The Achilles Heel of the Trojan horse model of HIV-1 trans-infection

PLoS Pathogens

Volumn 4, Issue 6, 2008, Pages

  Cavrois, Marielle ^a   Neidleman, Jason ^a   Greene, Warner C ^a,b  

^a GLADSTONE INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL MEMBRANE; CELL VACUOLE; DENDRITIC CELL; ENDOCYTOSIS; EXOCYTOSIS; HOST RESISTANCE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNITY; REVIEW; VIRION; VIRUS STRAIN; VIRUS TRANSMISSION; DISEASE TRANSMISSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; PATHOGENICITY; PHYSIOLOGY; VIROLOGY;

EQUIDAE; HUMAN IMMUNODEFICIENCY VIRUS 1;

CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; HIV INFECTIONS; HIV-1; HUMANS; VIRION;

EID: 46449129399     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000051     Document Type: Review

References (70)

1. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392: 245-252.
2. Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216.
3. Underhill DM, Ozinsky A (2002) Toll-like receptors: key mediators of microbe detection. Curr Opin Immunol 14: 103-110.
4. van Kooyk Y, Geijtenbeek TB (2003) DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol 3: 697-709.
5. Figdor CG, van Kooyk Y, Adema GJ (2002) C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol 2: 77-84.
6. Martinelli E, Cicala C, Van Ryk D, Goode DJ, Macleod K, et al. (2007) HIV-1 gp120 inhibits TLR9-mediated activation and IFN-{alpha} secretion in plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 104: 3396-3401.
7. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, et al. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526-1529.
8. Steinman RM, Granelli-Piperno A, Pope M, Trumpfheller C, Ignatius R, et al. (2003) The interaction of immunodeficiency viruses with dendritic cells. Curr Top Microbiol Immunol 276: 1-30.
9. de Witte L, Nabatov A, Pion M, Fluitsma D, de Jong MA, et al. (2007) Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med 13: 367-371.
10. Cameron PU, Freudenthal PS, Barker JM, Gezelter S, Inaba K, et al. (1992) Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257: 383-387.
11. Hu J, Miller CJ, O'Doherty U, Marx PA, Pope M (1999) The dendritic cell-T cell milieu of the lymphoid tissue of the tonsil provides a locale in which SIV can reside and propagate at chronic stages of infection. AIDS Res Hum Retroviruses 15: 1305-1314.
12. Pope M, Betjes MG, Romani N, Hirmand H, Cameron PU, et al. (1994) Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1. Cell 78: 389-398.
13. Frank I, Kacani L, Stoiber H, Stossel H, Spruth M, et al. (1999) Human immunodeficiency virus type 1 derived from cocultures of immature dendritic cells with autologous T cells carries T-cell-specific molecules on its surface and is highly infectious. J Virol 73: 3449-3454.
14. Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, et al. (2000) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 575-585.
15. Encabo A, Solves P, Mateu E, Sepulveda P, Carbonell-Uberos F, et al. (2004) Selective generation of different dendritic cell precursors from CD34+ cells by interleukin-6 and interleukin-3. Stem Cells 22: 725-740.
16. Granelli-Piperno A, Pritsker A, Pack M, Shimeliovich I, Arrighi JF, et al. (2005) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J Immunol 175: 4265-4273.
17. Krutzik SR, Tan B, Li H, Ochoa MT, Liu PT, et al. (2005) TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med 11: 653-660.
18. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, et al. (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
19. Curtis BM, Scharnowske S, Watson AJ (1992) Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc Natl Acad Sci USA 89: 8356-8360.
20. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR (2002) DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16: 135-144.
21. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, et al. (2003) Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300: 1295-1297.
22. Mitchell DA, Fadden AJ, Drickamer K (2001) A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands. J Biol Chem 276: 28939-28945.
23. Hong PW, Flummerfelt KB, de Parseval A, Gurney K, Elder JH, et al. (2002) Human immunodeficiency virus envelope (gp120) binding to DC-SIGN and primary dendritic cells is carbohydrate dependent but does not involve 2G12 or cyanovirin binding sites: implications for structural analyses of gp120-DC-SIGN binding. J Virol 76: 12855-12865.
24. Pohlmann S, Baribaud F, Doms RW (2001) DC-SIGN and DC-SIGNR: helping hands for HIV. Trends Immunol 22: 643-646.
25. Wu L, Martin TD, Carrington M, KewalRamani VN (2004) Raji B cells, misidentified as THP-1 cells, stimulate DC-SIGN-mediated HIV transmission. Virology 318: 17-23.
26. Arrighi JF, Pion M, Wiznerowicz M, Geijtenbeek TB, Garcia E, et al. (2004) Lentivirus-mediated RNA interference of DC-SIGN expression inhibits human immunodeficiency virus transmission from dendritic cells to T cells. J Virol 78: 10848-10855.
27. Arrighi JF, Pion M, Garcia E, Escola JM, van Kooyk Y, et al. (2004) DC-SIGN-mediated infectious synapse formation enhances X4 HIV-1 transmission from dendritic cells to T cells. J Exp Med 200: 1279-1288.
28. Gummuluru S, Rogel M, Stamatatos L, Emerman M (2003) Binding of human immunodeficiency virus type 1 to immature dendritic cells can occur independently of DC-SIGN and mannose binding C-type lectin receptors via a cholesterol-dependent pathway. J Virol 77: 12865-12874.
29. Boggiano C, Manel N, Littman DR (2007) Dendritic cell-mediated trans-enhancement of human immunodeficiency virus type 1 infectivity is independent of DC-SIGN. J Virol 81: 2519-2523.
30. Wang JH, Janas AM, Olson WJ, Wu L (2007) Functionally distinct transmission of human immunodeficiency virus type 1 mediated by immature and mature dendritic cells. J Virol 81: 8933-8943.
31. Jameson B, Baribaud F, Pohlmann S, Ghavimi D, Mortari F, et al. (2002) Expression of DC-SIGN by dendritic cells of intestinal and genital mucosae in humans and rhesus macaques. J Virol 76: 1866-1875.
32. Turville S, Wilkinson J, Cameron P, Dable J, Cunningham AL (2003) The role of dendritic cell C-type lectin receptors in HIV pathogenesis. J Leukoc Biol 74: 710-718.
33. Turville SG, Cameron PU, Handley A, Lin G, Pohlmann S, et al. (2002) Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3: 975-983.
34. Kavanagh DG, Bhardwaj N (2002) A division of labor: DC subsets and HIV receptor diversity. Nat Immunol 3: 891-893.
35. Nguyen DG, Hildreth JE (2003) Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages. Eur J Immunol 33: 483-493.
36. Cavrois M, Neidleman J, Kreisberg JF, Greene WC (2007) In vitro derived dendritic cells trans-infect CD4 T cells primarily with surface-bound HIV-1 virions. PLoS Pathog 3: e4. doi:10.1371/journal.ppat.0030004.
37. Fahrbach KM, Barry SM, Ayehunie S, Lamore S, Klausner M, et al. (2007) Activated CD34-derived Langerhans cells mediate transinfection with human immunodeficiency virus. J Virol 81: 6858-6868.
38. Blauvelt A, Asada H, Saville MW, Klaus-Kovtun V, Altman DJ, et al. (1997) Productive infection of dendritic cells by HIV-1 and their ability to capture virus are mediated through separate pathways. J Clin Invest 100: 2043-2053.
39. Cameron PU, Lowe MG, Crowe SM, O'Doherty U, Pope M, et al. (1994) Susceptibility of dendritic cells to HIV-1 infection in vitro. J Leukoc Biol 56: 257-265.
40. Hladik F, Lentz G, Akridge RE, Peterson G, Kelley H, et al. (1999) Dendritic cell-T-cell interactions support coreceptor-independent human immunodeficiency virus type 1 transmission in the human genital tract. J Virol 73: 5833-5842.
41. Frank I, Piatak M Jr, Stoessel H, Romani N, Bonnyay D, et al. (2002) Infectious and whole inactivated simian immunodeficiency viruses interact similarly with primate dendritic cells (DCs): differential intracellular fate of virions in mature and immature DCs. J Virol 76: 2936-2951.
42. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127: 915-934.
43. Welsch S, Keppler OT, Habermann A, Allespach I, Krijnse-Locker J, et al. (2007) HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog 3: e36. doi:10.1371/journal.ppat.0030036.
44. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, et al. (2005) HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 6: 488-501.
45. Izquierdo-Useros N, Blanco J, Erkizia I, Fernandez-Figueras MT, Borras FE, et al. (2007) Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J Virol 81: 7559-7570.
46. Hladik F, Sakchalathorn P, Ballweber L, Lentz G, Fialkow M, et al. (2007) Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 26: 257-270.
47. Hunger RE, Sieling PA, Ochoa MT, Sugaya M, Burdick AE, et al. (2004) Langerhans cells utilize CD1a and langerin to efficiently present nonpeptide antigens to T cells. J Clin Invest 113: 701-708.
48. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, et al. (2004) Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 103: 2170-2179.
49. Wiley RD, Gummuluru S (2006) Immature dendritic cell-derived exosomes can mediate HIV-1 trans infection. Proc Natl Acad Sci U S A 103: 738-743.
50. Wu L, KewalRamani VN (2006) Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 6: 859-868.
51. Piguet V, Sattentau Q (2004) Dangerous liaisons at the virological synapse. J Clin Invest 114: 605-610.
52. Moris A, Pajot A, Blanchet F, Guivel-Benhassine F, Salcedo M, et al. (2006) Dendritic cells and HIV-specific CD4+ T cells: HIV antigen presentation, T-cell activation, and viral transfer. Blood 108: 1643-1651.
53. VanCompernolle SE, Taylor RJ, Oswald-Richter K, Jiang J, Youree BE, et al. (2005) Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells. J Virol 79: 11598-11606.
54. Chang TL, Teleshova N, Rapista A, Paluch M, Anderson RA, et al. (2007) SAMMA, a mandelic acid condensation polymer, inhibits dendritic cell-mediated HIV transmission. FEBS Lett 581: 4596-4602.
55. Herold BC, Scordi-Bello I, Cheshenko N, Marcellino D, Dzuzelewski M, et al. (2002) Mandelic acid condensation polymer: novel candidate microbicide for prevention of human immunodeficiency virus and herpes simplex virus entry. J Virol 76: 11236-11244.
56. Boes M, Cerny J, Massol R, Op den Brouw M, Kirchhausen T, et al. (2002) T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418: 983-988.
57. Lavoie PM, Thibodeau J, Erard F, Sekaly RP (1999) Understanding the mechanism of action of bacterial superantigens from a decade of research. Immunol Rev 168: 257-269.
58. Douek DC, Brenchley JM, Betts MR, Ambrozak DR, Hill BJ, et al. (2002) HIV preferentially infects HIV-specific CD4+ T cells. Nature 417: 95-98.
59. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, et al. (2005) Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol 79: 5386-5399.
60. Burleigh L, Lozach PY, Schiffer C, Staropoli I, Pezo V, et al. (2006) Infection of dendritic cells (DCs), not DC-SIGN-mediated internalization of human immunodeficiency virus, is required for long-term transfer of virus to T cells. J Virol 80: 2949-2957.
61. Wang JH, Janas AM, Olson WJ, KewalRamani VN, Wu L (2007) CD4 coexpression regulates DC-SIGN-mediated transmission of human immunodeficiency virus type 1. J Virol 81: 2497-2507.
62. Ganesh L, Leung K, Lore K, Levin R, Panet A, et al. (2004) Infection of specific dendritic cells by CCR5-tropic human immunodeficiency virus type 1 promotes cell-mediated transmission of virus resistant to broadly neutralizing antibodies. J Virol 78: 11980-11987.
63. van Montfort T, Nabatov AA, Geijtenbeek TB, Pollakis G, Paxton WA (2007) Efficient capture of antibody neutralized HIV-1 by cells expressing DC-SIGN and transfer to CD4+ T lymphocytes. J Immunol 178: 3177-3185.
64. Sanders RW, de Jong EC, Baldwin CE, Schuitemaker JH, Kapsenberg ML, et al. (2002) Differential transmission of human immunodeficiency virus type 1 by distinct subsets of effector dendritic cells. J Virol 76: 7812-7821.
65. Granelli-Piperno A, Delgado E, Finkel V, Paxton W, Steinman RM (1998) Immature dendritic cells selectively replicate macrophagetropic (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J Virol 72: 2733-2737.
66. Weissman D, Li Y, Orenstein JM, Fauci AS (1995) 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 155: 4111-4117.
67. Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M (2007) In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J Cell Biol 177: 329-341.
68. Trumpfheller C, Park CG, Finke J, Steinman RM, Granelli-Piperno A (2003) Cell type-dependent retention and transmission of HIV-1 by DC-SIGN. Int Immunol 15: 289-298.
69. Moris A, Nobile C, Buseyne F, Porrot F, Abastado JP, et al. (2004) DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood 103: 2648-2654.
70. Cambi A, de Lange F, van Maarseveen NM, Nijhuis M, Joosten B, et al. (2004) Microdomains of the C-type lectin DC-SIGN are portals for virus entry into dendritic cells. J Cell Biol 164: 145-155.