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PMID: 9584140 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

HIV-1 selection by epidermal dendritic cells during transmission across human skin.

The Journal of experimental medicine ·Vol. 187 ·No. 10 ·1998-05-18 ·Pages 1623-31

Reece JC, Handley AJ, Anstee EJ, Morrison WA, Crowe SM, Cameron PU

Abstract

Macrophage tropic HIV-1 is predominant during the initial viremia after person to person transmission of HIV-1 (Zhu, T., H. Mo, N. Wang, D.S. Nam, Y. Cao, R.A. Koup, and D.D. Ho. 1993. Science. 261:1179-1181.), and this selection may occur during virus entry and carriage to the lymphoid tissue. Human skin explants were used to model HIV-1 selection that may occur at the skin or mucosal surface. Macrophage tropic, but not T cell line tropic strains of HIV-1 applied to the abraded epidermis were recovered from the cells emigrating from the skin explants. Dermis and epidermis were separated by dispase digestion after virus exposure to determine the site of viral selection within the skin. Uptake and transmission to T cells of all HIV-1 isolates was found with the dermal emigrant cells, but only macrophage tropic virus was transferred by emigrants from the epidermis exposed to HIV-1, indicating selection only within the epidermis. CD3+, CD4+ T cells were found in both the dermal and epidermal emigrant cells. After cell sorting to exclude contaminating T cells, macrophage tropic HIV-1 was found in both the dermal emigrant dendritic cells and in dendritic cells sorted from the epidermal emigrants. These observations suggest that selective infection of the immature epidermal dendritic cells represents the cellular mechanism that limits the initial viremia to HIV-1 that can use the CCR5 coreceptor.

MeSH Terms
CD4-Positive T-Lymphocytes/virology Coculture Techniques Dendritic Cells/virology HIV Infections/virology HIV-1/physiology Humans Macrophages/virology Organ Culture Techniques Skin/virology Virus Replication
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Reece J C
Department of Microbiology and Immunology, University of Melbourne, Parkville, Victoria, Australia 3052.
Handley A J
Anstee E J
Morrison W A
Crowe S M
Cameron P U
References (49)
49 references, click to expand
  1. Human immunodeficiency virus type 1 variants with increased replicative capacity develop during the asymptomatic stage before disease progression.
    J Virol. 1994 Jul;68(7):4400-8 PMID: 7515972
  2. 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):1149-58 PMID: 8674120
  3. Both a precursor and a mature population of dendritic cells can bind HIV. However, only the mature population that expresses CD80 can pass infection to unstimulated CD4+ T cells.
    J Immunol. 1995 Oct 15;155(8):4111-7 PMID: 7561124
  4. In vitro HIV1 infection of human cervical tissue.
    Res Virol. 1994 May-Aug;145(3-4):155-61 PMID: 7800940
  5. Low infection frequency of macrophages in the spleens of HIV+ patients.
    Res Virol. 1996 Mar-Jun;147(2-3):115-21 PMID: 8901430
  6. 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):11-7 PMID: 7798627
  7. 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-cell-tropic virus population.
    J Virol. 1992 Mar;66(3):1354-60 PMID: 1738194
  8. Infection and apoptotic cell death of CD4+ T cells during an immune response to HIV-1-pulsed dendritic cells.
    AIDS Res Hum Retroviruses. 1994 Jan;10(1):61-71 PMID: 7910031
  9. Productive infection of dendritic cells by HIV-1 and their ability to capture virus are mediated through separate pathways.
    J Clin Invest. 1997 Oct 15;100(8):2043-53 PMID: 9329969
  10. Migration and maturation of Langerhans cells in skin transplants and explants.
    J Exp Med. 1990 Nov 1;172(5):1483-93 PMID: 2230654
  11. Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1.
    Cell. 1994 Aug 12;78(3):389-98 PMID: 7914836
  12. In vitro HIV1 infection of CD34+ progenitor-derived dendritic/Langerhans cells at different stages of their differentiation in the presence of GM-CSF/TNF alpha.
    Res Virol. 1996 Mar-Jun;147(2-3):89-95 PMID: 8901426
  13. Efficient interaction of HIV-1 with purified dendritic cells via multiple chemokine coreceptors.
    J Exp Med. 1996 Dec 1;184(6):2433-8 PMID: 8976200
  14. Replication of HIV-1 in dendritic cell-derived syncytia at the mucosal surface of the adenoid.
    Science. 1996 Apr 5;272(5258):115-7 PMID: 8600520
  15. 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.
    J Virol. 1995 Jul;69(7):4544-7 PMID: 7769720
  16. Syncytium induction in primary CD4+ T-cell lines from normal donors by human immunodeficiency virus type 1 isolates with non-syncytium-inducing genotype and phenotype in MT-2 cells.
    J Virol. 1995 Nov;69(11):7099-105 PMID: 7474129
  17. Animal model of mucosally transmitted human immunodeficiency virus type 1 disease: intravaginal and oral deposition of simian/human immunodeficiency virus in macaques results in systemic infection, elimination of CD4+ T cells, and AIDS.
    J Virol. 1997 May;71(5):4016-23 PMID: 9094679
  18. Susceptibility of dendritic cells to HIV-1 infection in vitro.
    J Leukoc Biol. 1994 Sep;56(3):257-65 PMID: 8083598
  19. CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1.
    Science. 1996 Jun 28;272(5270):1955-8 PMID: 8658171
  20. Presentation of exogenous protein antigens by dendritic cells to T cell clones. Intact protein is presented best by immature, epidermal Langerhans cells.
    J Exp Med. 1989 Mar 1;169(3):1169-78 PMID: 2522497
  21. The dendritic cell system and its role in immunogenicity.
    Annu Rev Immunol. 1991;9:271-96 PMID: 1910679
  22. Phagocytosis of antigens by Langerhans cells in vitro.
    J Exp Med. 1993 Aug 1;178(2):509-19 PMID: 8393477
  23. Blood monocytes infected in vivo by HIV-1 variants with a syncytium-inducing phenotype.
    AIDS Res Hum Retroviruses. 1994 Jun;10(6):683-90 PMID: 8074932
  24. Syncytium-inducing (SI) phenotype suppression at seroconversion after intramuscular inoculation of a non-syncytium-inducing/SI phenotypically mixed human immunodeficiency virus population.
    J Virol. 1995 Mar;69(3):1810-8 PMID: 7853521
  25. 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):1856-62 PMID: 8791590
  26. Transmission of human immunodeficiency virus type 1 (HIV-1) from mother to child correlates with viral phenotype.
    Virology. 1993 Dec;197(2):624-9 PMID: 8249285
  27. Human and murine dermis contain dendritic cells. Isolation by means of a novel method and phenotypical and functional characterization.
    J Clin Invest. 1993 Dec;92(6):2587-96 PMID: 8254016
  28. Macrophage tropism of human immunodeficiency virus type 1 and utilization of the CC-CKR5 coreceptor.
    J Virol. 1997 Feb;71(2):1657-61 PMID: 8995695
  29. Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission.
    J Clin Invest. 1994 Nov;94(5):2060-7 PMID: 7962552
  30. Isolation and characterization of migratory human skin dendritic cells.
    Clin Exp Immunol. 1994 Nov;98(2):330-6 PMID: 7955541
  31. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection.
    Cell. 1996 Aug 9;86(3):367-77 PMID: 8756719
  32. HIV-1 infection in an individual homozygous for the CCR5 deletion allele.
    Nat Med. 1997 Mar;3(3):252-3 PMID: 9055842
  33. Change in coreceptor use correlates with disease progression in HIV-1--infected individuals.
    J Exp Med. 1997 Feb 17;185(4):621-8 PMID: 9034141
  34. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor.
    Science. 1996 May 10;272(5263):872-7 PMID: 8629022
  35. Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype.
    J Virol. 1997 Oct;71(10):7478-87 PMID: 9311827
  36. Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes.
    J Virol. 1996 Jun;70(6):3863-9 PMID: 8648722
  37. 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):215-25 PMID: 8551225
  38. Identification of a major co-receptor for primary isolates of HIV-1.
    Nature. 1996 Jun 20;381(6584):661-6 PMID: 8649511
  39. The interaction of macrophage and non-macrophage tropic isolates of HIV-1 with thymic and tonsillar dendritic cells in vitro.
    J Exp Med. 1996 Apr 1;183(4):1851-6 PMID: 8666941
  40. The role of CD40 and CD80 accessory cell molecules in dendritic cell-dependent HIV-1 infection.
    Immunity. 1994 Jul;1(4):317-25 PMID: 7534204
  41. Biological properties of HIV isolates in primary HIV infection: consequences for the subsequent course of infection.
    AIDS. 1993 Aug;7(8):1035-40 PMID: 8104421
  42. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes.
    Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1925-30 PMID: 9050881
  43. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells.
    Science. 1992 Jul 17;257(5068):383-7 PMID: 1352913
  44. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5.
    Nature. 1996 Jun 20;381(6584):667-73 PMID: 8649512
  45. Genotypic and phenotypic characterization of HIV-1 patients with primary infection.
    Science. 1993 Aug 27;261(5125):1179-81 PMID: 8356453
  46. 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):2045-56 PMID: 7500050
  47. In vitro infection of human epidermal Langerhans' cells with HIV-1.
    Immunology. 1995 May;85(1):94-8 PMID: 7635527
  48. Definition of the range and distribution of human immunodeficiency virus macrophage tropism using PCR-based infectivity measurements.
    J Gen Virol. 1994 Jul;75 ( Pt 7):1597-603 PMID: 8021591
  49. Early molecular replication of human immunodeficiency virus type 1 in cultured-blood-derived T helper dendritic cells.
    J Clin Invest. 1993 Jun;91(6):2721-6 PMID: 8514880
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
DOI
10.1084/jem.187.10.1623
Published
1998-05-18
Pages
1623-31
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2212292
Subset
IM
External Links
PubMed source DOI: 10.1084/jem.187.10.1623 PMC Full Text View journal details
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