Biological basis for the protective effect conferred by male circumcision against HIV infection

International Journal of STD and AIDS

Volumn 23, Issue 3, 2012, Pages 153-159

  Morris, B J ^a   Wamai, R J ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Foreskin; HIV; Langerhans cells; Male circumcision; T cells

Indexed keywords

BALANOPOSTHITIS; CELL MIGRATION; CIRCUMCISION; DENDRITE; HERPES SIMPLEX VIRUS 2; HETEROSEXUALITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; KERATINOCYTE; LANGERHANS CELL; PREPUCE; PRIORITY JOURNAL; REVIEW; SEXUAL INTERCOURSE; SEXUAL TRANSMISSION; SEXUALLY TRANSMITTED DISEASE; T LYMPHOCYTE;

CIRCUMCISION, MALE; HIV; HIV INFECTIONS; HUMANS; MALE; VIRUS INTERNALIZATION;

EID: 84860903972     PISSN: 09564624     EISSN: None     Source Type: Journal    
DOI: 10.1258/ijsa.2011.011228     Document Type: Review

References (82)

1. Auvert B, Taljaard D, Lagarde E, et al. Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 Trial. PLoS Med 2005;2:1112-22
2. Bailey RC, Moses S, Parker CB, et al. Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial. Lancet 2007;369:643-56
3. Gray RH, Kigozi G, Serwadda D, et al. Male circumcision for HIV prevention in men in Rakai, Uganda: a randomised trial. Lancet 2007;369:657-66
4. Siegfried N, Muller M, Deeks JJ, Volmink J. Male circumcision for prevention of heterosexual acquisition of HIV in men. Cochrane Database Syst Rev 2009;CD003362:38
5. Weiss HA, Halperin D, Bailey RC, et al. Male circumcision for HIV prevention: from evidence to action? (Review). AIDS 2008;22:567-74
6. Siegfried N, Muller M, Deeks JJ, Volmink J. Male circumcision for preventing heterosexual acquisition of HIV in men. Int J Epidemiol 2010;39:968-72
7. Gebremedhin S. Assessment of the protective effect of male circumcision from HIV infection and sexually transmitted diseases: evidence from 18 demographic and health surveys in sub-Saharan Africa. Afr J Reprod Health 2010;14:105-13
8. Auvert B, Taljaard D, Rech D, et al. Effect of the Orange Farm (South Africa) male circumcision roll-out (ANRS-12126) on the spread of HIV. Rome: Sixth IAS Conference on HIV Pathogenesis, Treatment and Prevention, 2011:WELBC02
9. Kong X, Kigozi G, Ssempija V, et al. Longer-term effects of male circumcision on HIV incidence and risk behaviors during post-trial surveillance in Rakai, Uganda. Boston: 18th Conference on Retroviruses and Opportunistic Infections, 2011:Abstract 36
10. Templeton DJ, Jin F, Mao L, et al. Circumcision and risk of HIV infection in Australian homosexual men. AIDS 2009;23:2347-51
11. Millett GA, Ding H, Lauby J, et al. Circumcision status and HIV infection among Black and Latino men who have sex with men in 3 US cities. J Acquir Immune Defic Syndr 2007;46:643-50
12. Millett GA, Flores SA, Marks G, Reed JB, Herbst JH. Circumcision status and risk of HIV and sexually transmitted infections among men who have sex with men: a meta-analysis. JAMA 2008;300:1674-84
13. Wiysonge CS, Kongnyuy EJ, Shey M, et al. Male circumcision for prevention of homosexual acquisition of HIV in men. Cochrane Database Syst Rev 2011;6:CD007496
14. Szabo R, Short RV. How does male circumcision protect against HIV infection? Br Med J 2000;320:1592-94
15. Cameron BE, Simonsen JN, D'Costa LJ, et al. Female to male transmission of human immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet 1989;ii:403-07
16. Weiss GN. Prophylactic neonatal surgery and infectious diseases. Pediatr Infect Dis J 1997;16:727-34
17. Patterson BK, Landy A, Siegel JN, et al. Susceptibility to human immunodeficiency virus-1 infection of human foreskin and cervical tissue grown in explant culture. Am J Pathol 2002;161:867-73
18. Qin Q, Zheng XY, Wang YY, et al. Langerhans' cell density and degree of keratinization in foreskins of Chinese preschool boys and adults. Int Urol Nephrol 2009;41:747-53
19. Dinh MH, McRaven MD, Kelley Z, Penugonda S, Hope TJ. Keratinization of the adult male foreskin and implications for male circumcision. AIDS 2010;24:899-906
20. Gray RH, Bailey RC, Morris BJ. [Comment on] Keratinization of the adult male foreskin and implications for male circumcision. AIDS 2010;24:1381
21. Hirbod T, Bailey RC, Agot K, et al. Abundant expression of HIV target cells and C-type lectin receptors in the foreskin tissue of young Kenyan men. Am J Pathol 2010;176:2798-805
22. Ganor Y, Zhou Z, Tudor D, et al. 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 2010;3:506-22
23. Ganor Y, Bomsel M. HIV-1 transmission in the male genital tract. Am J Reprod Immunol 2011;65:284-91
24. Hussain LA, Lehner T. Comparative investigation of Langerhans cells and potential receptors for HIV in oral, genitourinary and rectal epithelia. Immunology 1995;85:475-84
25. McCoombe SG, Short RV. Potential HIV-1 target cells in the human penis. AIDS 2006;20:1491-95
26. Donoval BA, Landay AL, Moses S, et al. HIV-1 target cells in foreskins of African men with varying histories of sexually transmitted infections. Am J Clin Pathol 2006;125:386-91
27. Soilleux EJ, Coleman N. Expression of DC-SIGN in human foreskin may facilitate sexual transmission of HIV. J Clin Pathol 2004;57:77-78
28. Fischetti L, Barry SM, Hope TJ, Shattock RJ. HIV-1 infection of human penile explant tissue and protection by candidate microbicides. AIDS 2009;23:319-28
29. Weiss G, Westbrook R, Sanders M. The distribution and density of Langerhans cells in the human prepuce: site of a diminished immune response. Isr J Med Sci 1993;29:42-43
30. Ganor Y, Revol M, Bomsel M. Urethra-a novel and efficient HIV-1 entry site in men Boston: 18th Conference on Retroviruses and Opportunistic Infections, 2011:Abstract 500
31. Miller CJ, Alexander NJ, Sutjipto S, et al. Genital mucosal transmission of simian immunodeficiency virus: animal model for heterosexual transmission of human immunodeficiency virus. J Virol 1989;63:4277-84
32. Wawer MJ, Reynolds SJ, Serwadda D, et al. Might male circumcision be more protective against HIV in the highly exposed? An immunological hypothesis. AIDS 2005;19:2181-82
33. Peters B, Whittall T, Babaahmady K, et al. Effect of heterosexual intercourse on mucosal alloimmunisation and resistance to HIV-1 infection. Lancet 2004;363:518-24
34. Miller C. Localization of simian immunodeficiency virus-infected cells in the genital tract of male and female rhesus macaques. J Reprod Immunol 1998;4:331-39
35. Anderson DJ, Politch JA, Nadolski AM, et al. Targeting Trojan Horse leukocytes for HIV prevention. AIDS 2010;24:163-87
36. Alfsen A, Yu H, Magérus-Chatinet A, Schmitt A, Bomsel M. HIV-1-infected blood mononuclear cells form an integrin-and agrin-dependent viral synapse to induce efficient HIV-1 transcytosis across epithelial cell monolayer. Mol Biol Cell 2005;16:4267-79
37. Alanis MC, Lucidi RS. Neonatal circumcision: a review of the world's oldest and most controversial operation. Obstet Gynecol Surv 2004;59:379-95
38. Turville SG, Cameron PU, Handley A, et al. Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 2002;3:975-83
39. Boggiano C, Littman DR. HIV's vagina travelogue. Immunity 2007;26:145-47
40. Fahrbach KM, Barry SM, Anderson MR, Hope TJ. Enhanced cellular responses and environmental sampling within inner foreskin explants: implications for the foreskin's role in HIV transmission. Mucosal Immunol 2010;3:410-18
41. Hladik F, Sakchalathorn P, Ballweber L, et al. Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 2007;26:257-70
42. de Witte L, Nabatov A, Pion M, et al. Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med 2007;13:367-71
43. Schwartz O. Langerhans cells lap up HIV-1. Nat Med 2007;13:245-46
44. Zhou Z, Barry de Longchamps N, Schmitt A, et al. 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 Pathol 2011;7:e1002100-114
45. van der Vlist M, van der Aar AM, Gringhuis SI, Geijtenbeek TB. Innate signaling in HIV-1 infection of dendritic cells. Curr Opin HIV AIDS 2011;6:348-52
46. Sabatté J, Ceballos A, Raiden S, et al. Human seminal plasma abrogates the capture and transmission of human immunodeficiency virus type 1 to CD4{thorn} T cells mediated by DC-SIGN. J Virol 2007;81:13723-34
47. Stax MJ, van Montfort T, Sprenger RR, et al. Mucin 6 in seminal plasma binds DC-SIGN and potently blocks dendritic cell mediated transfer of HIV-1 to CD4{thorn} T-lymphocytes. Virology 2009;391:203-11
48. Wu Z, Chen Z, Phillips DM. Human genital epithelial cells capture cell-free human immunodeficiency virus type 1 and transmit the virus to CD4{thorn} cells: implications for mechanisms of sexual transmission. J Infect Dis 2003;188:1473-82
49. Munch J, Rucker E, Standker L, et al. Semen-derived amyloid fibrils drastically enhance HIV infection. Cell 2007;131:1059-71
50. Roan NR, Greene WC. A seminal finding for understanding HIV transmission. Cell 2007;131:1044-46
51. Mehta SD, Krieger JN, Agot K, et al. Circumcision and reduced risk of self-reported penile coital injuries: Results from a randomized controlled trial in Kisumu, Kenya. J Urol 2010;184:203-09
52. Kaizu M, Weiler AM, Weisgrau KL, et al. Repeated intravaginal inoculation with cell-associated simian immunodeficiency virus results in persistent infection of nonhuman primates. J Infect Dis 2006;194:912-16
53. Kigozi G, Wawer M, Ssettuba A, et al. Foreskin surface area and HIV acquisition in Rakai, Uganda (size matters). AIDS 2009;23:2209-13
54. Morris BJ, Castellsague X. The role of circumcision in the prevention of STIs. In: Gross GE, Tyring S, eds. Sexually Transmitted Infections and Sexually Transmitted Diseases. Heidelberg: Springer, 2011:715-39
55. Gray RH, Serwadda D, Tobian AAR, et al. Effects of genital ulcer disease and herpes simplex virus type 2 on the efficacy of male circumcision for HIV prevention: Analyses from the Rakai trials. PLoS Med 2009;6:e1000187
56. Weiss HA, Thomas SL, Munabi SK, Hayes RJ. Male circumcision and risk of syphilis, chancroid, and genital herpes: a systematic review and meta-analysis. Sex Transm Infect 2006;82:101-09
57. Cohen MS, Hoffman IF, Royce RA, et al. Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. AIDSCAP Malawi Research Group. Lancet 1997;349:1868-73
58. Waskett JH, Morris BJ, Weiss HA. Errors in meta-analysis by Van Howe. Int J STD AIDS 2009;20:216-18
59. Freeman EE, Weiss HA, Glynn JR, et al. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 2006;20:73-83
60. Todd J, Grosskurth H, Changalucha J, et al. Risk factors influencing HIV infection incidence in a rural African population: a nested case-control study. J Infect Dis 2006;193:458-66
61. Stephenson J. New HIV prevention strategies urged: averting new infections key to controlling pandemic. J Am Med Assoc 2004;292:1163-64
62. White RG, Orroth KK, Glynn JR, et al. Treating curable sexually transmitted infections to prevent HIV in Africa: still an effective control strategy? J Acquir Immune Defic Syndr 2008;47:346-53
63. Desai K, Boily MC, Garnett GP, et al. The role of sexually transmitted infections in male circumcision effectiveness against HIV-insights from clinical trial simulation. Emerg Themes Epidemiol 2006;3:19
64. Boily MC, Desai K, Masse B, Gumel A. Incremental role of male circumcision on a generalised HIV epidemic through its protective effect against other sexually transmitted infections: from efficacy to effectiveness to population-level impact. Sex Transm Infect 2008;84(Suppl 2):ii28-34
65. Bailey RC, Mehta SD. Circumcision's place in the vicious cycle involving herpes simplex virus type 2 and HIV. J Infect Dis 2009;199:923-25
66. Freeman EE, White RG, Bakker R, et al. Population-level effect of potential HSV2 prophylactic vaccines on HIV incidence in sub-Saharan Africa. Vaccine 2008;27:940-46
67. Mahiane SG, Legeai C, Taljaard D, et al. Transmission probabilities of HIV and herpes simplex virus type 2, effect of male circumcision and interaction: a longitudinal study in a township of South Africa. AIDS 2009;23:377-83
68. Tobian AA, Quinn TC. Herpes simplex virus type 2 and syphilis infections with HIV: an evolving synergy in transmission and prevention. Curr Opin HIV AIDS 2009;4:294-99
69. Watson-Jones D, Weiss HA, Rusizoka M, et al. Effect of herpes simplex suppression on incidence of HIV among women in Tanzania. N Engl J Med 2008;358:1560-71
70. Sobngwi-Tambekou J, Taljaard D, Lissouba P, et al. Effect of HSV-2 serostatus on acquisition of HIV by young men: results of a longitudinal study in Orange Farm, South Africa. J Infect Dis 2009;199:958-64
71. Zhu J, Hladik F, Woodward A, et al. Persistence of HIV-1 receptor-positive cells after HSV-2 reactivation is a potential mechanism for increased HIV-1 acquisition. Nat Med 2009;15:886-92
72. Auvert B, Sobngwi-Tambekou J, Cutler E, et al. Effect of male circumcision on the prevalence of high-risk human papillomavirus in young men: results of a randomized controlled trial conducted in orange farm, South Africa. J Infect Dis 2009;199:14-19
73. Lu B, Wu Y, Nielson CM, et al. Factors associated with acquisition and clearance of human papillomavirus infection in a cohort of US men: a prospective study. J Infect Dis 2009;199:362-71
74. Hernandez BY, Shvetsov YB, Goodman MT, et al. Reduced clearance of penile human papillomavirus infection in uncircumcised men. J Infect Dis 2010;201:1340-43
75. Gray RH, Serwadda D, Kong X, et al. Male circumcision decreases acquisition and increases clearance of high-risk human papillomavirus in HIV-negative men: a randomized trial in Rakai, Uganda. J Infect Dis 2010;201:1455-62
76. Johnson KE, Sherman ME, Ssempiija V, et al. Foreskin inflammation is associated with HIV and herpes simplex virus type-2 infections in Rakai, Uganda. AIDS 2009;23:1807-15
77. Johnson KE, Redd AD, Quinn TC, et al. Effects of HIV-1 and herpes simplex virus type 2 infection on lymphocyte and dendritic cell density in adult foreskins from Rakai, Uganda. J Infect Dis 2011;203:602-9
78. O'Farrell N, Morison L, Moodley P, et al. Association between HIV and subpreputial penile wetness in uncircumcised men in South Africa. J Acquir Immune Defic Syndr 2006;43:69-77
79. Price LB, Liu CM, Johnson KE, et al. The effects of circumcision on the penis microbiome. PLoS ONE 2010;5:e8422
80. Haase AT. Targeting early infection to prevent HIV-1 mucosal transmission. Nature 2010;464:217-23
81. Weiss HA, Hankins CA, Dickson K. Male circumcision and risk of HIV infection in women: a systematic review and meta-analysis. Lancet Infect Dis 2009;9:669-77
82. Hallett TB, Alsallaq RA, Baeten JM, et al. Will circumcision provide even more protection from HIV to women and men? New estimates of the population impact of circumcision interventions. Sex Transm Infect 2011;87:88-93