Endometriosis and unexplained recurrent spontaneous abortion: Pathological states resulting from aberrant modulation of natural killer cell function?

Human Reproduction Update

Volumn 5, Issue 1, 1999, Pages 40-51

  Somigliana, E ^a   Vigano P ^a   Vignali, M ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Endometriosis; Natural killer cells; NK cells; Recurrent spontaneous abortion

Indexed keywords

CELL RECEPTOR; HLA G ANTIGEN;

CELL ACTIVITY; CELL FUNCTION; DECIDUA; ENDOMETRIOSIS; FEMALE; HUMAN; NATURAL KILLER CELL; PRIORITY JOURNAL; RECURRENT ABORTION; REVIEW; SPONTANEOUS ABORTION;

ABORTION, HABITUAL; ENDOMETRIOSIS; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; INFERTILITY, FEMALE; KILLER CELLS, NATURAL; PREGNANCY; UTERUS;

EID: 0033001886     PISSN: 13554786     EISSN: None     Source Type: Journal    
DOI: 10.1093/humupd/5.1.40     Document Type: Review

References (122)

1. Alsalili, M., Yuzpe, A., Tummon, I. et al. (1995) Cumulative pregnancy rates and pregnancy outcome after in-vitro fertilization: >5000 cycles at one centre. Hum. Reprod., 10, 470-474.
2. Altman, D.J., Scheneider, S.L., Thompson, D.A. et al. (1990) A transforming growth factor β2 (TGF-β2)-like immunosuppressive factor in amniotic fluid and localization of TGF-β2 mRNA in the pregnant uterus. J. Exp. Med., 172, 1391-1401.
3. Aoki, D., Katsuki, Y., Shimizu, A. et al. (1994) Successful heterotransplantation human endometrium in SClD mice. Obstet. Gynecol., 83, 220-228.
4. Aoki, K., Kajiura, S., Matsumoto, Y. et al. (1995) Preconceptional natural-killer-cell activity as a predictor of miscarriage. Lancet, 345, 1340-1342.
5. Arici, A., Oral, E., Bukulmez, O. et al. (1996) The effect of endometriosis on implantation: results from the Yale University in vitro fertilization and embryo transfer program. Fertil. Steril., 65, 603-607.
6. Beer, A.E., Kwak, J.Y.H. and Ruiz, J.E. (1996) Immunophenotypic profiles of peripheral blood lymphocytes in women with recurrent pregnancy losses and in infertile women with multiple failed in vitro fertilization cycles. Am. J. Reprod. Immunol., 35, 376-382.
7. Billington, W.D. (1988) Maternal-fetal interactions in normal human pregnancy. Baillieres Clin. Immunol. Allerg., 2, 527-549.
8. Biassoni, R., Cantoni, C., Falco, M. et al. (1996) The human leukocyte antigen (HLA)-C-specific 'activatory' natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmatic portions. J. Exp. Med., 183, 645-650.
9. Brinton, L.A., Gridley, G., Persson, I. et al. (1997) Cancer risk after hospital discharge diagnosis of endometriosis. Am. J. Obstet. Gynecol., 176, 572-579.
10. Brizek, C.L., Schlaff, S., Pellegrini, V.A. et al. (1995) Increased incidence of aberrant morphological phenoypes in human embryogenesis-an association with endometriosis. J. Assist. Reprod.Genet., 12, 106-112.
11. Braud, V.B., Allan, D.S.J., O'Callaghan, C.A. et al. (1998) HLA-E binds to natural killer cell receptors. Nature, 391, 795-799.
12. Busacca, M., Viganò, P., Magri, B. and Vignali, M. (1994) The adhesion molecules of human endometrial stromal cells. Immunological implications. Ann. N.Y. Acad. Sci., 734, 43-46.
13. Chao, K.H., Yang, Y.S., Ho, H.N. et al. (1995) Decidual natural killer cytotoxicity decreased in normal pregnancy but not in anembryonic pregnancy and recurrent spontaneous abortion. Am. J. Reprod. Immunol., 34, 274-280.
14. Chaouat, G., Menu, E., Clark, D.A. et al. (1990) Control of fetal survival in CBA DBA/2 by lymphokine therapy. J. Reprod. Fertil., 89, 447-458.
15. Clark, D.A. (1997) HLA-G finally does something! Am. J. Reprod. Immunol., 38, 75-78.
16. Clark, D.A. and Chaouat, G. (1989) What do we know about spontaneous abortion mechanisms? Am. J. Reprod. Immunol., 19, 28-37.
17. Clark, D.A. and Daya S. (1998) Is there hope for IVIG? Am. J. Reprod. Immunol., 39, 65-68.
18. Clark, D.A., Chapat, A. and Tutton, D. (1986) Active suppression of host-versus-graft reaction in pregnant mice. VII. Spontaneous abortion of allogeneic CBA/J, DBA/2 fetuses in the uterus of CBA/J mice correlates with deficient non-T cell suppressor cell activity. J. Immunol., 136, 1668-1675.
19. Clark, D.A., Flanders, K.L. and Banwatt, D. (1990) Murine pregnancy decidua produces a unique immunosuppressive molecule related to transforming growth factor β-2. J. Immunol., 144, 3008-3014.
20. Clark, D.A., Lea, R.G., Podor, T. et al. (1991) Cytokines determining the success or failure of pregnancy. Ann. N.Y. Acad. Sci., 629, 524-536.
21. Colonna, M., Navarro, F., Bellòn, T. et al. (1997) A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med., 186, 1809-1818.
22. Cornillie, F.J., Lauweryns, J.M., Seppala, M. et al. (1991) Expression of endometrial PP14 in pelvic and ovarian endometriotic implants. Hum. Reprod., 6, 1411-1415.
23. Coulam, C.B., Goodman, C., Roussev, R.G. et al. (1995) Systemic CD56+ cells can predict pregnancy outcome. Am. J. Reprod. Immunol., 33, 40-46.
24. Cross, J.C., Werb, Z. and Fisher, S.J. ( 1994) Implantation and the Placenta: key pieces of the development puzzle. Science, 266, 1508-1518.
25. D'Hooghe, T.M. and Hill, J.A. (1996) Immunobiology of endometriosis. In Bronson, R.A., Alexander, N.J., Anderson, D. et al. (eds), Reproductive Immunology. Blackwell Science, London, pp. 322-356.
26. Deniz, G., Christmas, S.E., Brew, R. and Johnson, P.M. (1994) Phenotypic and functional cellular differences between human CD3-decidual and peripheral blood leukocytes. J. Immunol., 152, 4255-4261.
27. Dicker, D., Goldman, J.A., Levy, T. et al. (1992) The impact of long-term gonadotropin-releasing hormone analogue treatment on preclinical abortions in patients with severe endometriosis undergoing in vitro fertilization-embryo transfer. Fertil. Steril., 57, 597-600.
28. Dmowski, W.P., Rana, N., Michalowska, J. et al. (1995) The effect of endometriosis, its stage and activity, and of autoantibodies on in vitro fertilization and embryo transfer success rates. Fertil. Steril., 63, 555-562.
29. Dmonski, W.P. ( 1997) Effect of autoantibodies on embryo implantation. In Minaguchi, H. and Sugimoto, O. (eds), Endometriosis Today: Advances in Research and Practice. Parthenon Publishing, London, pp. 123-131.
30. Dudley, D.J. (1996) The immunobiology of nidiation and implantation: novel regulation of innate and adaptive immunity. In Bronson, R.A., Alexander, N.J., Anderson, D. et al. (eds), Reproductive Immunology. Blackwell Science, London, pp. 359-382.
31. Edwards, R.G., Morcos, S., Magnamee, M. et al. (1991) High fecundity of amenorrhoic women in embryo-transfer programmes. Lancet, 338, 292-294.
32. Ferry, B.L., Starkey, P.M., Sargent, I.L. et al. (1990) Cell populations in the human early pregnancy decidua: natural killer activity and response to interleukin-2 of CD56-positive large granular lymphocytes. Immunology, 70, 446-452.
33. Fujino, Y., Nakamura, Y., Ueda, K. et al. (1997) Effects of serum from pregnant versus non-pregnant women on natural killer cell activity. Am. J. Reprod. Immunol., 37, 365-367.
34. Garzetti, G.G., Ciavattini, A., Provinciali, M. et al. (1993) Natural killer cell activity in endometriosis: correlation between serum estradiol levels and cytotoxicity. Obstet. Gynecol., 81, 665-668.
35. Geber, S., Paraschos, T., Atkinson, G. et al. (1995) Results of IVF in patients with endometriosis: the severity of the disease does not affect outcome, or the incidence of miscarriage. Hum. Reprod., 10, 1507-1511.
36. Giglio, T., Imro, M.A., Filaci, G. et al. (1994) Immune cell circulating subsets are affected by gonadal function. Life Sci., 54, 1305-1312.
37. Gillessen, S., Carvajal, D., Ling, P. et al. (1995) Mouse interleukin-12 p40 homodimer: a potent IL-12 antagonist Eur. J. Immunol., 25, 200-206.
38. Giudice, L.C., Tazuke, S.I. and Swiersz, L. (1998) Status of current research on endometriosis. J. Reprod. Med., 43, 252-262.
39. Haimovici, F., Hill, J.A. and Anderson, D.J. (1991) The effects of soluble products of activated lymphocytes and macrophages on blastocyst implantation events in vitro. Anticancer Res., 9, 167-171.
40. Hammer, A., Hutter, H. and Dohr, G. (1997) HLA class I expression on the materno-fetal interface. Am. J. Reprod. Immunol., 38, 150-157.
41. Halme, J.K. (1997) Role of peritoneal inflammation associated with infertility. In Minaguchi, H. and Sugimoto, O. (eds) Endometriosis Today: Advances in Research and Practice. Parthenon Publishing, London, pp. 132-137.
42. Hibi, S.E., King, A., Sharkey, A.M. and Loke, YW. (1997) Human uterine NK cells have a similar repertoire of killer inhibitory and activatory receptors to those found in blood, as demonstrated by RT-PCR and sequencing. Mol. Immunol., 34, 419-430.
43. Higuchi, K., Aoki, K., Kimbara, T. et al. (1995) Suppression of natural killer cell activity by monocytes following immunotherapy for recurrent spontaneous aborters. Am. J. Reprod. Immunol., 33, 221-227.
44. Hill, J.A. (1996) Immunologic factors in spontaneous abortion. In Bronson, R.A., Alexander, N.J., Anderson, D. et al. (eds), Reproductive Immunology. Blackwell Science, London, pp. 433-442.
45. Hill, J.A., Faris, H.M., Schiff, I. and Anderson, D.J. (1988) Characterization of leukocytes subpopulations in the peritoneal fluid of women with endometriosis. Fertil. Steril., 50, 216-222.
46. Hill, J.A., Polgar, K. and Anderson, D.J. (1995) T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. J. Am. Med. Assoc., 273, 1933-1936.
47. Hirata, J., Kikuchi, Y., Imaizumi, E. et al. (1994) Endometriotic tissues produce immunosuppressive factors. Gynecol. Obstet. Invest., 37, 43-47.
48. Ho, H.-N., Chao, K.-H., Chen, H.-F. et al. (1995) Peritoneal natural killer cytotoxicity and CD25+ CD3+ lymphocyte subpopulation are decreased in women with stage III-IV endometriosis. Hum. Reprod., 10, 2671-2675.
49. Ho, H.-N., Chao, K.-H., Chen, H.-F. et al.(1996) Activation status of T and NK cells in the endometrium throughout menstrual cycle and normal and abnormal early pregnancy. Hum. Immunol., 1, 130-136.
50. Ho, H.-N., Wu, M.-Y and Yang, Y-S. (1997a) Peritoneal cell immunity and endometriosis. Am. J. Reprod. Immunol., 38, 400-412.
51. Ho, H.-N., Wu, M.-Y, Chao, K.-H. et al. ( 1997b) Peritoneal interleukin-10 increases with decrease in activated CD4+ T lymphocytes in women with endometriosis. Hum. Reprod., 12, 2528-2533.
52. Hsu, C-C., Yang, B.-C., Wu, M.-H. and Huang, K.-E. (1997) Enhanced interleukin-4 expression in patients with endometriosis. Fertil. Steril., 67, 1059-1064.
53. Inoue, M., Kobayashi, Y, Honda, I. et al. (1992) The impact of endometriosis on the reproductive outcome of infertile patients. Am. J. Obstet. Gynecol., 167, 278-282.
54. Iwasaki, K., Makino, T., Maruyama, T. et al. (1993) Leukocyte subpopulations and natural killer activity in endometriosis. Int. J. Fertil., 38, 229-234.
55. Kanzaki, H., Wang, H.S., Kariya, M. and Mori, T. (1992) Suppression of natural killer cell activity by sera from patients with endometriosis. Am. J. Obstet. Gynecol., 167, 257-261.
56. Karre, K. (1995) Express yourself or die: peptides, MHC molecules and NK cells. Science, 276, 978-979.
57. Kelly, R.W. and Critchley, H.O.D. (1998) T-cell modulation in decidua. Immunol. Today, 19, 142-143.
58. Kenny, D.T. (1995) In vitro fertilisation and gamete intrafallopian transfer: an integrative analysis of research, 1987-1992. Br. J. Obstet. Gynecol., 102, 317-325.
59. King, A. and Loke, Y.W. (1990) Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell. Immunol., 129, 435-448.
60. King, A. and Loke, Y.W. (1991) On the nature and function of human uterine granular lymphocytes. Immunol. Today, 12, 432-435.
61. King, A., Burkby, C. and Loke, Y.W. (1989) Early human decidual cells exhibit NK activity against K 562 cell line but not against first trimester trophoblast. Cell. Immunol., 118, 337-344.
62. King, A., Hiby, S., Verma, T. et al. (1997) Uterine NK cells and trophoblast HLA class I molecules. Am. J. Reprod. Immunol., 37, 459-462.
63. Koninckx, P.R., Riittinen, L., Seppala, M. and Cornillie, F.J. (1992) CA-125 and placental protein 14 concentrations in plasma and peritoneal fluid of women with deeply infiltrating pelvic endometriosis. Fertil. Steril., 57, 523-530.
64. Krishnaraj, R. and Blandford, G. (1987) Age-associated alterations in human NK cells. Increased activity as per conventional and kinetic analysis. Clin. Immunol. Immunopathol., 45, 268-285.
65. Kwak, J.Y.H., Kwak, F.M.Y, Ainbinder, S.W. et al. (1996) Elevated peripheral blood natural killer cells are effectively suppressed by immunoglobulin G infusion in women with recurrent spontaneous abortions. Am. J. Reprod. Immunol., 35, 363-369.
66. Lala, P.K., Scodras, J.M., Graham, C.H. et al. (1990) Activation of maternal killer cells in the pregnant uterus with chronic indomethacin therapy, IL-2 therapy or a combination therapy is associated with embryonic demise. Cell Immunol., 127, 368-381.
67. Lanier, L.L. (1997) Natural killer cells: form no receptors to too many. Immunity, 6, 371-378.
68. Lanier, L.L. ( 1998) Follow the leader: NK cell receptors for classical and nonclassical MHC class I. Cell, 92, 705-707.
69. Lanier, L.L., Corliss, B. and Phillips, J.H. ( 1997) Arousal and inhibition of human NK cells. Immunol. Rev., 155, 145-154.
70. Lea, R.G., Underwood, J., Flanders, K.C. et al. (1995) A subset of patients with recurrent spontaneous abortion is deficient in transforming growth factor beta-2-producing suppressor cells in decidua near the placental attachment site. Am. J. Reprod. Immunol., 34, 52-61.
71. Lee, N., Llano, M., Carretero, M. et al. (1998) HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA, 95, 5199-5204.
72. Loke, Y.W. and King, A. (1995) Human implantation. In Cell biology and Immunology. Cambridge University Press, Cambridge, pp. 5-17.
73. Loke, Y.W. and King, A. (1996) Immunology of human implantation: an evolutionary perspective. Hum. Reprod., 11, 283-286.
74. Loke, Y.W., King, A. and Burrows, T.D. (1995) Decidua in human implantation. Hum. Reprod., 10 (Suppl. 2), 14-20.
75. Makida, R., Minami, M., Takamizawa, M. et al. (1991) Natural killer cell activity and immunotherapy for recurrent spontaneous abortion. Lancet, 338, 579-580.
76. Manetti, R., Parronchi, P., Giudizi, M.G. et al. (1993) Natural killer cell stimulatory factor (interleukin 12, IL-12) induces T helper type 1 (Thl)-specific immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med., 177, 1199-1204.
77. Marcus, S.F. and Edwards, R.G. (1994) High rates of pregnancy after long-term down-regulation of women with severe endometriosis. Am. J. Obstet. Gynecol., 171, 812-817.
78. Mattner, F., Fisher, S., Guckes, S. et al. (1993) The interleukin-12 subunit p40 specifically inhibits effects of the interleukin-12 heterodimer. Eur. J. Immunol., 23, 2202-2208.
79. Mazzeo, D., Viganò, P., Di Blasio, A.M. et al. (1998) Interleukin-12 and its free p40 subunit regulate immune recognition ofendometrial cells: potential role in endometriosis. J. Clin. Endocrinol Metab., 83, 911-916.
80. Medawar, P.B. (1953) Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. In Society for Experimental Biology, Vol. 7. Academic Press, New York, pp. 320-338.
81. Melioli, G., Semino, C., Semino, A. et al. (1993) Recombinant interleukin-2 corrects in vitro the immunological defect of endometriosis. Am. J. Reprod. Immunol., 30, 218-227.
82. Miron, P., Lachapelle, M.-H. and Roy, D.C. (1997) Endometrial immunology in endometriosis. In Bronson, R.A., Alexander, N.J., Anderson, D. et al. (eds), Reproductive Immunology. Blackwell Science, London, pp. 118-119.
83. Moretta, A., Sivori, S., Vitale, M. et al. (1995) Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J. Exp. Med., 182, 875-884.
84. Munz, C., Holmes, N., King, A. et al. (1997) Human histocompatibility leukocyte antigen (HLA)-G molecules inhibit NKAT3 expressing natural killer cells. J. Exp. Med., 185, 385-391.
85. Ober, C. ( 1998) HLA and pregnancy: the paradox of the fetal allograft. Am. J. Hum. Genet., 62, 1-5.
86. Oehninger, S., Acosta, A.A., Kreiner, D. et al. (1988) In vitro fertilization and embryo transfer (IVF/ET): an established and successful therapy for endometriosis. J. In Vitro Fertil. Embryo Transfer, 5, 249-256.
87. Olivennes, F., Feldberg, D., Liu, H.C. et al. (1995) Endometriosis: a stage-by-stage analysis-the role of in vitro fertilization. Fertil. Steril., 64, 392-398.
88. Oosterlynck, D.J., Cornillie, F.J., Waer, M. et al. (1991) Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil. Steril., 56, 45-51.
89. Oosterlynck, D.J., Meuleman, C., Waer, M. et al. (1992) The natural killer cell activity of peritoneal fluid is decreased in women with endometriosis. Fertil. Steril., 58, 290-295.
90. Oosterlynck, D.J., Meuleman, C., Waer, M. et al. (1993) Immunosuppressive activity of peritoneal fluid in women with endometriosis. Obstet. Gynecol., 82, 206-212.
91. Oosterlynck, D.J., Meuleman, C., Waer, M. et al. (1994) Transforming growth factor-β in peritoneal fluid of women with endometriosis.Obstet. Gynecol., 83, 287-290.
92. Osteen, K. (1997) Progesterone and transforming growth factor-β co-mediate matrix metalloproteinase expression in a model of endometriosis. In Minaguchi, H. and Sugimoto, O. (eds), Endometriosis Today: Advances in Research and Practice. Parthenon Publishing, London, pp. 200-209.
93. Pazmany, L., Mendelboim, O., Valès-Gomez, M. et al. (1996) Protection from natural killer cell-mediated lysis by HLA-G expression on target cells. Science, 274, 792-795.
94. Pende, D., Sivori, S., Accame, L. et al. (1997) HLA-G recognition by human natural killer cells. Involvement of CD94 both as inhibitory and as activating receptor complex. Eur. J. Immunol., 27, 1875-1880.
95. Perez-Villar, J.J., Melero, I., Navarro, F. et al. (1997) The CD94/NKG2-A inhibitory receptor complex is involved in natural killer cell-mediated recognition of cells expression HLA-Gl. J. Immunol., 158, 5736-5743.
96. Pross, H.F. and Brines, M.G. (1982) Studies of human NK cells. I. In vivo parameters affecting normal cytotoxic functions. Int. J. Cancer, 29, 383-390.
97. Raghupathy, R. ( 1997) Th1 -type immunity is incompatible with successful pregnancy. Immunol Today, 18, 478-482.
98. Renard, V, Cambiaggi, A., Vely, F. et al. (1997)Transduction of cytotoxic signals in natural killer cell: a general model of fine tuning between activatory and inhibitory pathway in lymphocytes. Immunol Rev., 155, 205-221.
99. Reyburn, H., Mandelboim, O., Vales-Gomez, M. et al. (1997) Human NK cells: their ligands, receptors and functions. Immunol. Rev., 155, 119-125.
100. Rouas-Freiss, N., Marchai, R.E., Kirszenbaum, M. et al. (1997a) The α1 domain of HLA-Gl and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors? Proc. Natl. Acad. Sci. USA, 94, 5249-5254.
101. Rouas-Freiss, N., Marchal-Bras Goncalves, R., Menier, C. and Carosella, E.D. (1997b) Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc. Natl. Acad. Sci. USA, 94, 11520-11525.
102. Ruiz, J.E., Kwak, J.Y.H., Baum, L. et al. (1996) Intravenous immunoglobulin inhibits natural killer cell activity in vivo in women with recurrent spontaneous abortion. Am. J. Reprod. Immunol., 35, 370-375.
103. Satoh, K., Tochigi, M. and Teng, J.M. (1997) Endometriosis and pain: the role of prostaglandins. In Minaguchi, H. and Sugimoto, O. (eds) Endometriosis Today: Advances in Research and Practice. Parthenon Publishing, London, pp. 75-79.
104. Semino, C., Semino, A., Pietra, G. et al. (1995) Role of major histocompatibility complex class I expression and natural killer-like T cells in the genetic control of endometriosis. Fertil. Steril., 64, 909-916.
105. Simon, C., Gutiérrez, A., Vidai, A. et al. (1994) Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum. Reprod., 9, 725-729.
106. Soderstrom, K., Corliss, B., Lanier, L.L. and Phillips, J.H. (1997) CD94/NKG2 is the predominant inhibitory receptor involved in recognition of HLA-G by decidual and peripheral blood NK cells. J. Immunol., 159, 1072-1075.
107. Somigliana, E., Viganò, P., Gaffuri, B. et al. (1996a) Modulation of NK cell lytic function by endometrial secretory factors: potential role in endometriosis. Am. J. Reprod. Immunol., 36, 296-300.
108. Somigliana, E., Viganò, P., Gaffuri, B. et al. (1996b) Endometrial stromal cells as a source of intercellular adhesion molecule (ICAM)-I molecules. Hum. Reprod., 11, 1190-1194.
109. Sung, L., Mukherjee, T., Takeshige, T. et al. (1997) Endometriosis is not detrimental to embryo implantation in oocyte recipients.J. Assist. Reprod. Genet., 14, 153-156.
110. Tan, S.L., Royston, P. and Campbell, S. (1992) Cumulative conception and livebirth rates after in vitro fertilization. Lancet, 339, 1390-1394.
111. Tanaka, E., Sendo, F, Kawagoe, S. and Hiroi, M. (1992) Decreased natural killer cell activity in women with endometriosis. Gynecol. Obstet. Invest., 34, 27-30.
112. Trinchieri, G. (1994) Interleukin-12: a cytokine produced by antigen-presenting cells with immunoregulatory functions in the generation of T-helper cells type-1 andcytotoxic lymphocytes. Blood, 84, 4008-4027.
113. Tuo, W., Ott, T.L. and Bazer, F.W. (1993) Natural killer cell activity of lymphocytes exposed to ovine, typel, trophoblast interferon. Am. J. Reprod. Immunol., 29, 26-34.
114. Verma, S., King, A. and Loke, Y.W. (1997) Expression of killer cell inhibitory receptors on human uterine natural killer cells. Eur. J. Immunol., 27, 979-983.
115. Viganò, P., Vercellini, P., Di Blasio, A.M. et al. (1991) Deficient anti-endometrium lymphocyte-mediated cytotoxicity in patients with endometriosis. Fertil. Steril., 56, 894-899.
116. Viganö, P., Pardi, R., Magri, B. et al. (1994) Expression of intercellular adhesion molecule-1 (ICAM-I) on cultured human endometrial stromal cells and its role in the interaction with natural killers. Am. J. Reprod. Immunol., 32, 139-145.
117. Wardle, P.O., McLaughlin, E.A., McDermott, A. et al. (1985) Endometriosis and ovulatory disorder: reduced fertilisation in vitro compared with tubal and unexplained inferility. Lancet, ii, 236-239.
118. Wegmann, T.G., Lin, H., Guilbert, J. and Mosmann, T.R. (1993) Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol. Today, 14, 353-356.
119. Wilson, T.J., Hertzog, P.J., Angus, D. et al. (1994) Decreased natural killer cell activity in endometriosis patients: relationship to disease pathogenesis. Fertil. Steril., 62, 1086-1088.
120. Yanushpolsky, E.H., Best, C.L., Jackson, K.V. et al. (1998) Effects of endometriomas on oocyte quality, embryo quality and pregnancy rates in in vitro fertilization cycles: prospective case-controlled study. J. Assist. Reprod. Genet., 15, 193-197.
121. Yovich, J.L., Yovich, J.M. and Tuvik, A.I. (1985) In vitro fertilization for endometriosis. Lancet, ii, 552.
122. Yui, J., Garcia-Lloret, M., Wegmann, T.G. and Guilbert, L. (1994) Cytotoxicity of tumor necrosis factor alpha and gamma-interferon against primary human placental trophoblast. Placenta, 15, 819-827.