Infection of semen-producing organs by SIV during the acute and chronic stages of the disease

PLoS ONE

Volumn 3, Issue 3, 2008, Pages

  Le Tortorec, Anna ^a   Le Grand, Roger ^b   Denis, Hélène ^a   Satie, Anne Pascale ^a   Mannioui, Karim ^b   Roques, Pierre ^b   Maillard, Anne ^c   Daniels, Sylvanne ^a   Jégou, Bernard ^a   Dejucq Rainsford, Nathalie ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

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

^c RENNES UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TESTOSTERONE; VIRUS ANTIGEN; VIRUS RNA; VIRUS DNA;

ACUTE DISEASE; ACUTE PHASE RESPONSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CHRONIC DISEASE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOLOGY; EPIDIDYMIS; GERM CELL; IMMUNE RESPONSE; INOCULATION; MACACA; MALE; MALE GENITAL SYSTEM; MALE GENITAL TRACT INFECTION; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PERSISTENT INFECTION; PROSTATE; RETROVIRUS INFECTION; SEMINAL VESICLE; SIMIAN IMMUNODEFICIENCY VIRUS; SPERM; SPERMATOGENESIS; T LYMPHOCYTE; TESTIS; TESTOSTERONE BLOOD LEVEL; VIREMIA; VIRUS DETECTION; VIRUS LOAD; ANIMAL; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ISOLATION AND PURIFICATION; LABORATORY DIAGNOSIS; PATHOGENICITY; PHYLOGENY; POLYMERASE CHAIN REACTION; VIROLOGY;

MACACA; SIMIAN IMMUNODEFICIENCY VIRUS;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; DNA, VIRAL; GENITALIA, MALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACACA FASCICULARIS; MALE; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, VIRAL; SEMEN; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIMEN HANDLING; VIRAL LOAD;

EID: 46349099527     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001792     Document Type: Article

References (109)

1. Zhu T, Wang N, Carr A, Nam DS, Moor Jankowski R, et al. (1996) Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: evidence for viral compartmentalization and selection during sexual transmission. J Virol 70: 3098-3107.
2. Byrn RA, Zhang D, Eyre R, McGowan K, Kiessling AA (1997) HIV-1 in semen: an isolated virus reservoir. Lancet 350: 1141.
3. Kiessling AA, Fitzgerald LM, Zhang D, Chhay H, Brettler D, et al. (1998) Human immunodeficiency virus in semen arises from a genetically distinct virus reservoir. AIDS Res Hum Retroviruses 14: 0889-2229.
4. 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.
5. Gupta P, Leroux C, Patterson BK, Kingsley L, Rinaldo C, et al. (2000) Human immunodeficiency virus type 1 shedding pattern in semen correlates with the compartmentalization of viral quasi species between blood and semen. J Infect Dis 182: 79-87.
6. Ping LH, Cohen MS, Hoffman I, Vernazza P, Seillier-Moiseiwitsch F, et al. (2000) Effects of genital tract inflammation on human immunodeficiency virus type 1 V3 populations in blood and semen. J Virol 74: 8946-8952.
7. Pillai SK, Good B, Pond SK, Wong JK, Strain MC, et al. (2005) Semen-specific genetic characteristics of human immunodeficiency virus type 1 env. J Virol 79: 1734-1742.
8. Vernazza PL, Eron JJ, Cohen MS, van der Horst CM, Troiani L, et al. (1994) Detection and biologic characterization of infectious HIV-1 in semen of seropositive men. AIDS 8: 1325-1329.
9. Hecht FM, Grant RM, Petropoulos CJ, Dillon B, Chesney MA, et al. (1998) Sexual transmission of an HIV-1 variant resistant to multiple reverse-transcriptase and protease inhibitors N Engl J Med 339: 307-311.
10. Kroodsma KL, Kozal MJ, Hamed KA, Winters MA, Merigan TC (1994) Detection of drug resistance mutations in the human immunodeficiency virus type 1 (HIV-1) pol gene: differences in semen and blood HIV-1 RNA and proviral DNA. J Infect Dis 170: 1292-1295.
11. Eron J, Vernazza PL, Johnston DM, Seillier-Moiseiwitsch F, Alcorn TM, Fiscus SA, Cohen MS (1998) Resistance of HIV-1 to antiretroviral agents in blood and seminal plasma: implications for transmission. AIDS 12: F181-189.
12. Eyre RC, Zheng G, Kiessling AA (2000) Multiple drug resistance mutations in human immunodeficiency virus in semen but not blood of a man on antiretroviral therapy. Urology 55: 591.
13. 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.
14. Zhang H, Dornadula G, Beumont M, Livornese LJ, Van Uitert B, et al. (1998) Human immunodeficiency virus type 1 in the semen of men receiving highly active antiretroviral therapy. N Engl J Med 339: 1803-1809.
15. 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.
16. Lafeuillade A, Solas C, Halfon P, Chadapaud S, Hittinger G, et al. (2002) Differences in the detection of three HIV-I protease inhibitors in non-blood compartments: Clinical correlations. HIV Clin Trials 3: 27-35.
17. Solas C, Lafeuillade A, Halfon P, Chadapaud S, Hittinger G, et al. (2003) Discrepancies between Protease Inhibitor Concentrations and Viral Load in Reservoirs and Sanctuary Sites in Human Immunodeficiency Virus-Infected Patients. Antimicrob Agents Chemother 47: 238-243.
18. Bujan L, Daudin M, Matsuda T, Righi L, Thauvin L, et al. (2004) Factors of intermittent HIV-1 excretion in semen and efficiency of sperm processing in obtaining spermatozoa without HIV-1 genomes. Aids 18: 757-766.
19. Little SJ, Holte S, Routy JP, Daar ES, Markowitz M, et al. (2002) Antiretroviral-drug resistance among patients recently infected with HIV. N Engl J Med 347: 385-394.
20. Grant RM, Hecht FM, Warmerdam M, Liu L, Liegler T, et al. (2002) Time trends in primary HIV-1 drug resistance among recently infected persons. Jama 288: 181-188.
21. Markowitz M, Mohri H, Mehandru S, Shet A, Berry L, et al. (2005) Infection with multidrug resistant, dual-tropic HIV-1 and rapid progression to AIDS: a case report. Lancet 365: 1031-1038.
22. Da Silva M, Shevchuk MM, Cronin WJ, Armenakas NA, Tannenbaum M, et al. (1990) Detection of HIV related protein in testes and prostates of patients with AIDS. Am J Clin Pathol 93: 196-201.
23. Pudney J, Anderson D (1991) Orchitis and human immunodeficiency virus type 1 infected cells in reproductive tissues from men with the acquired immune deficiency syndrome. Am J Pathol 139: 149-160.
24. Nuovo GJ, Becker J, Simsir A, Margiotta M, Khalife G, et al. (1994) HIV-1 nucleic acids localize to the spermatogonia and their progeny. A study by polymerase chain reaction in situ hybridization. Am J Pathol 144: 1142-1148.
25. Miller CJ, Vogel P, Alexander NJ, Dandekar S, Hendrickx AG, et al. (1994) Pathology and localization of simian immunodeficiency virus in the reproductive tract of chronically infected male rhesus macaques. Lab Invest 70: 255-262.
26. Pilcher CD, Tien HC, Eron JJ Jr, Vernazza PL, Leu SY, et al. (2004) Brief but efficient: acute HIV infection and the sexual transmission of HIV. J Infect Dis 189: 1785-1792.
27. Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Li X, et al. (2005) Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 191: 1403-1409.
28. Vicenzi E, Poli G (1994) Ultraviolet irradiation and cytokines as regulators of HIV latency and expression. Chem Biol Interact 91: 101-109.
29. Leynaert B, Downs AM, de Vincenzi I (1998) Heterosexual transmission of human immunodeficiency virus: variability of infectivity throughout the course of infection. European Study Group on Heterosexual Transmission of HIV. Am J Epidemiol 148: 88-96.
30. Shiboski SC, Padian NS (1998) Epidemiologic evidence for time variation in HIV infectivity. J Acquir Immune Defic Syndr Hum Retrovirol 19: 527-535.
31. Anderson RM (1988) The role of mathematical models in the study of HIV transmission and the epidemiology of AIDS. J Acquir Immune Defic Syndr 1: 241-256.
32. Haigwood NL (2004) Predictive value of primate models for AIDS. AIDS Rev 6: 187-198.
33. Dioszeghy V, Benlhassan-Chahour K, Delache B, Dereuddre-Bosquet N, Aubenque C, et al. (2006) Changes in soluble factor-mediated CD8+ cell-derived antiviral activity in cynomolgus macaques infected with simian immunodeficiency virus SIVmac251: relationship to biological markers of progression. J Virol 80: 236-245.
34. Puaux AL, Marsac D, Prost S, Singh MK, Earl P, et al. (2004) Efficient priming of simian/human immunodeficiency virus (SHIV-specific T-cell responses with DNA encoding hybrid SHIV/hepatitis B surface antigen particles. Vaccine 22: 3535-3545.
35. Thiebot H, Vaslin B, Derdouch S, Bertho JM, Mouthon F, et al. (2005) Impact of bone marrow hematopoiesis failure on T-cell generation during pathogenic simian immunodeficiency virus infection in macaques. Blood 105: 2403-2409.
36. Hu LH, Chen FH, Li YR, Wang L (2004) Real-time determination of human telomerase reverse transcriptase mRNA in gastric cancer. World J Gastroenterol 10: 3514-3517.
37. Greenier JL, Miller CJ, Lu D, Dailey PJ, Lu FX, et al. (2001) Route of simian immunodeficiency virus inoculation determines the complexity but not the identity of viral variant populations that infect rhesus macaques. J Virol 75: 3753-3765.
38. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
39. Swofford D (1999) PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4; Associates S, ed. Sunderland, MA.
40. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
41. Vivier E, Sorrell JM, Ackerly M, Robertson MJ, Rasmussen RA, et al. (1993) Developmental regulation of a mucinlike glycoprotein selectively expressed on natural killer cells. J Exp Med 178: 2023-2033.
42. Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP (2000) The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci U S A 97: 9585-9590.
43. Roulet V, Satie AP, Ruffault A, Le Tortorec A, Denis H, et al. (2006) Susceptibility to HIV-1 infection of human testis in situ and in vitro. American Journal of Pathology 169: 2094-2103.
44. Roulet V, Denis H, Staub C, Le Tortorec A, Delaleu B, et al. (2006) Human testis in organotypic culture: application for basic or clinical research. Human Reprod 21: 1564-1575.
45. Abel K, Alegria-Hartman MJ, Zanotto K, McChesney MB, Marthas ML, et al. (2001) Anatomic site and immune function correlate with relative cytokine mRNA expression levels in lymphoid tissues of normal rhesus macaques. Cytokine 16: 191-204.
46. Terasawa E, Krook C, Eman S, Watanabe G, Bridson WE, et al. (1987) Pulsatile luteinizing hormone (LH) release during the progesterone-induced LH surge in the female rhesus monkey. Endocrinology 120: 2265-2271.
47. El-Demiry M, Hargreave T, Busuttil A, James K, Ritchie A, et al. (1985) Lymphocyte subpopulation in the male genital tract. Br J Urol 57: 769.
48. Anderson DJ, Pudney J (2005) Human male genital tract immunity and experimental models. In: Mestecky J, Lamm M, Strober W, Bienenstock J, McGhee J, et al., eds. Mucosal Immunology. 3rd ed. New-York, NY: Elsevier Academic Press. pp 1647-1659.
49. Staprans SI, Dailey PJ, Rosenthal A, Horton C, Grant RM, et al. (1999) Simian immunodeficiency virus disease course is predicted by the extent of virus replication during primary infection. J Virol 73: 4829-4839.
50. Dejucq-Rainsford N, Jégou B (2004) Viruses in semen and male genital tissues: consequences for the reproductive system and therapeutic perspectives. Current Pharmaceutical Design 10: 557-575.
51. Miyake A, Ibuki K, Enose Y, Suzuki H, Horiuchi R, et al. (2006) Rapid dissemination of a pathogenic simian/human immunodeficiency virus to systemic organs and active replication in lymphoid tissues following intrarectal infection. J Gen Virol 87: 1311-1320.
52. Davis LE, Hjelle BL, Miller VE, Palmer DI, Llewellyn AL, et al. (1992) Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 42: 1736-1739.
53. Chakrabarti L, Hurtrel M, Maire MA, Vazeux R, Dormont D, et al. (1991) Early viral replication in the brain of SIV-infected rhesus monkeys. Am J Pathol 139: 1273-1280.
54. Pullium JK, Adams DR, Jackson E, Kim CN, Smith DK, et al. (2001) Pig-tailed macaques infected with human immunodeficiency virus (HIV) type 2GB122 or simian/HIV89.6p express virus in semen during primary infection: new model for genital tract shedding and transmission. J Infect Dis 183: 1023-1030.
55. Tachet A, Dulioust E, Salmon D, De Almeida M, RivaRand 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 [In Process Citation]. Aids 13: 823-831.
56. Bourlet T, Cazorla C, Berthelot P, Grattard F, Cognasse F, et al. (2001) Compartmentalization of HIV-1 according to antiretroviral therapy: viral loads are correlated in blood and semen but poorly in blood and saliva. Aids 15: 284-285.
57. Coombs RW, Reichelderfer PS, Landay AL (2003) Recent observations on HIV type-1 infection in the genital tract of men and women. Aids 17: 455-480.
58. Moniuszko M, Bogdan D, Pal R, Venzon D, Stevceva L, et al. (2005) Correlation between viral RNA levels but not immune responses in plasma and tissues of macaques with long-standing SIVmac251 infection. Virology 333: 159-168.
59. Pollanen P, von Euler M, Soder O (1990) Testicular immunoregulatory factors. J Reprod Immunol 18: 51-76.
60. Araneo BA, Dowell T, Diegel M, Daynes RA (1991) Dihydrotestosterone exerts a depressive influence on the production of interleukin-4 (IL-4), IL-5, and gamma-interferon, but not IL-2 by activated murine T cells. Blood 78: 688-699.
61. De Cesaris P, Filippini A, Cervelli C, Riccioli A, Muci S, et al. (1992) Immunosuppressive molecules produced by Sertoli cells cultured in vitro: biological effects on lymphocytes. Biochem Biophys Res Common 186: 1639-1646.
62. Streilein JW (1995) Unraveling immune privilege. Science 270: 1158-1159.
63. Bladergroen BA, Strik MC, Bovenschen N, van Berkum O, Scheffer GL, et al. (2001) The granzyme B inhibitor, protease inhibitor 9, is mainly expressed by dendritic cells and at immune-privileged sites. J Immunol 166: 3218-3225.
64. Shehu-Xhilaga M, Kent S, Batten J, Ellis S, Van der Meulen J, et al. (2007) The testis and epididymis are productively infected by SIV and SHIV in juvenile macaques during the post-acute stage of infection. Retrovirology 4: 7.
65. 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.
66. 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.
67. Ling B, Veazey RS, Luckay A, Penedo C, Xu K, et al. (2002) SIV(mac) pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. Aids 16: 1489-1496.
68. Benveniste O, Vaslin B, Le Grand R, Cheret A, Matheux F, et al. (1996) Comparative interleukin (IL-2)/interferon IFN-gamma and IL-4/IL-10 responses during acute infection of macaques inoculated with attenuated neftruncated or pathogenic SICmac251 virus. Proc Natl Acad Sci U S A 93: 3658-3663.
69. Cheret A, Le Grand R, Caufour P, Dereuddre-Bosquet N, Matheux F, et al. (1996) Cytokine mRNA expression in mononuclear cells from different tissues during acute SIVmac251 infection of macaques. AIDS Res Hum Retroviruses 12: 1263-1272.
70. Graziosi C, Gantt KR, Vaccarezza M, Demarest JF, Daucher M, et al. (1996) Kinetics of cytokine expression during primary human immunodeficiency virus type 1 infection. Proc Natl Acad Sci U S A 93: 4386-4391.
71. Decrion AZ, Dichamp I, Varin A, Herbein G (2005) HIV and inflammation. Curr HIV Res 3: 243-259.
72. Nilsson J, Kinloch-de-Loes S, Granath A, Sonnerborg A, Goh LE, et al. (2007) Early immune activation in gut-associated and peripheral lymphoid tissue during acute HIV infection. Aids 21: 565-574.
73. Abel K, Rocke DM, Chohan B, Fritts L, Miller CJ (2005) Temporal and anatomic relationship between virus replication and cytokine gene expression after vaginal simian immunodeficiency virus infection. J Virol 79: 12164-12172.
74. Holmann-Lehmann R, Williams AL, Swenerton RK, Li PL, Rasmussen RA, et al. (2002) Quantitation of simian cytokine and beta-chemokine mRNAs, using real-time reverse transcriptase-polymerase chain reaction: variations in expression during chronic primate lentivirus infection. AIDS Res Hum Retroviruses 18: 627-639.
75. Kedzierska K, Crowe SM (2001) Cytokines and HIV-1: interactions and clinical implications. Antivir Chem Chemother 12: 133-150.
76. Alexander RB, Ponniah S, Hasday J, Hebel JR (1998) Elevated levels of proinflammatory cytokines in the semen of patients with chronic prostatitis/ chronic pelvic pain syndrome. Urology 52: 744-749.
77. Miller LJ, Fischer KA, Goralnick SJ, Litt M, Burleson JA, et al. (2002) Interleukin-10 levels in seminal plasma: implications for chronic prostatitis-chronic pelvic pain syndrome. J Urol 167: 753-756.
78. Paulis G, Conti E, Voliani S, Bertozzi MA, Sarteschi ML, et al. (2003) Evaluation of the cytokines in genital secretions of patients with chronic prostatitis. Arch Ital Urol Androl 75: 179-186.
79. Suarez-Pinzon W, Korbutt GS, Power R, Hooton J, Rajotte RV, et al. (2000) Testicular sertoli cells protect islet beta-cells from autoimmune destruction in NOD mice by a transforming growth factor-betal-dependent mechanism. Diabetes 49: 1810-1818.
80. Filippini A, Riccioli A, Padula F, Lauretti P, D'Alessio A, et al. (2001) Control and impairment of immune privilege in the testis and in semen. Hum Reprod Update 7: 444-449.
81. Dai Z, Nasr IW, Reel M, Deng S, Diggs L, et al. (2005) Impaired recall of CD8 memory T cells in immunologically privileged tissue. J Immunol 174: 1165-1170.
82. Nasr IW, Wang Y, Gao G, Deng S, Diggs L, et al. (2005) Testicular immune privilege promotes transplantation tolerance by altering the balance between memory and regulatory T cells. J Immunol 174: 6161-6168.
83. Naito M, Itoh M (2008) Patterns of infiltration of lymphocytes into the testis under normal and pathological conditions in mice. Am J Reprod Immunol 59: 55-61.
84. O'Bryan MK, Gerdprasert O, Nikolic-Paterson DJ, Meinhardt A, Muir JA, et al. (2005) Cytokine profiles in the testes of rats treated with lipopolysaccharide reveal localized suppression of inflammatory responses. Am J Physiol Regul Integr Comp Physiol 288: R1744-1755.
85. Dejucq N, Jegou B (2001) Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev 65: 208-231.
86. Delwart EL, Mullins JI, Gupta P, Learn GH Jr, Holodniy M, et al. (1998) Human immunodeficiency virus type 1 populations in blood and semen. J Virol 72: 617-623.
87. Paranjpe S, Craigo J, Patterson B, Ding M, Barroso P, et al. (2002) Subcompartmentalization of HIV-1 Quasispecies between Seminal Cells and Seminal Plasma Indicates Their Origin in Distinct Genital Tissues. AIDS Res Hum Retroviruses 18: 1271-1280.
88. Setchell BP, Brooks DE (1988) Anatomy, vasculature, innervation and fluids of the male reproductive tract; Knobil E, Neill JD, eds. New York: Raven Press. pp 753-836.
89. Behre HM, Nieschlag E, Meschede D (1997) Disease of the seminal ducts. In: Nieschlag E, Behre HM, eds. Andrology, male reproductive health and dysfunction. Heidelberg: Springer-Verlag. pp 163-172.
90. Bomsel M, Alfsen A (2003) Entry of viruses through the epithelial barrier: pathogenic trickery. Nat Rev Mol Cell Biol 4: 57-68.
91. Wolff H (1995) The biologic significance of white blood cells in semen. Fertil Steril 63: 1143-1157.
92. Smith DM, Kingery JD, Wong JK, Ignacio CC, Richman DD, et al. (2004) The prostate as a reservoir for HIV-1. Aids 18: 1600-1602.
93. 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.
94. Anderson DJ, Politch JA, Martinez A, Van Voorhis BJ, Padian NS, et al. (1991) White blood cells and HIV-1 in semen from vasectomised seropositive men Lancet 338: 573-574.
95. Wolff H, Anderson DJ (1988) Immunohistologic characterization and quantitation of leukocyte subpopulations in human semen. Fertil Steril 49: 497-504.
96. 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.
97. Shevchuk MM, Nuovo GJ, Khalife G (1998) HIV in testis: quantitative histology and HIV localization in germ cells. J Reprod Immunol 41: 69-79.
98. Muciaccia B, Uccini S, Filippini A, Ziparo E, Paraire F, et al. (1998) Presence and cellular distribution of HIV in the testes of seropositive subjects: an evaluation by in situ PCR hybridization. FASEB J 12: 151-163.
99. Pudney J, Nguyen H, Xu C, Anderson D (1998) Microscopic evidence against HIV-1 infection of germ cells or attachment to sperm. J Reprod Immunol 41: 105-125.
100. Brogi A, Presentini R, Piomboni P, Collodel G, Strazza M, et al. (1995) Human sperm and spermatogonia express a galactoglycerolipid which interacts with gp120. J Submicrosc Cytol Pathol 27: 565-571.
101. Liu X, Zha J, Chen H, Nishitani J, Camargo P, et al. (2003) Human immunodeficiency virus type 1 infection and replication in normal human oral keratinocytes. J Virol 77: 3470-3476.
102. Delezay O, Koch N, Yahi N, Hammache D, Tourres C, et al. (1997) Co-expression of CXCR4/fusin and galactosylceramide in the human intestinal epithelial cell line HT-29. AIDS 11: 1311-1318.
103. Fantini J, Cook DG, Nathanson N, Spitalnik SL, Gonzalez-Scarano F (1993) Infection of colonic epithelial cell lines by type 1 human immunodeficiency virus is associated with cell surface expression of galactosylceramide, a potential alternative gp120 receptor. Proc Natl Acad Sci U S A 90: 2700-2704.
104. Willey S, Roulet V, Reeves JD, Kergadallan M-L, Thomas E, et al. (2003) Human Leydig cells are productively infected by some HIV-2 and SIV strains but not by HIV-1. AIDS 17: 183-188.
105. Rivenson A, Ohmori T, Hamazaki M, Madden R (1981) Cell surface recognition: spontaneous identification of mouse Leydig cells by lymphocytes, macrophages and eosinophils. Cell Mol Biol Incl Cyto Enzymol 27: 49-56.
106. Hales DB (2002) Testicular macrophage modulation of Leydig cell steroidogenesis. J Reprod Immunol 57: 3-18.
107. Bujan L, Sergerie M, Moinard N, Martinet S, Porte L, et al. (2007) Decreased semen volume and spermatozoa motility in HIV-1 infected patients under antiretroviral treatment. J Androl 28: 444-452.
108. Garrido N, Meseguer M, Remohi J, Simon C, Pellicer A (2005) Semen characteristics in human immunodeficiency virus (HIV)- and hepatitis C (HCV)-seropositive males: predictors of the success of viral removal after sperm washing. Hum Reprod 20: 1028-1034.
109. Nicopoullos JD, Almeida PA, Ramsay JW, Gilling-Smith C (2004) The effect of human immunodeficiency virus on sperm parameters and the outcome of intrauterine insemination following sperm washing. Hum Reprod 19: 2289-2297.