Role of semen in altering the balance between inflammation and tolerance in the female genital tract: Does it contribute to HIV risk?

Viral Immunology

Volumn 27, Issue 5, 2014, Pages 200-206

  Rametse, Cosnet L ^a   Olivier, Abraham J ^a   Masson, Lindi ^a   Barnabas, Shaun ^a,b   McKinnon, Lyle R ^a   Ngcapu, Sinaye ^c   Liebenberg, Lenine J ^c   Jaumdally, Shameem Z ^a   Gray, Clive M ^a,d   Jaspan, Heather B ^a   Passmore, Jo Ann S ^a,c,d  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b Institute of Infectious Disease and Molecular Medicine   (South Africa)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

^d NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE;

CELLULAR IMMUNITY; FEMALE GENITAL SYSTEM; FEMALE GENITAL TRACT INFLAMMATION; HETEROSEXUALITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INFECTION RISK; MICROFLORA; MUCOSAL IMMUNITY; PROTEIN EXPRESSION; REVIEW; SEMEN ANALYSIS; SEMINAL PLASMA; SEXUAL TRANSMISSION; SPERM; T LYMPHOCYTE; FEMALE; IMMUNOLOGY; MALE; TRANSMISSION; VIROLOGY;

FEMALE; GENITALIA, FEMALE; HIV INFECTIONS; HUMANS; IMMUNE TOLERANCE; MALE; SEMEN;

EID: 84901975091     PISSN: 08828245     EISSN: 15578976     Source Type: Journal    
DOI: 10.1089/vim.2013.0136     Document Type: Review

References (76)

1. Abbas AK, and Lichtman AH. Cytokines. In: Abbas AK, and Lichtman AH, eds. Cellular and Molecular Immunology. 6th ed. Philadelphia: Elsevier and Saunders, 2007:243-274.
2. Anderson D, Politch JA, and Pudney J. HIV infection and immune defense of the penis. Am J Reprod Immunol 2011;202:333-336.
3. Arck PC, Ferrick DA, Steele-Norwood D, Croitoru K, and Clark DA. Murine T cell determination of pregnancy outcome. Effect of strain, ab T cell receptor, cd T cell receptor and cd T cell subsets. Am J Reprod Immunol 1997;37:492-502.
4. Baeten JM, Kahle E, Lingappa JR, et al. Genital HIV-1 RNA predicts risk of heterosexual HIV-1 transmission. Sci Transl Med 2011;3:77.
5. Battersby S, Sales KJ, Williams AR, Anderson RA, Gardner S, and Jabbour HN. Seminal plasma and prostaglandin E2 up-regulate fibroblast growth factor 2 expression in endo-metrial adenocarcinoma cells via E-series prostanoid-2 receptor-mediated transactivation of the epidermal growth factor receptor and extracellular signal-regulated kinase pathway. Hum Reprod 2007;22:36-44.
6. Belkaid Y, Bouladoux N, and Hand TW. Effector and memory T cell responses to commensal bacteria. Trends Immunol 2013;34:299-306.
7. Camejo MI. Relation between immunosuppressive Pge 2 and Il-10 to pro-inflammatory Il-6 in seminal plasma of infertile and fertile men. Syst Biol Reprod Med 2003;49: 111-116.
8. Carias AM, McCoombe S, McRaven M, et al. Defining the interaction of HIV-1 with the mucosal barriers of the female reproductive tract. J Virol 2013;87:11388-11400.
9. Chahroudi A, and Silvestri G. Interleukin-7 in HIV path-ogenesis and therapy. Eur Cyt Net 2010;21:202-207.
10. Coleman JS, Hitti J, Bukusi EA, et al. Infectious correlates of HIV-1 shedding in the female upper and lower genital tracts. AIDS 2007;21:755-759.
11. Cone RA, Hoen T, Wong X, Abusuwwa R, Anderson DJ, and Moench TR. Vaginal microbicides: detecting toxicities in vivo that paradoxically increase pathogen transmission. BMC Infect Dis 2006;6:90.
12. Denison FC, Grant VE, Calder AA, and Kelly RW. Seminal plasma components stimulate interleukin-8 and interleukin-10 release. Mol Hum Reprod 1999;5:220-226.
13. Eschenbach DA, Patton DL, Hooton TM, et al. Effects of vaginal intercourse with and without a condom on vaginal flora and vaginal epithelium. J Infect Dis 2001;183:913-918.
14. Faas M, Bouman A, Moes H, Heineman MJ, de Leij L, and Schuiling G. The immune response during the luteal phase of the ovarian cycle: a Th2-type response? Fert Steril 2000;74:1008-1013.
15. Fiore JR, Suligoi B, Saracino A, et al. Correlates of HIV-1 shedding in cervicovaginal secretions and effects of anti-retroviral therapies. AIDS 2003;17:2169-2176.
16. Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat Rev Immunol 2008;8: 737-744.
17. Fong AM, Robinson LA, Steeber DA, et al. Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow. J Exp Med 1998;188:1413-1419.
18. Foxman B, Zhang L, Tallman P, et al. Transmission of uropathogens between sex partners. J Infect Dis 1997;175: 989-992.
19. Fredricks DN, Fiedler TL, and Marrazzo JM. Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 2005;353:1899-1911.
20. Fung KY, Glode LM, Green S, et al. A comprehensive characterization of the peptide and protein constituents of human seminal fluid. Prostate 2004;61:171-181.
21. Gallo MF, Warner L, King CC, et al. Association between semen exposure and incident bacterial vaginosis. Infect Dis Obs Gynecol 2011;842652.
22. Garcia-Closas M, Herrero R, Bratti C, et al. Epidemiologic determinants of vaginal pH. Am J Obstet Gynaecol 1999; 180:1060-1066.
23. Goswami B, Rajappa M, Sharma M, and Sharma A. Inflammation: its role and interplay in the development of cancer, with special focus on gynecological malignancies. Int J Gynecol Cancer 2008;18:591-599.
24. Gupta K, and Klasse PJ. How do viral and host factors modulate the sexual transmission of HIV? Can transmission be blocked? PLoS Med 2006;3:e79.
25. Guerin LR, Prins JR, and Robertson SA. Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? Hum Reprod Update 2009;15:517-535.
26. Guerin LR, Moldenhauer LM, Prins JR, Bromfield JJ, Hayball JD, and Robertson SA. Seminal fluid regulates accumulation of FOXP3 regulatory T cells in the preim-plantation mouse uterus through expanding the FOXP3 cell pool and CCL19-mediated recruitment. Biol Reprod 2011;85:397-408.
27. Haase AT. Targeting early infection to prevent HIV-1 mucosal transmission. Nature 2010;464: 217-223.
28. Hooton TM, Hillier S, Johnson C, Roberts PL, and Stamm WE. Escherichia coli bacteriuria and contraceptive method. JAMA 1991;265:64-69.
29. Horbul JE, Schmechel SC, Miller BRL, Rice SA, and Southern PJ. Herpes simplex virus-induced epithelial damage and susceptibility to human immunodeficiency virus type 1 infection in human cervical organ culture. PLoS One 2011;6:e22638.
30. Janczewski Z, and Bablok L. Semen characteristics in pubertal boys. Arch Androl 1985;15:199-205.
31. Kachkache M, and Garabedian M. Hormonal and local factors control the immunohistochemical distribution of immunocytes in the rat uterus before conceptus implantation: effects of ovariectomy, fallopian tube section, and injection. Biol Reprod 1991;868:860-868.
32. Kelly RW, and Critchley HO. Immunomodulation of human seminal plasma: a benefit for spermatozoan and pathogen? Hum Reprod 1995;12:2200-2207.
33. Khan KN, Kitajima M, Hiraki K, et al. Effect of human seminal fluid on the growth of endometrial cells of women with endometriosis. Eur J Obstet Gynecol Reprod Biol 2010;149:204-209.
34. Lawn SD, Butera ST, and Folks TM. Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin Mi-crobiol Rev 2001;14:753-777.
35. LeGoff J, Weiss HA, Gresenguet G, et al. Cervicovaginal HIV-1 and herpes simplex virus type 2 shedding during genital ulcer disease episodes. AIDS 2007;21:1569-1578.
36. Lisco A, Munawwar A, Introini A, et al. Semen of HIV-1-infected individuals: local shedding of herpesviruses and reprogrammed cytokine network. J Infect Dis 2012;205: 97-105.
37. Male D. Mechanisms of innate immunity. In: Male D, Brostoff J Roth DB, and Roitt I, eds. Immunology. 7th ed. Mosby Elsevier, London; 2006; p.43.
38. Mayer KH, Boswell S, Goldstein R, et al. Persistence of human immunodeficiency virus in semen after adding in-dinavir to combination antiretroviral therapy. Clin Infect Dis 1999;28:1252-1259.
39. Moldenhauer LM, Keenihan SN, Hayball JD, and Robertson S. GM-CSF is an essential regulator of T cell activation competence in uterine dendritic cells during early pregnancy in mice. J Immunol 2010;185:7085-7096.
40. Morrison C, Fichorova R, Mauck C, et al. Cervical inflammation and immunity associated with hormonal contraception, pregnancy and HIV-1 seroconversion. J Acquir Imm Def Syndr 2014 Jan 9. doi: 10.1097/QAI. 0000000000000103. [Epub ahead of print]
41. Mueller YM, and Katsikis PD. IL-15 in HIV infection: pathogenic or therapeutic potential? Eur Cyt Net 2010;21: 219-221.
42. Muller M, Sales KJ, Katz A, and Jabbour HN. Seminal plasma promotes the expression of tumorigenic and an-giogenic genes in cervical adenocarcinoma cells via the E-series prostanoid 4 receptor. Endocrinology 2006;147: 3356-3365.
43. Murphy K, Irvin SC, and Herold BC. Research gaps in defining the biological link between HIV risk and hormonal contraception. Am J Reprod Immunol 2014 Feb 19. doi: 10.1111/aji.12209. [Epub ahead of print]
44. Nkwanyana NN, Gumbi PP, Roberts L, et al. Impact of HIV-1 infection and inflammation on composition and yield of cervical mononuclear cells in the female genital tract. Immunol 2009;128:e746-757.
45. O'Hanlon DE, Lanier BR, Moench TR, and Cone RA. Cervicovaginal fluid and semen block the microbicidal activity of hydrogen peroxide produced by vaginal lacto-bacilli. BMC Infect Dis 2010;10:120.
46. O'Leary S, Jasper MJ, Warnes GM, Armstrong DT, and Robertson S. Seminal plasma regulates endometrial cyto-kine expression, leukocyte recruitment and embryo development in the pig. Reproduction 2004;128:237-247.
47. Olivier AJ, Masson L, Ronacher K, et al. Distinct cytokine patterns in semen influence local HIV shedding and HIV target cell activation. J Infect Dis 2014;209:1174-1184.
48. Patton DL, Thwin SS, Meier A, Hooten TM, Stapleton AE, and Eschenbach DA. Epithelial cell layer thickness and immune cell populations in the normal human vagina at different stages of the menstrual cycle. Am J Obstet Gy-necol 2000;183:967-973.
49. Pendergrass PB, Belovicz MW, and Reeves CA. Surface area of the human vagina as measured from vinyl poly-siloxane casts. Gynecol Obstet Invest 2003;55:110-113.
50. Pierucci-Alves F, Yi S, and Schultz BD. Transforming growth factor beta 1 induces tight junction disruptions and loss of transepithelial resistance across porcine vas deferens epithelial cells. Biol Reprod 2012;86:36.
51. Pilch B, and Mann M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 2006;7:R40.
52. Politch JA, Tucker L, Bowman FP, and Anderson DJ. Concentrations and significance of cytokines and other immunologic factors in semen of healthy fertile men. Hum Reprod 2007;22: 2928-2935.
53. Pudney J, Quayle AJ, and Anderson DJ. Immunological microenvironments in the human vagina and cervix: mediators of cellular immunity are concentrated in the cervical transformation zone. Biol Reprod 2005;73:1253-1263.
54. Purcell D, Cunningham A, Turville S, Tachedjian G, and Landay A. Biology of mucosally transmitted sexual infection-translating the basic science into novel HIV intervention: a workshop summary. AIDS Res Hum Retroviruses 2012;28:1389-1396.
55. Rehan N, Sobrero AJ, and Fertig JW. The semen of fertile men: statistical analysis of 1300 men. Fertil Steril 1975; 26:492-502.
56. Roberts AW. G-CSF: a key regulator of neutrophil production, but that's not all! Growth Factors 2005;23:33-41.
57. Robertson SA, Allanson M, and Mau VJ. Molecular regulation of uterine leukocyte recruitment during early pregnancy in the mouse. Placenta 1998;19:101-119.
58. Robertson SA, Ingman WV, O'Leary S, Sharkey DJ, and Tremellen KP. Transforming growth factor beta-a mediator of immune deviation in seminal plasma. J Reprod Immunol 2002;57:109-128.
59. Robertson SA. Seminal fluid signaling in the female reproductive tract: lessons from rodents and pigs. J Anim Sci 2007;85:E36-44.
60. Robertson SA, Guerin LR, Moldenhauer LM, and Hayball JD. Activating T regulatory cells for tolerance in early pregnancy-the contribution of seminal fluid. J Reprod Immunol 2009;83:109-116.
61. Robertson SA, O'Connell AC, Hudson SN, and Seamark RF. Granulocyte-macrophage colony-stimulating factor (GM-CSF) targets myeloid leukocytes in the uterus during the post-mating inflammatory response in mice. J Reprod Immunol 2000;46:131-154.
62. Sabatté J, Remes Lenicov F, Cabrini M, et al. The role of semen in sexual transmission of HIV: beyond a carrier for virus particles. Microbes Infect 2011;13:977-982.
63. Serhan CN. The resolution of inflammation: the devil in the flask and in the details. FASEB J 2011;25:1441-1448.
64. Sha BE, Zariffard MR, Wang QJ, et al. Female genital-tract HIV load correlates inversely with Lactobacillus species but positively with bacterial vaginosis and mycoplasma hominis. J Infect Dis 2005;191:25-32.
65. Sharkey DJ, Tremellen KP, Jasper MJ, Gemzell-Danielsson K, and Robertson SA. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol 2012;188: 2445-2454.
66. Sharkey DJ, Macpherson AM, Tremellen KP, and Robertson SA. Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol Hum Reprod 2007;13:491-501.
67. Sharkey DJ, Macpherson AM, Tremellen KP, Mottershead DG, Gilchrist RB, and Robertson SA. TGF-b mediates proinflammatory seminal fluid signaling in human cervical epithelial cells. J Immunol 2012;189:1024-1035.
68. Sheridan WP, Hunt P, Simonet S, and Ulrich TR. Hema-tological effects of cytokines. In: Remick DG, and Fried-land JS, eds. Cytokines in Health and Disease, 2nd ed. New York: Marcel Dekker, 1997:487-505.
69. Sutherland JR, Sales KJ, Jabbour HN, and Katz AA. Seminal plasma enhances cervical adenocarcinoma cell proliferation and tumour growth in vivo. PLoS One 2012; 7:e33848.
70. Tachet A, Dulioust E, Salmon D, et al. Detection and quantification of HIV-1 in semen: identification of a sub-population of men at high potential risk of viral sexual transmission. AIDS 1999;13:823-831.
71. Tremellen KP, Seamark RF, and Robertson SA. Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol Reprod 1998;58:1217-1225.
72. Van de Wijgert JH, Verwijs MC, Turner AN, and Morrison CS. Hormonal contraception decreases bacterial vaginosis but oral contraception may increase candidiasis: implications for HIV transmission. AIDS 2013;27:2141-2153.
73. Verstraelen H, Verhelst R, Vaneechoutte M, and Tem-merman M. The epidemiology of bacterial vaginosis in relation to sexual behavior. BMC Infect Dis 2010;10:81
74. Willeén M, Hoist E, Myhre EB, and Olsson AM. The bacterial flora of the genitourinary tract in healthy fertile men. Urology 1996;30:387-393.
75. Wolters-Everhardt E, Dony JM, Lemmens WA, et al. Buffering capacity of human semen. Fert Steril 1986;46: 114-119.
76. Zenclussen AC. Adaptive immune responses during pregnancy. Am J Reprod Immunol 2013;69:291-303.