Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1997 Oct;71(10):8001–8007. doi: 10.1128/jvi.71.10.8001-8007.1997

Human immunodeficiency virus type 1 strains of subtypes B and E replicate in cutaneous dendritic cell-T-cell mixtures without displaying subtype-specific tropism.

M Pope 1, S S Frankel 1, J R Mascola 1, A Trkola 1, F Isdell 1, D L Birx 1, D S Burke 1, D D Ho 1, J P Moore 1
PMCID: PMC192162  PMID: 9311895

Abstract

A report that genetic subtype E human immunodeficiency virus type 1 (HIV-1) strains display a preferential tropism for Langerhans cells (epidermal dendritic cells [DCs]) compared to genetic subtype B strains suggested a possible explanation for the rapid heterosexual spread of subtype E strains in Thailand (L. E. Soto-Ramirez et al., Science 271:1291-1293, 1996). In an independent system, we applied subtype E and B isolates to skin leukocytes, since skin is a relevant model for the histologically comparable surfaces of the vagina and ectocervix. Isolates of both HIV-1 subtypes infected DC-T-cell mixtures, and no subtype-specific pattern of infection was observed. Purified DCs did not support the replication of strains of either subtype B or E. Our findings do not support the conclusion that subtype E strains have a preferential tropism for DCs, suggesting that other explanations for the rapid heterosexual spread of subtype E strains in Asia should be considered.

Full Text

The Full Text of this article is available as a PDF (289.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Artenstein A. W., VanCott T. C., Mascola J. R., Carr J. K., Hegerich P. A., Gaywee J., Sanders-Buell E., Robb M. L., Dayhoff D. E., Thitivichianlert S. Dual infection with human immunodeficiency virus type 1 of distinct envelope subtypes in humans. J Infect Dis. 1995 Apr;171(4):805–810. doi: 10.1093/infdis/171.4.805. [DOI] [PubMed] [Google Scholar]
  2. Austyn J. M., Kupiec-Weglinski J. W., Hankins D. F., Morris P. J. Migration patterns of dendritic cells in the mouse. Homing to T cell-dependent areas of spleen, and binding within marginal zone. J Exp Med. 1988 Feb 1;167(2):646–651. doi: 10.1084/jem.167.2.646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ayehunie S., Groves R. W., Bruzzese A. M., Ruprecht R. M., Kupper T. S., Langhoff E. Acutely infected Langerhans cells are more efficient than T cells in disseminating HIV type 1 to activated T cells following a short cell-cell contact. AIDS Res Hum Retroviruses. 1995 Aug;11(8):877–884. doi: 10.1089/aid.1995.11.877. [DOI] [PubMed] [Google Scholar]
  4. Berger R., Gartner S., Rappersberger K., Foster C. A., Wolff K., Stingl G. Isolation of human immunodeficiency virus type 1 from human epidermis: virus replication and transmission studies. J Invest Dermatol. 1992 Sep;99(3):271–277. doi: 10.1111/1523-1747.ep12616619. [DOI] [PubMed] [Google Scholar]
  5. Bujdoso R., Hopkins J., Dutia B. M., Young P., McConnell I. Characterization of sheep afferent lymph dendritic cells and their role in antigen carriage. J Exp Med. 1989 Oct 1;170(4):1285–1301. doi: 10.1084/jem.170.4.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cameron P. U., Freudenthal P. S., Barker J. M., Gezelter S., Inaba K., Steinman R. M. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science. 1992 Jul 17;257(5068):383–387. doi: 10.1126/science.1352913. [DOI] [PubMed] [Google Scholar]
  7. Cameron P. U., Lowe M. G., Crowe S. M., O'Doherty U., Pope M., Gezelter S., Steinman R. M. Susceptibility of dendritic cells to HIV-1 infection in vitro. J Leukoc Biol. 1994 Sep;56(3):257–265. doi: 10.1002/jlb.56.3.257. [DOI] [PubMed] [Google Scholar]
  8. Cameron P., Pope M., Granelli-Piperno A., Steinman R. M. Dendritic cells and the replication of HIV-1. J Leukoc Biol. 1996 Feb;59(2):158–171. doi: 10.1002/jlb.59.2.158. [DOI] [PubMed] [Google Scholar]
  9. Charbonnier A. S., Mallet F., Fiers M. M., Desgranges C., Dezutter-Dambuyant C., Schmitt D. Detection of HIV-specific DNA sequences in epidermal Langerhans cells infected in vitro by means of a cell-free system. Arch Dermatol Res. 1994;287(1):36–41. doi: 10.1007/BF00370716. [DOI] [PubMed] [Google Scholar]
  10. Chesebro B., Wehrly K., Nishio J., Perryman S. Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. J Virol. 1992 Nov;66(11):6547–6554. doi: 10.1128/jvi.66.11.6547-6554.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Choe H., Farzan M., Sun Y., Sullivan N., Rollins B., Ponath P. D., Wu L., Mackay C. R., LaRosa G., Newman W. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell. 1996 Jun 28;85(7):1135–1148. doi: 10.1016/s0092-8674(00)81313-6. [DOI] [PubMed] [Google Scholar]
  12. Cáceres C. F., Hearst N. HIV/AIDS in Latin America and the Caribbean: an update. AIDS. 1996;10 (Suppl A):S43–S49. doi: 10.1097/00002030-199601001-00007. [DOI] [PubMed] [Google Scholar]
  13. Daniels T. E. Human mucosal Langerhans cells: postmortem identification of regional variations in oral mucosa. J Invest Dermatol. 1984 Jan;82(1):21–24. doi: 10.1111/1523-1747.ep12259038. [DOI] [PubMed] [Google Scholar]
  14. Dean M., Carrington M., Winkler C., Huttley G. A., Smith M. W., Allikmets R., Goedert J. J., Buchbinder S. P., Vittinghoff E., Gomperts E. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science. 1996 Sep 27;273(5283):1856–1862. doi: 10.1126/science.273.5283.1856. [DOI] [PubMed] [Google Scholar]
  15. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R. E., Hill C. M. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 1996 Jun 20;381(6584):661–666. doi: 10.1038/381661a0. [DOI] [PubMed] [Google Scholar]
  16. Doranz B. J., Rucker J., Yi Y., Smyth R. J., Samson M., Peiper S. C., Parmentier M., Collman R. G., Doms R. W. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell. 1996 Jun 28;85(7):1149–1158. doi: 10.1016/s0092-8674(00)81314-8. [DOI] [PubMed] [Google Scholar]
  17. Dragic T., Litwin V., Allaway G. P., Martin S. R., Huang Y., Nagashima K. A., Cayanan C., Maddon P. J., Koup R. A., Moore J. P. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature. 1996 Jun 20;381(6584):667–673. doi: 10.1038/381667a0. [DOI] [PubMed] [Google Scholar]
  18. Frankel S. S., Tenner-Racz K., Racz P., Wenig B. M., Hansen C. H., Heffner D., Nelson A. M., Pope M., Steinman R. M. Active replication of HIV-1 at the lymphoepithelial surface of the tonsil. Am J Pathol. 1997 Jul;151(1):89–96. [PMC free article] [PubMed] [Google Scholar]
  19. 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. Replication of HIV-1 in dendritic cell-derived syncytia at the mucosal surface of the adenoid. Science. 1996 Apr 5;272(5258):115–117. doi: 10.1126/science.272.5258.115. [DOI] [PubMed] [Google Scholar]
  20. Gebert A., Rothkötter H. J., Pabst R. M cells in Peyer's patches of the intestine. Int Rev Cytol. 1996;167:91–159. doi: 10.1016/s0074-7696(08)61346-7. [DOI] [PubMed] [Google Scholar]
  21. Granelli-Piperno A., Moser B., Pope M., Chen D., Wei Y., Isdell F., O'Doherty U., Paxton W., Koup R., Mojsov S. Efficient interaction of HIV-1 with purified dendritic cells via multiple chemokine coreceptors. J Exp Med. 1996 Dec 1;184(6):2433–2438. doi: 10.1084/jem.184.6.2433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Huang Y., Paxton W. A., Wolinsky S. M., Neumann A. U., Zhang L., He T., Kang S., Ceradini D., Jin Z., Yazdanbakhsh K. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat Med. 1996 Nov;2(11):1240–1243. doi: 10.1038/nm1196-1240. [DOI] [PubMed] [Google Scholar]
  23. Inaba K., Metlay J. P., Crowley M. T., Steinman R. M. Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. J Exp Med. 1990 Aug 1;172(2):631–640. doi: 10.1084/jem.172.2.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kalish M. L., Baldwin A., Raktham S., Wasi C., Luo C. C., Schochetman G., Mastro T. D., Young N., Vanichseni S., Rübsamen-Waigmann H. The evolving molecular epidemiology of HIV-1 envelope subtypes in injecting drug users in Bangkok, Thailand: implications for HIV vaccine trials. AIDS. 1995 Aug;9(8):851–857. doi: 10.1097/00002030-199508000-00004. [DOI] [PubMed] [Google Scholar]
  25. Kalish M. L., Luo C. C., Weniger B. G., Limpakarnjanarat K., Young N., Ou C. Y., Schochetman G. Early HIV type 1 strains in Thailand were not responsible for the current epidemic. AIDS Res Hum Retroviruses. 1994 Nov;10(11):1573–1575. doi: 10.1089/aid.1994.10.1573. [DOI] [PubMed] [Google Scholar]
  26. Knight S. C., Macatonia S. E., Patterson S. HIV I infection of dendritic cells. Int Rev Immunol. 1990;6(2-3):163–175. doi: 10.3109/08830189009056627. [DOI] [PubMed] [Google Scholar]
  27. Korber B. T., Allen E. E., Farmer A. D., Myers G. L. Heterogeneity of HIV-1 and HIV-2. AIDS. 1995;9 (Suppl A):S5–18. [PubMed] [Google Scholar]
  28. Kunanusont C., Foy H. M., Kreiss J. K., Rerks-Ngarm S., Phanuphak P., Raktham S., Pau C. P., Young N. L. HIV-1 subtypes and male-to-female transmission in Thailand. Lancet. 1995 Apr 29;345(8957):1078–1083. doi: 10.1016/s0140-6736(95)90818-8. [DOI] [PubMed] [Google Scholar]
  29. Langhoff E., Terwilliger E. F., Bos H. J., Kalland K. H., Poznansky M. C., Bacon O. M., Haseltine W. A. Replication of human immunodeficiency virus type 1 in primary dendritic cell cultures. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):7998–8002. doi: 10.1073/pnas.88.18.7998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lasky M., Perret J. L., Peeters M., Bibollet-Ruche F., Liegeois F., Patrel D., Molinier S., Gras C., Delaporte E. Presence of multiple non-B subtypes and divergent subtype B strains of HIV-1 in individuals infected after overseas deployment. AIDS. 1997 Jan;11(1):43–51. doi: 10.1097/00002030-199701000-00007. [DOI] [PubMed] [Google Scholar]
  31. Liu L. M., MacPherson G. G. Antigen acquisition by dendritic cells: intestinal dendritic cells acquire antigen administered orally and can prime naive T cells in vivo. J Exp Med. 1993 May 1;177(5):1299–1307. doi: 10.1084/jem.177.5.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Louwagie J., McCutchan F. E., Peeters M., Brennan T. P., Sanders-Buell E., Eddy G. A., van der Groen G., Fransen K., Gershy-Damet G. M., Deleys R. Phylogenetic analysis of gag genes from 70 international HIV-1 isolates provides evidence for multiple genotypes. AIDS. 1993 Jun;7(6):769–780. doi: 10.1097/00002030-199306000-00003. [DOI] [PubMed] [Google Scholar]
  33. Ludewig B., Holzmeister J., Gentile M., Gelderblom H. R., Rokos K., Becker Y., Pauli G. Replication pattern of human immunodeficiency virus type 1 in mature Langerhans cells. J Gen Virol. 1995 Jun;76(Pt 6):1317–1325. doi: 10.1099/0022-1317-76-6-1317. [DOI] [PubMed] [Google Scholar]
  34. Mascola J. R., Louwagie J., McCutchan F. E., Fischer C. L., Hegerich P. A., Wagner K. F., Fowler A. K., McNeil J. G., Burke D. S. Two antigenically distinct subtypes of human immunodeficiency virus type 1: viral genotype predicts neutralization serotype. J Infect Dis. 1994 Jan;169(1):48–54. doi: 10.1093/infdis/169.1.48. [DOI] [PubMed] [Google Scholar]
  35. Mastro T. D., Kunanusont C., Dondero T. J., Wasi C. Why do HIV-1 subtypes segregate among persons with different risk behaviors in South Africa and Thailand? AIDS. 1997 Jan;11(1):113–116. doi: 10.1097/00002030-199701000-00017. [DOI] [PubMed] [Google Scholar]
  36. Mastro T. D., de Vincenzi I. Probabilities of sexual HIV-1 transmission. AIDS. 1996;10 (Suppl A):S75–S82. doi: 10.1097/00002030-199601001-00011. [DOI] [PubMed] [Google Scholar]
  37. Mazzarelli J. M., Mengus G., Davidson I., Ricciardi R. P. The transactivation domain of adenovirus E1A interacts with the C terminus of human TAF(II)135. J Virol. 1997 Oct;71(10):7978–7983. doi: 10.1128/jvi.71.10.7978-7983.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. McCutchan F. E., Hegerich P. A., Brennan T. P., Phanuphak P., Singharaj P., Jugsudee A., Berman P. W., Gray A. M., Fowler A. K., Burke D. S. Genetic variants of HIV-1 in Thailand. AIDS Res Hum Retroviruses. 1992 Nov;8(11):1887–1895. doi: 10.1089/aid.1992.8.1887. [DOI] [PubMed] [Google Scholar]
  39. Miller C. J., Alexander N. J., Sutjipto S., Lackner A. A., Gettie A., Hendrickx A. G., Lowenstine L. J., Jennings M., Marx P. A. Genital mucosal transmission of simian immunodeficiency virus: animal model for heterosexual transmission of human immunodeficiency virus. J Virol. 1989 Oct;63(10):4277–4284. doi: 10.1128/jvi.63.10.4277-4284.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Miller C. J., Alexander N. J., Vogel P., Anderson J., Marx P. A. Mechanism of genital transmission of SIV: a hypothesis based on transmission studies and the location of SIV in the genital tract of chronically infected female rhesus macaques. J Med Primatol. 1992 Feb-May;21(2-3):64–68. [PubMed] [Google Scholar]
  41. Miller C. J., McChesney M., Moore P. F. Langerhans cells, macrophages and lymphocyte subsets in the cervix and vagina of rhesus macaques. Lab Invest. 1992 Nov;67(5):628–634. [PubMed] [Google Scholar]
  42. Miller C. J., McGhee J. R., Gardner M. B. Mucosal immunity, HIV transmission, and AIDS. Lab Invest. 1993 Feb;68(2):129–145. [PubMed] [Google Scholar]
  43. Moore J. P., Cao Y., Leu J., Qin L., Korber B., Ho D. D. Inter- and intraclade neutralization of human immunodeficiency virus type 1: genetic clades do not correspond to neutralization serotypes but partially correspond to gp120 antigenic serotypes. J Virol. 1996 Jan;70(1):427–444. doi: 10.1128/jvi.70.1.427-444.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Moore J. P., McCutchan F. E., Poon S. W., Mascola J., Liu J., Cao Y., Ho D. D. Exploration of antigenic variation in gp120 from clades A through F of human immunodeficiency virus type 1 by using monoclonal antibodies. J Virol. 1994 Dec;68(12):8350–8364. doi: 10.1128/jvi.68.12.8350-8364.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Moore J. P., McKeating J. A., Huang Y. X., Ashkenazi A., Ho D. D. 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. J Virol. 1992 Jan;66(1):235–243. doi: 10.1128/jvi.66.1.235-243.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Nuovo G. J., Forde A., MacConnell P., Fahrenwald R. In situ detection of PCR-amplified HIV-1 nucleic acids and tumor necrosis factor cDNA in cervical tissues. Am J Pathol. 1993 Jul;143(1):40–48. [PMC free article] [PubMed] [Google Scholar]
  47. Ou C. Y., Takebe Y., Weniger B. G., Luo C. C., Kalish M. L., Auwanit W., Yamazaki S., Gayle H. D., Young N. L., Schochetman G. Independent introduction of two major HIV-1 genotypes into distinct high-risk populations in Thailand. Lancet. 1993 May 8;341(8854):1171–1174. doi: 10.1016/0140-6736(93)91001-3. [DOI] [PubMed] [Google Scholar]
  48. Patterson S., Knight S. C. Susceptibility of human peripheral blood dendritic cells to infection by human immunodeficiency virus. J Gen Virol. 1987 Apr;68(Pt 4):1177–1181. doi: 10.1099/0022-1317-68-4-1177. [DOI] [PubMed] [Google Scholar]
  49. Pavli P., Maxwell L., Van de Pol E., Doe F. Distribution of human colonic dendritic cells and macrophages. Clin Exp Immunol. 1996 Apr;104(1):124–132. doi: 10.1046/j.1365-2249.1996.d01-642.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pinchuk L. M., Polacino P. S., Agy M. B., Klaus S. J., Clark E. A. The role of CD40 and CD80 accessory cell molecules in dendritic cell-dependent HIV-1 infection. Immunity. 1994 Jul;1(4):317–325. doi: 10.1016/1074-7613(94)90083-3. [DOI] [PubMed] [Google Scholar]
  51. Pomerantz R. J., de la Monte S. M., Donegan S. P., Rota T. R., Vogt M. W., Craven D. E., Hirsch M. S. Human immunodeficiency virus (HIV) infection of the uterine cervix. Ann Intern Med. 1988 Mar;108(3):321–327. doi: 10.7326/0003-4819-108-3-321. [DOI] [PubMed] [Google Scholar]
  52. Pope M., Betjes M. G., Hirmand H., Hoffman L., Steinman R. M. Both dendritic cells and memory T lymphocytes emigrate from organ cultures of human skin and form distinctive dendritic-T-cell conjugates. J Invest Dermatol. 1995 Jan;104(1):11–17. doi: 10.1111/1523-1747.ep12613452. [DOI] [PubMed] [Google Scholar]
  53. Pope M., Betjes M. G., Romani N., Hirmand H., Cameron P. U., Hoffman L., Gezelter S., Schuler G., Steinman R. M. Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1. Cell. 1994 Aug 12;78(3):389–398. doi: 10.1016/0092-8674(94)90418-9. [DOI] [PubMed] [Google Scholar]
  54. Pope M., Gezelter S., Gallo N., Hoffman L., Steinman R. M. Low levels of HIV-1 infection in cutaneous dendritic cells promote extensive viral replication upon binding to memory CD4+ T cells. J Exp Med. 1995 Dec 1;182(6):2045–2056. doi: 10.1084/jem.182.6.2045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Ramazzotti E., Marconi A., Re M. C., Girolomoni G., Cenacchi G., Vignoli M., Zambruno G., Furlini G., La Placa M., Giannetti A. In vitro infection of human epidermal Langerhans' cells with HIV-1. Immunology. 1995 May;85(1):94–98. [PMC free article] [PubMed] [Google Scholar]
  56. Ramirez G., Braathen L. R., Kunze R. O., Gelderblom H. In vitro infection of human epidermal Langerhans cells with HIV. Adv Exp Med Biol. 1988;237:901–905. doi: 10.1007/978-1-4684-5535-9_135. [DOI] [PubMed] [Google Scholar]
  57. Richters C. D., Hoekstra M. J., Van Baare J., Du Pont J. S., Hoefsmit E. C., Kamperdijk E. W. Migratory properties and functional capacities of human skin dendritic cells. Br J Dermatol. 1995 Nov;133(5):721–727. doi: 10.1111/j.1365-2133.1995.tb02745.x. [DOI] [PubMed] [Google Scholar]
  58. Richters C. D., Hoekstra M. J., van Baare J., Du Pont J. S., Hoefsmit E. C., Kamperdijk E. W. Isolation and characterization of migratory human skin dendritic cells. Clin Exp Immunol. 1994 Nov;98(2):330–336. doi: 10.1111/j.1365-2249.1994.tb06146.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sornasse T., Flamand V., De Becker G., Bazin H., Tielemans F., Thielemans K., Urbain J., Leo O., Moser M. Antigen-pulsed dendritic cells can efficiently induce an antibody response in vivo. J Exp Med. 1992 Jan 1;175(1):15–21. doi: 10.1084/jem.175.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Soto-Ramirez L. E., Renjifo B., McLane M. F., Marlink R., O'Hara C., Sutthent R., Wasi C., Vithayasai P., Vithayasai V., Apichartpiyakul C. HIV-1 Langerhans' cell tropism associated with heterosexual transmission of HIV. Science. 1996 Mar 1;271(5253):1291–1293. doi: 10.1126/science.271.5253.1291. [DOI] [PubMed] [Google Scholar]
  61. Spira A. I., Marx P. A., Patterson B. K., Mahoney J., Koup R. A., Wolinsky S. M., Ho D. D. Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J Exp Med. 1996 Jan 1;183(1):215–225. doi: 10.1084/jem.183.1.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Steinman R. M. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol. 1991;9:271–296. doi: 10.1146/annurev.iy.09.040191.001415. [DOI] [PubMed] [Google Scholar]
  63. Subbarao S., Schochetman G. Genetic variability of HIV-1. AIDS. 1996;10 (Suppl A):S13–S23. doi: 10.1097/00002030-199601001-00003. [DOI] [PubMed] [Google Scholar]
  64. Trkola A., Dragic T., Arthos J., Binley J. M., Olson W. C., Allaway G. P., Cheng-Mayer C., Robinson J., Maddon P. J., Moore J. P. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature. 1996 Nov 14;384(6605):184–187. doi: 10.1038/384184a0. [DOI] [PubMed] [Google Scholar]
  65. Weissman D., Li Y., Ananworanich J., Zhou L. J., Adelsberger J., Tedder T. F., Baseler M., Fauci A. S. Three populations of cells with dendritic morphology exist in peripheral blood, only one of which is infectable with human immunodeficiency virus type 1. Proc Natl Acad Sci U S A. 1995 Jan 31;92(3):826–830. doi: 10.1073/pnas.92.3.826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Weniger B. G., Limpakarnjanarat K., Ungchusak K., Thanprasertsuk S., Choopanya K., Vanichseni S., Uneklabh T., Thongcharoen P., Wasi C. The epidemiology of HIV infection and AIDS in Thailand. AIDS. 1991;5 (Suppl 2):S71–S85. doi: 10.1097/00002030-199101001-00011. [DOI] [PubMed] [Google Scholar]
  67. Zhang L., Huang Y., He T., Cao Y., Ho D. D. HIV-1 subtype and second-receptor use. Nature. 1996 Oct 31;383(6603):768–768. doi: 10.1038/383768a0. [DOI] [PubMed] [Google Scholar]
  68. van Harmelen J., Wood R., Lambrick M., Rybicki E. P., Williamson A. L., Williamson C. An association between HIV-1 subtypes and mode of transmission in Cape Town, South Africa. AIDS. 1997 Jan;11(1):81–87. doi: 10.1097/00002030-199701000-00012. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES