HIV-1 efficient entry in inner foreskin is mediated by elevated CCL5/RANTES that recruits T cells and fuels conjugate formation with Langerhans cells

PLoS Pathogens

Volumn 7, Issue 6, 2011, Pages

  Zhou, Zhicheng ^a,b,c   Barry de Longchamps, Nicolas ^a,c   Schmitt, Alain ^a,b,c   Zerbib, Marc ^c,d   Vacher Lavenu, Marie Cécile ^c,e   Bomsel, Morgane ^a,b,c   Ganor, Yonatan ^a,b,c  

^a CNRS   (France)

^b INSTITUT COCHIN   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Urology Service   (France)

^e NONE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; CCL20 PROTEIN, HUMAN; CCL5 PROTEIN, HUMAN;

ADULT; ARTICLE; BASEMENT MEMBRANE; CELL MIGRATION; CONJUGATE; DERMIS; EPIDERMIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN TISSUE; INOCULATION; LANGERHANS CELL; MALE; PREPUCE; T LYMPHOCYTE; VIRUS ENTRY; VIRUS TRANSMISSION; BIOSYNTHESIS; CELL COMMUNICATION; CELL CULTURE; CELL MOTION; CIRCUMCISION; DISEASE TRANSMISSION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CELL COMMUNICATION; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL20; CHEMOKINE CCL5; CIRCUMCISION, MALE; FORESKIN; HIV INFECTIONS; HIV-1; HUMANS; LANGERHANS CELLS; LYMPHOCYTE ACTIVATION; MALE; T-LYMPHOCYTES; VIRUS INTERNALIZATION;

EID: 79959822361     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002100     Document Type: Article

References (51)

1. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, et al. (2005) Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 Trial. PLoS Med 2: e298.
2. Bailey RC, Moses S, Parker CB, Agot K, Maclean I, et al. (2007) Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial. Lancet 369: 643-56.
3. Gray RH, Kigozi G, Serwadda D, Makumbi F, Watya S, et al. (2007) Male circumcision for HIV prevention in men in Rakai, Uganda: a randomised trial. Lancet 369: 657-66.
4. Quinn TC, (2007) Circumcision and HIV transmission. Curr Opin Infect Dis 20: 33-8.
5. Ross HM, Romrell LJ, Kaye GI, Histology, a text an atlas. Third ed ed, ed. P.A. Coryell 1995 Baltimore Williams & Wilkins pp. 58-93.
6. Hussain LA, Lehner T, (1995) Comparative investigation of Langerhans' cells and potential receptors for HIV in oral, genitourinary and rectal epithelia. Immunology 85: 475-84.
7. Patterson BK, Landay A, Siegel JN, Flener Z, Pessis D, et al. (2002) Susceptibility to human immunodeficiency virus-1 infection of human foreskin and cervical tissue grown in explant culture. Am J Pathol 161: 867-73.
8. McCoombe SG, Short RV, (2006) Potential HIV-1 target cells in the human penis. Aids 20: 1491-5.
9. Ganor Y, Bomsel M, (2010) HIV-1 Transmission in the Male Genital Tract. Am J Reprod Immunol In press.
10. Ganor Y, Zhou Z, Tudor D, Schmitt A, Vacher-Lavenu MC, et al. (2010) Within 1 h, HIV-1 uses viral synapses to enter efficiently the inner, but not outer, foreskin mucosa and engages Langerhans-T cell conjugates. Mucosal Immunol 3: 506-22.
11. Qin Q, Zheng XY, Wang YY, Shen HF, Sun F, et al. (2009) Langerhans' cell density and degree of keratinization in foreskins of Chinese preschool boys and adults. Int Urol Nephrol 41: 747-53.
12. Dinh MH, McRaven MD, Kelley Z, Penugonda S, Hope TJ, (2010) Keratinization of the adult male foreskin and implications for male circumcision. Aids 24: 899-906.
13. Pask AJ, McInnes KJ, Webb DR, Short RV, (2008) Topical oestrogen keratinises the human foreskin and may help prevent HIV infection. PLoS ONE 3: e2308.
14. Donoval BA, Landay AL, Moses S, Agot K, Ndinya-Achola JO, et al. (2006) HIV-1 target cells in foreskins of African men with varying histories of sexually transmitted infections. Am J Clin Pathol 125: 386-91.
15. Hirbod T, Bailey RC, Agot K, Moses S, Ndinya-Achola J, et al. (2010) Abundant expression of HIV target cells and C-type lectin receptors in the foreskin tissue of young Kenyan men. Am J Pathol 176: 2798-805.
16. Fischetti L, Barry SM, Hope TJ, Shattock RJ, (2009) HIV-1 infection of human penile explant tissue and protection by candidate microbicides. Aids 23: 319-28.
17. Soilleux EJ, Coleman N, (2004) Expression of DC-SIGN in human foreskin may facilitate sexual transmission of HIV. J Clin Pathol 57: 77-8.
18. Valladeau J, Ravel O, Dezutter-Dambuyant C, Moore K, Kleijmeer M, et al. (2000) Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12: 71-81.
19. 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: 975-83.
20. 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: 587-97.
21. Figdor CG, van Kooyk Y, Adema GJ, (2002) C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol 2: 77-84.
22. 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: 367-71.
23. Schall TJ, Bacon K, Toy KJ, Goeddel DV, (1990) Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347: 669-71.
24. Schall TJ, (1991) Biology of the RANTES/SIS cytokine family. Cytokine 3: 165-83.
25. 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: 257-70.
26. Merad M, Ginhoux F, Collin M, (2008) Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 8: 935-47.
27. Salle B, Brochard P, Bourry O, Mannioui A, Andrieu T, et al. (2010) Infection of macaques after vaginal exposure to cell-associated simian immunodeficiency virus. J Infect Dis 202: 337-44.
28. Anderson DJ, Politch JA, Nadolski AM, Blaskewicz CD, Pudney J, et al. (2010) Targeting Trojan Horse leukocytes for HIV prevention. Aids 24: 163-87.
29. de Nadai P, Chenivesse C, Gilet J, Porte H, Vorng H, et al. (2006) CCR5 usage by CCL5 induces a selective leukocyte recruitment in human skin xenografts in vivo. J Invest Dermatol 126: 2057-64.
30. Fahrbach KM, Barry SM, Anderson MR, Hope TJ, (2010) Enhanced cellular responses and environmental sampling within inner foreskin explants: implications for the foreskin's role in HIV transmission. Mucosal Immunol 3: 410-8.
31. Dieu-Nosjean MC, Massacrier C, Homey B, Vanbervliet B, Pin JJ, et al. (2000) Macrophage inflammatory protein 3alpha is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J Exp Med 192: 705-18.
32. Haase AT, (2010) Targeting early infection to prevent HIV-1 mucosal transmission. Nature 464: 217-23.
33. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-8.
34. Shen R, Richter HE, Clements RH, Novak L, Huff K, et al. (2009) Macrophages in vaginal but not intestinal mucosa are monocyte-like and permissive to human immunodeficiency virus type 1 infection. J Virol 83: 3258-67.
35. Hladik F, McElrath MJ, (2008) Setting the stage: host invasion by HIV. Nat Rev Immunol 8: 447-57.
36. Piguet V, Steinman RM, (2007) The interaction of HIV with dendritic cells: outcomes and pathways. Trends Immunol 28: 503-10.
37. Wu L, KewalRamani VN, (2006) Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 6: 859-68.
38. de Jong MA, de Witte L, Oudhoff MJ, Gringhuis SI, Gallay P, et al. (2008) TNF-alpha and TLR agonists increase susceptibility to HIV-1 transmission by human Langerhans cells ex vivo. J Clin Invest 118: 3440-52.
39. 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: 6858-68.
40. Kawamura T, Cohen SS, Borris DL, Aquilino EA, Glushakova S, et al. (2000) Candidate microbicides block HIV-1 infection of human immature Langerhans cells within epithelial tissue explants. J Exp Med 192: 1491-500.
41. Kawamura T, Koyanagi Y, Nakamura Y, Ogawa Y, Yamashita A, et al. (2008) Significant virus replication in Langerhans cells following application of HIV to abraded skin: relevance to occupational transmission of HIV. J Immunol 180: 3297-304.
42. 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: 389-98.
43. Sugaya M, Lore K, Koup RA, Douek DC, Blauvelt A, (2004) HIV-infected Langerhans cells preferentially transmit virus to proliferating autologous CD4+ memory T cells located within Langerhans cell-T cell clusters. J Immunol 172: 2219-24.
44. Reece JC, Handley AJ, Anstee EJ, Morrison WA, Crowe SM, et al. (1998) HIV-1 selection by epidermal dendritic cells during transmission across human skin. J Exp Med 187: 1623-31.
45. 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: 383-7.
46. Lusso P, (2006) HIV and the chemokine system: 10 years later. Embo J 25: 447-56.
47. Kuritzkes DR, (2009) HIV-1 entry inhibitors: an overview. Curr Opin HIV AIDS 4: 82-7.
48. Biswas P, Tambussi G, Lazzarin A, (2007) Access denied? The status of co-receptor inhibition to counter HIV entry. Expert Opin Pharmacother 8: 923-33.
49. Veazey RS, Ketas TJ, Dufour J, Moroney-Rasmussen T, Green LC, et al. (2010) Protection of rhesus macaques from vaginal infection by vaginally delivered maraviroc, an inhibitor of HIV-1 entry via the CCR5 co-receptor. J Infect Dis 202: 739-44.
50. Lederman MM, Veazey RS, Offord R, Mosier DE, Dufour J, et al. (2004) Prevention of vaginal SHIV transmission in rhesus macaques through inhibition of CCR5. Science 306: 485-7.
51. Lagaye S, Derrien M, Menu E, Coito C, Tresoldi E, et al. (2001) Cell-to-cell contact results in a selective translocation of maternal human immunodeficiency virus type 1 quasispecies across a trophoblastic barrier by both transcytosis and infection. J Virol 75: 4780-91.