Semen CD4+ T Cells and Macrophages Are Productively Infected at All Stages of SIV infection in Macaques

PLoS Pathogens

Volumn 9, Issue 12, 2013, Pages 1-13

  Bernard Stoecklin, Sibylle ^a,b,c   Gommet, Céline ^a,b,c   Corneau, Aurélien B ^a,b,c   Guenounou, Sabrina ^a,b,c   Torres, Claire ^a,b,c   Dejucq Rainsford, Nathalie ^d   Cosma, Antonio ^a,b,c   Dereuddre Bosquet, Nathalie ^a,b,c   Le Grand, Roger ^a,b,c  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Vaccine Research Institute (VRI)   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CYTOKINE; VIRUS DNA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; DENDRITIC CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOASSAY; IMMUNOFLUORESCENCE TEST; MACACA FASCICULARIS; MACROPHAGE; MALE; NONHUMAN; PHENOTYPE; POLYMORPHONUCLEAR CELL; REAL TIME POLYMERASE CHAIN REACTION; SEMEN ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS LOAD; VIRUS TRANSMISSION; ANIMAL; CD4 LYMPHOCYTE COUNT; CYTOLOGY; DISEASE MODEL; IMMUNOLOGY; PHYSIOLOGY; SPERM; VIROLOGY; VIRUS SHEDDING;

ANIMALS; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; DNA, VIRAL; MACACA FASCICULARIS; MACROPHAGES; MALE; PHENOTYPE; SEMEN; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS SHEDDING;

EID: 84892888299     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003810     Document Type: Article

References (47)

1. Haigwood NL, (2004) Predictive value of primate models for AIDS. AIDS Rev 6: 187-198.
2. Veazey RS, Shattock RJ, Klasse PJ, Moore JP, (2012) Animal models for microbicide studies. Curr HIV Res 10: 79-87.
3. Anderson DJ, Politch JA, Nadolski AM, Blaskewicz CD, Pudney J, et al. (2010) Targeting Trojan Horse leukocytes for HIV prevention. AIDS 24: 163-187.
4. Politch JA, Mayer KH, Anderson DJ, (2009) Depletion of CD4+ T cells in semen during HIV infection and their restoration following antiretroviral therapy. J Acquir Immune Defic Syndr 50: 283-289.
5. Anderson DJ, Yunis EJ, (1983) "Trojan Horse" leukocytes in AIDS. N Engl J Med 309: 984-985.
6. Alfsen A, Yu H, Magerus-Chatinet A, Schmitt A, Bomsel M, (2005) 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 16: 4267-4279.
7. Groot F, Welsch S, Sattentau QJ, (2008) Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood 111: 4660-4663.
8. Bomsel M, (1997) Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat Med 3: 42-47.
9. 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: 506-522.
10. Ganor Y, Zhou Z, Bodo J, Tudor D, Leibowitch J, et al. (2012) The adult penile urethra is a novel entry site for HIV-1 that preferentially targets resident urethral macrophages. Mucosal Immunol 6: 776-86.
11. 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.
12. Di Fabio S, Giannini G, Lapenta C, Spada M, Binelli A, et al. (2001) Vaginal transmission of HIV-1 in hu-SCID mice: a new model for the evaluation of vaginal microbicides. AIDS 15: 2231-2238.
13. 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: 337-344.
14. Le Tortorec A, Le Grand R, Denis H, Satie AP, Mannioui K, et al. (2008) Infection of semen-producing organs by SIV during the acute and chronic stages of the disease. PLoS One 3: e1792.
15. Kaizu M, Weiler AM, Weisgrau KL, Vielhuber KA, May G, et al. (2006) Repeated intravaginal inoculation with cell-associated simian immunodeficiency virus results in persistent infection of nonhuman primates. J Infect Dis 194: 912-916.
16. Baeten JM, Kahle E, Lingappa JR, Coombs RW, Delany-Moretlwe S, et al. (2011) Genital HIV-1 RNA predicts risk of heterosexual HIV-1 transmission. Sci Transl Med 3: 77ra29.
17. Tachet A, Dulioust E, Salmon D, De Almeida M, Rivalland S, et al. (1999) Detection and quantification of HIV-1 in semen: identification of a subpopulation of men at high potential risk of viral sexual transmission. AIDS 13: 823-831.
18. Coombs RW, Speck CE, Hughes JP, Lee W, Sampoleo R, et al. (1998) Association between culturable human immunodeficiency virus type 1 (HIV-1) in semen and HIV-1 RNA levels in semen and blood: evidence for compartmentalization of HIV-1 between semen and blood. J Infect Dis 177: 320-330.
19. Vernazza PL, Dyer JR, Fiscus SA, Eron JJ, Cohen MS, (1997) HIV-1 viral load in blood, semen and saliva. AIDS 11: 1058-1059.
20. Van Voorhis BJ, Martinez A, Mayer K, Anderson DJ, (1991) Detection of human immunodeficiency virus type 1 in semen from seropositive men using culture and polymerase chain reaction deoxyribonucleic acid amplification techniques. Fertil Steril 55: 588-594.
21. Mermin JH, Holodniy M, Katzenstein DA, Merigan TC, (1991) Detection of human immunodeficiency virus DNA and RNA in semen by the polymerase chain reaction. J Infect Dis 164: 769-772.
22. Hamed KA, Winters MA, Holodniy M, Katzenstein DA, Merigan TC, (1993) Detection of human immunodeficiency virus type 1 in semen: effects of disease stage and nucleoside therapy. J Infect Dis 167: 798-802.
23. Quayle AJ, Xu C, Mayer KH, Anderson DJ, (1997) T lymphocytes and macrophages, but not motile spermatozoa, are a significant source of human immunodeficiency virus in semen. J Infect Dis 176: 960-968.
24. Xu C, Politch JA, Tucker L, Mayer KH, Seage GR 3rd, et al. (1997) Factors associated with increased levels of human immunodeficiency virus type 1 DNA in semen. J Infect Dis 176: 941-947.
25. Krieger JN, Nirapathpongporn A, Chaiyaporn M, Peterson G, Nikolaeva I, et al. (1998) Vasectomy and human immunodeficiency virus type 1 in semen. J Urol 159: 820-825; discussion 825-826.
26. Mayer KH, Boswell S, Goldstein R, Lo W, Xu C, et al. (1999) Persistence of human immunodeficiency virus in semen after adding indinavir to combination antiretroviral therapy. Clin Infect Dis 28: 1252-1259.
27. Vernazza PL, Troiani L, Flepp MJ, Cone RW, Schock J, et al. (2000) Potent antiretroviral treatment of HIV-infection results in suppression of the seminal shedding of HIV. The Swiss HIV Cohort Study. AIDS 14: 117-121.
28. Ghosn J, Viard JP, Katlama C, de Almeida M, Tubiana R, et al. (2004) Evidence of genotypic resistance diversity of archived and circulating viral strains in blood and semen of pre-treated HIV-infected men. AIDS 18: 447-457.
29. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, et al. (2005) Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434: 1093-1097.
30. Brenchley JM, Hill BJ, Ambrozak DR, Price DA, Guenaga FJ, et al. (2004) T-cell subsets that harbor human immunodeficiency virus (HIV) in vivo: implications for HIV pathogenesis. J Virol 78: 1160-1168.
31. Veazey RS, Mansfield KG, Tham IC, Carville AC, Shvetz DE, et al. (2000) Dynamics of CCR5 expression by CD4(+) T cells in lymphoid tissues during simian immunodeficiency virus infection. J Virol 74: 11001-11007.
32. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ, (2004) HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J Exp Med 199: 283-293.
33. Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, et al. (2009) Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J Virol 83: 6234-6246.
34. Veazey RS, Tham IC, Mansfield KG, DeMaria M, Forand AE, et al. (2000) Identifying the target cell in primary simian immunodeficiency virus (SIV) infection: highly activated memory CD4(+) T cells are rapidly eliminated in early SIV infection in vivo. J Virol 74: 57-64.
35. Miller CJ, (1994) Animal models of viral sexually transmitted diseases. Am J Reprod Immunol 31: 52-63.
36. Lackner AA, Veazey RS, (2007) Current concepts in AIDS pathogenesis: insights from the SIV/macaque model. Annu Rev Med 58: 461-476.
37. Mannioui A, Bourry O, Sellier P, Delache B, Brochard P, et al. (2009) Dynamics of viral replication in blood and lymphoid tissues during SIVmac251 infection of macaques. Retrovirology 6: 106.
38. Miller CJ, Marthas M, Greenier J, Lu D, Dailey PJ, et al. (1998) In vivo replication capacity rather than in vitro macrophage tropism predicts efficiency of vaginal transmission of simian immunodeficiency virus or simian/human immunodeficiency virus in rhesus macaques. J Virol 72: 3248-3258.
39. Hladik F, Lentz G, Delpit E, McElroy A, McElrath MJ, (1999) Coexpression of CCR5 and IL-2 in human genital but not blood T cells: implications for the ontogeny of the CCR5+ Th1 phenotype. J Immunol 163: 2306-2313.
40. Prakash M, Kapembwa MS, Gotch F, Patterson S, (2001) Higher levels of activation markers and chemokine receptors on T lymphocytes in the cervix than peripheral blood of normal healthy women. J Reprod Immunol 52: 101-111.
41. Lehner T, Mitchell E, Bergmeier L, Singh M, Spallek R, et al. (2000) The role of gammadelta T cells in generating antiviral factors and beta-chemokines in protection against mucosal simian immunodeficiency virus infection. Eur J Immunol 30: 2245-2256.
42. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7557.
43. Li H, Bar KJ, Wang S, Decker JM, Chen Y, et al. (2010) High Multiplicity Infection by HIV-1 in Men Who Have Sex with Men. PLoS Pathog 6: e1000890.
44. Miller CJ, Li Q, Abel K, Kim EY, Ma ZM, et al. (2005) Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J Virol 79: 9217-9227.
45. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, et al. (2009) Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 206: 1273-1289.
46. Karlsson I, Malleret B, Brochard P, Delache B, Calvo J, et al. (2007) Dynamics of T-cell responses and memory T cells during primary simian immunodeficiency virus infection in cynomolgus macaques. J Virol 81: 13456-13468.
47. Benlhassan-Chahour K, Penit C, Dioszeghy V, Vasseur F, Janvier G, et al. (2003) Kinetics of lymphocyte proliferation during primary immune response in macaques infected with pathogenic simian immunodeficiency virus SIVmac251: preliminary report of the effect of early antiviral therapy. J Virol 77: 12479-12493.