytotoxic T lymphocytes in vaginal mucosa of simian immunodeficiency virus-infected rhesus macaque. Journal ofImmunology 155:5855–5860
    [Google Scholar]
  23. Lu Y., Brosio P., Lafaile M., Li J., Collman R. G., Sodroski J., Miller C. J. 1996; Vaginal transmission of chimeric simian/human immunodeficiency viruses in rhesus macaques. Journal of Virology 70:3045–3050
    [Google Scholar]
  24. Marx P. A., Spira A. I., Gettie A., Dailey P. J., Veazey R. S., Lackner A. A., Mahoney C. J., Miller C. J., Claypool L. E., Ho D. D., Alexander N. J. 1996; Progesterone implants enhance SIV vaginal transmission and early virus load. Nature Medicine 2:1084–1089
    [Google Scholar]
  25. Miller C. J., Alexander N. J., Sutjipto S., Lackner A. A., Gettie A., Hendrickx A. G., Lowenstine L. J., Jennings M., Marx P. A. 1989; Genital mucosal transmission of simian immunodeficiency virus: animal model for heterosexual transmission of human immunodeficiency virus. Journal of Virology 63:4277–4284
    [Google Scholar]
  26. Miller C. J., McGhee J. R., Gardner M. B. 1993; Mucosal immunity, HIV transmission, and AIDS. Laboratory Investigation 68:129–145
    [Google Scholar]
  27. Miller C. J., Marthas M., Greenier J., Lu D., Dailey P. J., Lu Y. 1998; In vivo replication capacity rather than in vitro macrophage tropism predicts efficiency of vaginal transmission of simian immunodeficiency virus or simian/human immunodeficiency virus in rhesus macaques. Journal of Virology 72:3248–3258
    [Google Scholar]
  28. Mori K., Ringler D. J., Kodama T., Desrosiers R. C. 1992; Complex determinants of macrophage tropism in env of simian immunodeficiency virus. Journal of Virology 66:2067–2075
    [Google Scholar]
  29. Mori K., Ringler D. J., Desrosiers R. C. 1993; Restricted replication of simian immunodeficiency virus strain 239 in macrophages is determined by env but is not due to restricted entry. Journal of Virology 67:2807–2814
    [Google Scholar]
  30. O’Doherty U., Ignatius R., Bhardwaj N., Pope M. 1997; Generation of monocyte-derived dendritic cells from precursors in rhesus macaque blood. Journal of Immunological Methods 207:185–194
    [Google Scholar]
  31. Pope M., Betjes M. G. H., Romani N., Hirmand H., Cameron P. U., Hoffman L., Gezelter S., Schuler G., Steinman R. M. 1994; Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1. Cell 78:389–398
    [Google Scholar]
  32. Pope M., Frankel S. S., Mascola J. R., Trkola A., Isdell F., Birx D. L., Burke D. S., Ho D. D., Moore J. P. 1997a; Human immunodeficiency virus type 1 strains of subtypes B and E replicate in cutaneous dendritic cell-T-cell mixtures without displaying subtype-specific tro-pism. Journal of Virology 71:8001–8007
    [Google Scholar]
  33. Pope M., Elmore D., Ho D., Marx P. 1997b; Dendrite cell-T cell mixtures, isolated from the skin and mucosae of macaques, support the replication of SIV. AIDS Research and Human Retroviruses 13:819–827
    [Google Scholar]
  34. Soto-Ramirez R. E., Renjifo B., McLane M. F., Marlink R., O’Hara C., Sutthent R., Wasi C., Vithayasai P., Vithayasai V., Apichartpiyakul C., Auewarakul P., Pena Cruz V., Chui D. S., Osathanondh R., Mayer K., Lee T. H., Essex M. 1996; HIV-1 Langerhans’ cells tropism associated with heterosexual transmission of HIV. Science 271:1291–1293
    [Google Scholar]
  35. Spira A. I., Marx P. A., Patterson B. K., Mahoney J., Koup R. A., Wolinsky S. M., Ho D. D. 1996; Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. Journal of Experimental Medicine 183:215–225
    [Google Scholar]
  36. Trivedi P., Meyer K. K., Streblow D. N., Preuninger B. L., Schultz K. T., Pauza C. D. 1994; Selective amplification of simian immunodeficiency virus genotypes after intrarectal inoculation of rhesus monkeys. Journal of Virology 68:7649–7653
    [Google Scholar]
  37. Trivedi P., Horejsh D., Hinds S. B., Hinds P. W. II, Wu M. S., Salvato M. S., Pauza C. D. 1996; Intrarectal transmission of simian immunodeficiency virus in rhesus macaques: selective amplification and host responses to transient or persistent viremia. Journal of Virology 70:6876–6883
    [Google Scholar]
  38. Tsunetsugu-Yokota Y., Akagawa K., Kimoto H., Suzuki K., Iwasaki M., Yasuda S., Hausser G., Hultgren C., Meyerhans A., Takemori T. 1995; Monocyte-derived cultured dendritic cells are susceptible to human immunodeficiency virus infection and transmit virus to resting T cells in the process of nominal antigen presentation. Journal of Virology 69:4544–4547
    [Google Scholar]
  39. Willey R. L., Smith D. H., Lasky L. A., Theodore T. S., Earl P. L., Moss B., Capon D. J., Martin M. A. 1988; In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. Journal of Virology 62:139–147
    [Google Scholar]
  40. Zaitseva M., Blauvelt A., Lee S., Lapham C. K., Klaus-Kovtun V., Mostowski H., Manischewitz J., Golding H. 1997; Expression and function of CCR5 and CXCR4 on human Langerhans cells and macrophages: implications for HIV primary infection. Nature Medicine 3:1369–1375
    [Google Scholar]
  41. Zhang L. Q., MacKenzie P., Cleland A., Holmes E. C., Brown A. J., Simmonds P. 1993; Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. Journal of Virology 67:3345–3356
    [Google Scholar]
  42. Zhu T., Mo H., Wang N., Nam D. S., Cao Y., Koup R. A., Ho D. D. 1993; Genotypic and phenotypic characterization of HIV-1 in patients with primary infection. Science 261:1179–1181
    [Google Scholar]
  43. Zhu T., Wang N., Carr A., Nam D. S., Moor-Jankowski R., Cooper D. A., Ho D. D. 1996; Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: evidence for viral compartmentalization and selection during sexual transmission. Journal of Virology 703098–3107
    [Google Scholar]
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