Immunomodulation by human seminal plasma: A benefit for spermatozoon and pathogen?

Human Reproduction

Volumn 12, Issue 10, 1997, Pages 2200-2207

  W Kelly, Rodney ^a   Critchley, Hilary O D ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cytokines; Immunomodulation; Prostaglandins; Seminal plasma; Sexually transmitted disease

Indexed keywords

COMPLEMENT INHIBITOR; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 12; POLYAMINE; PROSTAGLANDIN; PROSTAGLANDIN E; SPERM ANTIGEN; SPERMIDINE; SPERMINE;

ANTIGEN PRESENTING CELL; CELL SURVIVAL; CELLULAR IMMUNITY; FEMALE; FEMALE GENITAL SYSTEM; FERTILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOMODULATION; MALE; PAPILLOMA VIRUS; REVIEW; SEMINAL PLASMA; SEXUALLY TRANSMITTED DISEASE; SPERM; SPERMATOZOON; UTERINE CERVIX CARCINOMA;

HUMAN IMMUNODEFICIENCY VIRUS; PAPILLOMAVIRUS;

EID: 0030844074     PISSN: 02681161     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.humrep.a019559     Document Type: Review

References (100)

1. Alexander, N.J. and Anderson, D.J. (1987) Immunology of semen. Fertil. Steril., 47, 192-205.
2. Allen, R.D. and Roberts, T.K. (1986) Seminal plasma immunosuppression: an irrelevant biological phenomenon? Clin. Reprod. Fertil., 4, 353-355.
3. Bankhurst, A.D. (1982) The modulation of human natural killer cell activity by prostaglandins. J. Clin. Lab. Immunol., 7, 85-91.
4. Barker, E., Mackewicz, C.E. and Levy, J.A. (1995) Effects of T(h)1 and T(h)2 cytokines on CDS(+) cell response against human-immunodeficiency-virus - implications for long-term survival. Proc, Natl Acad. Sci. USA, 92, 11135-11139.
5. Barratt, C.L.R. (1997) Hypothesis to unify an embryonic defence system and HIV infection. Mol. Hum. Reprod., 3, 81-82.
6. Barrera, S., Lai, J., Fiocchi, C. and Roche, J.K. (1996) Regulation by prostaglandin E(2) of interleukin release by T-lymphocytes in mucosa. J. Cell. Physiol., 166, 130-137.
7. Belley, A. and Chadee, K. (1995) Eicosanoid production by parasites: from pathogenesis to immunomodulation? Parasitol. Today, 11, 327-334.
8. Betz, M. and Fox, B.S. (1991) Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J. Immunol., 146, 108-113.
9. Bogdan, C., Paik, J., Vodovotz, Y. and Nathan, C. (1992) Contrasting mechanisms for suppression of macrophage cytokine release by TGFβ and IL-10. J. Biol. Chem., 267, 23301-23308.
10. Brown, C.Y., Lagnado, C.A., Vadas, M.A. and Goodall, G.J. (1996) Differential regulation of the stability of cytokine mRNAs in lipopolysaccharide-activated blood monocytes in response to interleukin-10. J. Biol. Chem., 271, 20108-20112.
11. Chehimi, J., Starr, S.E., Frank, I. et al. (1992) Natural Killer (NK) cell stimulatory factor increases the cytotoxic activity of NK cells from both healthy donors and human immunodeficiency virus infected patients. J. Exp. Med., 175, 789-796.
12. Clark, G. F., Dell, A., Morris, H. R. et al. (1997) Viewing AIDS from a glycobiological perspective: potential linkages to the human fetoembryonic defence system hypothesis. Mol. Hum. Reprod., 3, 5-13.
13. Ding, L., Linsley, P.S., Huang, L.Y. et al. (1993) IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol., 151, 1224-1234.
14. Evans, C.H., Lee, T.S. and Flugelman, A.A. (1995) Spermine-directed immunosuppression of cervical-carcinoma cell sensitivity to a majority of lymphokine-activatcd killer lymphocyte cytotoxicity. Natural Immun., 14, 157-163.
15. Fënichel, P., Cervoni, F., Hofmann, P. et al. (1994) Expression of the complement regulatory protein CD59 on human spermatozoa: characterization and role in gametic interaction. Mol. Reprod. Dev., 38, 338-346.
16. Ghanekar, S., Zheng, L., Logar, A. et al. (1996) Cytokine expression by human peripheral-blood dendritic cells stimulated in-vitro with HIV-1 and herpes-simplex virus. J. Immunol., 157, 4028-4036.
17. Grossman, C.J., Wiseman, J., Lucas, F.S. et al. (1995) Inhibition of constitutive and inducible cyclooxygenase activity in human platelets and mononuclear cells by NSAIDs and cox-2 inhibitors. Inflammation Res., 44, 253-257.
18. Groux, H., Bigler, M., de Vries, J.E. and Roncarolo, M.G. (1996) Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells. J. Exp. Med., 184, 19-29.
19. Guidotti, L.G. and Chisari, F.V. (1996) To kill or to cure: options of host defense against viral infection. Curr. Opin. Immunol., 8, 478-483.
20. Hilkens, C.M.U., Snijders, A., Snijdewint, F.G.M. et al. (1996) Modulation of T-cell cytokine secretion by accessory cell-derived products. Eur. Resp. J., 9, S 90-S 94.
21. Humes, J.L., Bonney, R.W., Pelus, L. et al. (1977) Macrophages synthesize and release prostaglandins in response to inflammatory stimuli. Nature, 269, 149-151.
22. Ibata, B., Parr, E.L., King, N.J.C. and Parr, M.B. (1997) Migration of foreign lymphocytes from the mouse vagina into cervicovaginal mucosa and to the iliac lymph nodes. Biol. Reprod., 56, 537-543.
23. Imade, G.E., Baker, H.W.G., deKretser, D.M. and Hedger, M.P. (1997) Immunosuppressive activities in seminal plasma of infertile men: relationship to sperm antibodies and autoimmunity. Hum. Reprod., 12, 256-262.
24. James, K. and Hargreave, T.B. (1984) Immunosuppression by seminal plasma and its possible clinical significance. Immunol. Today, 5, 357-363.
25. James, K. and Skibinski, G. (1995) Immunosuppressive factors in human seminal plasma: their effects, characterization and possible mode of action. In Kurpisz, M. and Fernandez, N. (eds), Immunology of Human Reproduction. Bios Scientific, Oxford, pp. 267-283.
26. Kajino, T. Torry, D.S., McIntyre, J.A. and Faulk, W.P. (1988) Trophoblast antigens in human seminal plasma. Am. J. Reprod. Immunol., 17, 91-95.
27. Karp, C.L., Wysocka, M., Wahl, L.M. et al. (1996) Mechanism of suppression of cell-mediated-immunity by measles-virus. Science, 273, 228-231.
28. Katamura, K., Shimaku, N., Yamauchi, Y. et al. (1995) Prostaglandin E2 at priming of naive CD4+ T cells inhibits acquisition of ability to produce IFNγ and IL-2, but not IL-4 and IL-5. J. Immunol., 155, 4604-4612.
29. Kelly, R.W. (1995) Immunosuppressive mechanisms in semen: implications for contraception. Hum. Reprod., 10, 1686-1693.
30. Kelly, R.W., Taylor, PL., Hearn, J.P. et al. (1976) 19-Hydroxy prostaglandin El as a major component of the semen of primates. Nature, 260, 544-555.
31. Kelly, R.W., Holland, P., Skibinski, G. et al. (1991) Extracellular organelles (prostasomes) are immunosuppressive components of human semen. Clin. Exp, Immunol., 86, 550-556.
32. Kelly, R.W., Carr, G.C. and Critchley, H.O.D. (1997) A cytokine switch induced by human seminal plasma: an immune modulation with implications for sexually transmitted disease. Hum. Reprod., 12, 677-681.
33. King, C.L., Medhat, A., Malhotra, I. et al, (1996) Cytokine control of parasite-specific anergy in human urinary schistosomiasis - IL-10 modulates lymphocyte-reactivity. J. Immunol., 156, 4715-4721.
34. Koch, F., Stanzl, U., Jennewein, P. et al. (1996) High level IL-12 production by murine dendritic cells: up regulation via MHC class II and CD40 molecules and down regulation by IL-4 and IL-10. J. Exp. Med., 184, 741-746.
35. Kraan, T.C.T.M.V., Boeije, L.C.M., Smeenk, R.J.T. et al. (1995) Prostaglandin- E2 is a potent inhibitor of human interleukin-12 production. J. Exp. Med., 181, 775-779.
36. Kraan, T.C.T.M.V, Boeije, L.C.M., Snijders, A. et al. (1996) Regulation of IL-12 production by human monocytes and the influence of prostglandin E2. Ann. NY Acad. Sci., 795, 147-157.
37. Krause, D.S. and Deutsch, C. (1991) Cyclic AMP directly inhibits IL-2 receptor expression in human T cells: expression of both p55 and p75 subunits are affected. J. Immunol., 146, 2285-2294.
38. Kunkel, S.L., Chensue, S.W. and Phan, S.H. (1986) Prostaglandins as endogenous mediators of interleukin 1 production. J. Immunol., 136, 186-192.
39. Lea, R. G., Porat, O., Daya, S. et al. (1991) The detection of spermine and spermidine in human in vitro fertilization supernatants and their relation to early embryo-associated suppressor activity. Fertil, Steril., 56, 771-775.
40. Le Calvé, M., Segalen, J., Quernee, D. et al. (1995) Diamine oxidase activity and biochemical markers in human seminal plasma. Hum. Reprod., 10. 1141-1144.
41. Leung, K.H. (1989) Inhibition of human NK cell and LAK cell cytotoxicity and differentiation by PGE2. Cell, Immunol., 123, 384-395.
42. Leung, K.H. and Koren, H.S. (1982) Regulation of human natural killing: II. Protective effect of interferon on NK cells from suppression by PGE2. J. Immunol, 129, 1742-1747.
43. Levy, J.A. (1994) HIV and the Pathogenesis of AIDS. ASM Press, Washington, pp. 153-180.
44. Li, J., Yang, Y., Inoue, H. et al. (1996) Th expression of costimulatory molecules CD80 and CD86 in human carcinoma cell lines: its regulation by interferon γ and interleukin-10. Cancer Immunol. Immunother., 43, 213-219.
45. Liu, L.X., Serhan, C.N. and Weller, P.F. (1990) Intravascular filarial parasites elaborate cyclooxygenase-derived eicosanoids. J. Exp. Med., 172, 993-996.
46. Longo, N., Zabay, J.M., Sempere, J.M. et al. (1993) Altered production of PGE(2), IL-Iβ and TNFα by peripheral-blood monocytes from HIV-positive individuals at early stages of HIV-infection. J. Acquired Immune Deficiency Syndromes, 6, 1017-1023.
47. Maayan, R., Zukerman, Z. and Shohat, B. (1995) Oxidation of polyamines in human seminal plasma: a possible role in immunological infertility. Arch. Androl., 34, 95-99.
48. Macatonia, S.E., Hosken, N.A., Litton, M. et al. (1995) Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4(+) T-cells. J. Immunol, 154, 5071-5079.
49. Mannie, M.D., Prevost, K.D. and Marinakis, C.A. (1995) Prostaglandin E(2) promotes the induction of anergy during T-helper cell recognition of myelin basic-protein. Cell, Immunol., 160, 132-138.
50. Martinvilla, J.M., Luque, I., Martinezquiles, N. et al. (1996) Diploid expression of human-leukocyte antigen class-I and class-II molecules on spermatozoa and their cyclic inverse correlation with Inhibin concentration. Biol. Reprod., 55, 620-629.
51. Matzinger, P. (1994) Tolerance, danger, and the extended family. Annu. Rev. Immunol., 12, 991-1045.
52. Medzhitov, R. and Janeway, C.A. (1997) Innate immunity: impact on the adaptive immune repsonse. Curr. Opin. Immunol., 9, 4-9.
53. Melamed, D. and Friedman, A. (1993) Direct evidence for anergy in T lymphocytes tolerized by oral administration of ovalbumin. Eur, J. Immunol., 23, 935-942.
54. Mertz, P.M., DeWitt, D.L., Steiler Stevenson, W.G. and Wahl, L.M. (1994) Interleukin 10 suppression of monocyte prostaglandin H synthase-2. Mechanism of inhibition of prostaglandin-dependent matrix metalloproteinase production. J. Biol. Chem., 269, 21322-21329.
55. Miao, D., Skibinski, G. and James, K. (1996) The effects of human seminal plasma and PGE2 on mitogen induced proliferation and cytokine production of human splenic lymphocytes and peripheral blood mononuclear cells. J. Reprod. Immunol., 30, 97-114.
56. Miller, C.J., McChesney, M. and Moore, P.P. (1992) Langerhans cells, macrophages and lymphocyte subsets in the cervix and vagina of rhesus macaques. Lab. Invest., 67, 628-634.
57. Morel, A. S., Quaratino, S., Douek, D.C. and Londei, M. (1997) Split activity of interleukin-10 on antigen capture and antigen presentation by human dendritic cells: Definition of a maturative step. Eur. J. Immunol., 27, 26-34.
58. Mosmann, T.R. and Coffman, R.L. (1989) Heterogeneity of cytokine secretion patterns and functions of helper T cells. Adv. Immunol., 46, 111-147.
59. Naito, Y., Endo, H., Arai, K.I. et al. (1996) Signal-transduction in Th clones -target of differential modulation by PGE(2) may reside downstream of the PKC-dependent pathway. Cytokine, 8, 346-356.
60. Nakos, G. and Gossrau, R. (1994) Light-microscopic visualization of diamine oxidase using a cerium method. Eur. J. Histochem., 38, 13-22.
61. Naz, R.K. and Menge, A.C. (1994) Antisperm antibodies: origin, regulation. and sperm reactivity in human fertility. Fertil. Steril., 61, 1001-1013.
62. Nocera, M. and Chu, T.M. (1993) Transforming growth factor β as an immunosuppressive protein in human seminal plasma. Am. J. Reprod. Immunol., 30, 1-8.
63. Nokta, M.A., Hassan, M.I., Loesch, K. and Pollard, R.B. (1996) Human cytomegalovirus-induced immunosuppression - relationship to tumor necrosis factor-dependent release of arachidonic-acid and prostaglandin E(2) in human monocytes. J. Clin. Invent., 97, 2635-2641.
64. Pandya, I.J. and Cohen, J. (1985) The leukocytic reaction of the human uterine cervix to spermatozoa. Ferti. Steril., 43, 417-421.
65. Parr, M.B. and Parr, E.L. (1991) Langerhans cells and T lymphocyte subsets in the murine vagina and cervix. Biol. Reprod., 44, 491-498.
66. Phipps, R.P., Stein, S.H. and Roper, R.L. (1991) A new view of prostaglandin E regulation of the immune response. Immunol. Today, 12, 349-352.
67. Quan, C.P., Roux, C. Pillot, J. and Bouvet, J.-P. (1990) Delineation between T and B suppressive molecules from human seminal plasma: II Spermine is the major suppressor of T lymphocytes in vitro. Am. J. Reprod. Immunol., 22, 62-69.
68. Quayle, A.J., Kelly, R.W., Hargreave, T.B. and James, K. (1989) Immunosuppression by seminal prostaglandins. Clin. Exp. Immunol., 75, 387-391.
69. Rappaport, R.S. and Dodge, G.R. (1982) Prostaglandin E inhibits the production of interleukin-2. J. Exp. Med., 155, 943-948.
70. Robillard, P.Y., Hulsey, T.C., Périanin, J. et al. (1994) Association of pregnancy induced hypertension with duration of sexual cohabitation before conception. Lancet, 344, 973-975.
71. Romagnani, S. (1994) Lymphokine production by human T cells in disease states. Annu. Rev. Immunol., 12, 227-257.
72. Ronquist, G. and Stegmayr, B. (1982) Promotive effect on human sperm progressive motility by prostasomes. Urol. Res., 10, 253-257.
73. Rooney, I.A., Heuser, J.E. and Atkinson, J.P. (1996) GPI-anchored complement regulatory proteins in seminal plasma - an analysis of their physical condition and the mechanisms of their binding to exogenous cells. J. Clin. Invest., 97, 1675-1686.
74. Rooney, I.A., Atkinson, J.P, Krul, E.S. et al. (1993) Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J. Exp. Med., 177, 1409-1420.
75. Roper, R.L., Conrad, D.H., Brown, D.M. et al. (1990) Prostaglandin E2 promotes IL-4 induced IgE and IgG-1 synthesis. Journal of Immunology, 145, 2644-2651.
76. Rubinstein, S. and Breitbart, H. (1994) Cellular localization of polyamines: cytochemical and ultrastructural methods providing new clues to polyamine function in ram spermatozoa. Biol. Cell, 81, 177-183.
77. Sana, B., Das, G., Vohra, H. et al. (1994) Macrophage-T cell interaction in experimental mycobacterial infection. Selective regulation of co-stimulatory molecules on mycobacterium-infected macrophages and its implication in the suppression of cell-mediated immune response. Eur. J. Immunol., 24, 2618-26124.
78. Saifuddin, M., Parker, C. J., Peoples, M. E. et al. (1995) Role of virion-associated glycosylphosphatidylinositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1. J. Exp. Med., 182, 501-509.
79. Simpson, K.L. and Holmes, C.H. (1994) Differential expression of complement regulatory proteins decay-accelerating factor (CD55), membrane cofactor protein (CD46) and CD59 during human spermatogenesis. Immunology, 81, 452-461.
80. Soto-Ramirez, L.E., Renjifo, B., McLane, M.F. et al. (1996) HIV-1 Langerhans' cell tropism associated with heterosexual transmission of HIV. Science, 271, 1291-1293.
81. Southan, G.J., Szabo, C. and Thiemermann, C. (1994) Inhibition of the induction of nitric-oxide synthase by spermine is modulated by aldehyde dehydrogenase. Biochem. Biophys. Res. Commun., 203, 1638-1644.
82. Spira, A.I., Marx, P.A., Patterson, B.K. et al. (1996) Cellular targets of Infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J. Exp. Med., 183, 215-225.
83. Strassmann, G., Patil Koota, V., Finkelman, F. et al. (1994) Evidence for the involvement of interleukin 10 in the differential deactivation of murine peritoneal macrophages by prostaglandin E2. J. Exp. Med., 180, 2365-2370.
84. Sturgeon, S.R., Curtis, R.E., Johnson, K. et al. (1996) Second primary cancers after vulvar and vaginal cancers. Am. J. Obstet. Gynecol., 174, 929-933.
85. Suzuki, T., Tahara, H., Narula, S. et al. (1995) Viral imerleukin-10 (IL-10), the human herpes-virus-4 cellular IL-10 homolog, induces local anergy to allogeneic and syngeneic tumors. J. Exp. Med., 182, 477-486.
86. Szabo, C., Southan, G.J., Thiemermann, C. and Vane, J.R. (1994a) The mechanism of the inhibitory effect of polyamines on the induction of nitricoxide synthase - role of aldehyde metabolites. Br. J. Pharmacol., 113, 757-766.
87. Szabo, C., Southan, G.J., Wood, E. et al. (1994b) Inhibition by spermine of the induction of nitric-oxide synthase in J774.2 macrophages - requirement of a serum factor. Br. J. Pharmacol., 112, 355-356.
88. Szabo, S.J., Jacobson, N.C., Dighe, A.S. et al. (1995) Developmental commitment to the Th2 lineage by extinction of IL-12 signalling. Immunity, 2, 665-675.
89. Taga, K. and Tosato, G. (1992) IL-10 inhibits human T cell proliferation and IL-2 production. J. Immunol., 148, 1143-1148.
90. Tarter, T.H., Cunningham-Rundles, S. and Koide, S.S. (1986) Suppression of natural killer cell activity by human seminal plasma in vitro: identification of 19-OH-PGE as the suppressor factor. J. Immunol, 136, 2862-2867.
91. Taylor, P.L. and Kelly, R.W. (1974) 19-hydroxylated E prostaglandins as the major prostaglandins of human semen. Nature, 250, 665-667.
92. Templeton, A.A., Cooper, I. and Kelly, R.W. (1978) Prostaglandin concentrations in the semen of fertile men. J. Reprod. Fertil., 52, 147-150.
93. Thaler, C.J. (1989) Immunological role for seminal plasma in insemination and pregnancy. Am. J. Reprod. immunol., 21, 147-150.
94. Thaler, C.J. and McIntyre, J.A. (1990) Fetal wastage and nonrecognition of human pregnancy. Immunol. Allergy Clin. North Am., 10, 79-102.
95. Thomas, T., Gunnia, U.B., Yurkow, E.J. et al. (1993) Inhibition of calcium signalling in murine splenocytes by polyamines: differential effects on CD4 and CD8 T-cells. Biochem. 7., 291, 375-381.
96. Thomas, T.J., Gunnia, U.B., Seibold, J.R. and Thomas, T. (1995) Defective signal-transduction pathways in T-cells from autoimmune MRL-lpr/lpr mice are associated with increased polyamine concentrations. Biochem. J., 311, 175-182.
97. Trinchieri, G. and Gerosa, F. (1996) Immunoregulation by interleukin-12. J. Leukocyte Biol., 59, 505-511.
98. Viera, P., deWaal-Malefyt, R., Dang, M.N. et al. (1991) Isolation and expression of human cytokine synthesis inhibitory factor cDNA clones: homology to Epstein-Barr virus open reading frame BCRF1. Proc. Natl Acad. Sci. USA, 88, 1172-1176.
99. Vince, G.S. and Johnson, P.M. (1995) Materno-fetal immunobiology in normal pregnancy and its possible failure in recurrent spontaneous abortion? Hum. Reprod., 10 (Suppl. 2), 107-113.
100. Wang, L., Goillot, E. and Tepper, R.I. (1994) IL-10 inhibits alloreactive cytotoxic T-lymphocyte generation in-vivo. Cell Immunol, 159, 152-169.