Why did your mother reject you? Immunogenetic determinants of the response to environmental selective pressure expressed at the uterine level

American Journal of Reproductive Immunology

Volumn 41, Issue 1, 1999, Pages 5-22

  Clark, David A ^a   Arck, Petra C ^c   Chaouat, Gerard ^b  

^a MCMASTER UNIVERSITY   (Canada)

^b INSERM   (France)

^c NONE

Author keywords

Abortion; Blood clotting; Evolution; Imprinting; NK T cells; Pregnancy immunology; Prothrombinase; T cells

Indexed keywords

BLOOD CLOTTING FACTOR 10A; CYTOKINE; FETAL ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 4; TRANSFORMING GROWTH FACTOR BETA2;

BLOOD CLOTTING; CONFERENCE PAPER; GENOME IMPRINTING; HELPER CELL; HUMAN; IMMUNE RESPONSE; IMMUNOGENETICS; NATURAL KILLER CELL; PRIORITY JOURNAL; SPONTANEOUS ABORTION; UTERUS; VASCULITIS;

EID: 0033014385     PISSN: 10467408     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0897.1999.tb00071.x     Document Type: Conference Paper

References (165)

1. Clark DA: Immunobiological characterization of the trophoblast-decidual interface in human pregnancy. In Immunology of Human Reproduction, M Kurpisz, N Fernandez (eds). Oxford, UK, Bios Scientific Publishers, 1995, pp. 301-312.
2. Clark DA: Controversies in reproductive immunology. Crit Rev Immunol 1991; 11:215-247.
3. Clark DA, Chaouat G: What do we know about spontaneous abortion mechanisms? Am J Reprod Immunol 1989; 19:28-37.
4. Clark DA: Decidua-placenta immunologic interactions. In Immunology of the Fetus, G Chaouat (ed). Boca Raton, FL,CRC Press, 1990, pp. 161-178.
5. Clark DA, Arck PC, Jalali R, Merali FS, Manuel J, Chaouat G, Underwood JL, Mowbray JF: Psychoneuro-cytokine/endocrine pathways in immunoregulation during pregnancy. Am J Reprod Immunol 1996; 35:330-337.
6. Clark DA: Alloimmunity and pregnancy loss. In Medical Therapy in Pregnancy, 3rd ed, N Gleicher (ed). Norwalk, CT, Appleton and Lange, 1998, pp. 511-521.
7. Medawar PB: Some immunological and endocrinological problems raised by evolution of viviparity in vertebrates. In Society for Experimental Biology, Evolution Symposia Number 11. New York, Academic Press, 1953, pp. 320-338.
8. Wegmann TG: Maternal T cells promote placental growth and prevent spontaneous abortion. Immunol Lett 1988; 17:297-302.
9. Tafuri A, Alferink J, Moller P, Hammerling GJ, Arnold B: T cell awareness of paternal alloantigens during pregnancy. Science 1995; 270:630-633.
10. Clark DA, Lea RG, Podor T, Daya S, Banwatt D, Harley C: Cytokines determining the success or failure of pregnancy. Ann New York Acad Sci 1991; 626:524-536.
11. Clark DA: Animal models of recurrent pregnancy loss. In Immunologic Obstetrics, CB Coulam, WP Faulk, JA McIntyre (eds). New York, Norton, 1992, pp. 428-436.
12. Raghupathy R: Maternal antiplacental cell-mediated reactivity and spontaneous abortions. Am J Reprod Immunol 1997; 37:478-484.
13. Jiang S-P, Vacchio MS: The cutting edge: multiple mechanisms of peripheral T cell tolerance to the "fetal allograft". J Immunol 1998; 160:3086-3090.
14. Wegmann TG, Waters CA, Drell DW, Carlson GA: Pregnant mice are not primed but can be primed to paternal alloantigens during pregnancy. Proc Natl Acad Sci 1979; 76:2410-2412.
15. Beer AE, Billingham RE: Host response to intra-uterine tissue, cellular and fetal allografts. J Reprod Fertil 1974; Suppl 21:59-88.
16. Simmons RL, Ozerkis AJ, Butsch DW, Russell PS: The immunologic problem of pregnancy. III. Effect of pregnancy on survival of adult and neonatal skin grafts. Am J Obstet Gynecol 1967; 99:266-270.
17. Bonney EA, Matzinger P: The maternal immune system's interaction with circulating fetal cells. J Immunol 1997; 158:40-47.
18. Mattsson R, Holmdahl R, Scheynius A, Bernadotte F, Mattsson A, van de Meide PH: Placental MHC class I antigen expression is induced in mice following in vivo treatment with recombinant interferon-γ. J Reprod Immunol 1991; 19:115-129.
19. Zuckerman FA, Head JR: Murine trophoblast resists cell mediated lysis. I. Resistance to allospecific cytotoxic T lymphocytes. J Immunol 1987; 139:2856-2865.
20. Zhang L, Fung-Leung W, Miller RG: Downregulation of CD8 on mature antigen-reactive T cells as a mechanism of peripheral tolerance. J Immunol 1995; 155:3464-3471.
21. Voland JR, Becker C, Hooshmand F: Overexpression of Class I MHC in murine trophoblast and increased rates of spontaneous abortion. In Immunobiology of Reproduction, Serono Symposia USA, JS Hunt (ed). New York, Springer Verlag, 1994, pp. 214-235.
22. Athanassakis-Vassiladis I, Galanopoulos VK, Grigoriou M, Papamatheakis J: Induction of class II MHC antigen expression on the murine placenta by 5-azacytidine correlates with fetal abortion. Cell Immunol 1990; 128:438-439.
23. Yuan XJ, Dixon-McCarthy B, Kunz HW, Gill TJ III: Role of methylation in placental major histocompatibility complex antigen expression and fetal loss. Biol Reprod 1994; 51:831-842.
24. Clark DA, McDermott MR, Szewczuk M: Impairment of host-vs-graft reaction in pregnant mice. II. Selective suppression of cytotoxic T cell generation correlates with soluble suppressor activity and with successful pregnancy. Cell Immunol 1980; 52:106-118.
25. Brooks-Kaiser JC, Hoskin DW: Inhibition of DNA synthesis and IL-2 bioactivity in MLR by splenic pregnancy-associated natural suppressor cells involves the production of a TGF-β1-like molecule and a second distinct inhibitory factor. J Reprod Immunol 1993; 25:31-49.
26. Nagarkatti PS, Clark DA: In vitro activity and in vivo correlates of alloantigen-specific murine suppressor T cells induced by allogeneic pregnancy. J Immunol 1983; 131:638-643.
27. Robertson SH, Mau VJ, Hudson SH, Tremellen KP: Cytokine-leukocyte networks and the establishment of pregnancy. Am J Reprod Immunol 1997; 37:438-442.
28. Bennett MW, O'Connell JO, O'Sullivan GC, Brady C, Roche D, Collins JK, Shanahan F: The Fas counterattack in vivo: apoptotic depletion of tumor-infiltrating lymphocytes associated with Fas ligand expression by human esophageal carcinoma. J Immunol 1998; 160:5669-5675.
29. Hunt JS, Vassmer D, Ferguson TA, Miller L: Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between mother and conceptus. J Immunol 1997; 158:4122-4128.
30. lpr mice from early lethality. J Immunol 1997; 159:2058-2067.
31. Chaouat G, Clark DA: NK and T cells in immune abortion and local cytokine network. Immunologist 1998; Suppl 1:157.
32. Hill JA, Melling GC, Johnson PM: Immunohistochemical studies of human uteroplacental tissues from first trimester abortion. Am J Obstet Gynecol 1995; 173:90-96.
33. Chaouat G, Kolb JP, Wegmann TG: The murine placenta as an immunological barrier between mother and fetus. Immunol Rev 1983; 75:31-60.
34. Wick M, Dubey P, Koeppen H, Siegel CT, Fields PE, Chen L, Bluestone JA, Schreiber H: Antigenic cancer cells grow progressively in immune hosts without evidence for T cell exhaustion or systemic anergy. J Exp Med 1997; 186:229-238.
35. Zhang L, Miller RG: The correlation of prolonged survival of maternal skin grafts with the presence of naturally transferred maternal T cells. Transplantation 1993; 56:918-921.
36. Pitrowski P, Croy BA: Maternal cells are widely distributed in murine fetuses in utero. Biol Reprod 1996; 54:1103-1110.
37. King A, Gardner L, Loke YW: Human decidual leukocytes do not proliferate in response to either extravillous trophoblast or allogeneic peripheral blood lymphocytes. J Reprod Immunol 1996; 30:67-74.
38. Pollard JW: Regulation of polypeptide growth factor synthesis and growth factor-related gene expression in the rat and mouse uterus before and after implantation. J Reprod Fertil 1990; 88:721-729.
39. Clark DA: Cytokines and pregnancy. Curr Opin Immunol 1989; 1:1148-1152.
40. Clark DA, Lea RG, Denburg J, Banwatt D, Manuel J, Damji N, Underwood J, Michel M, Mowbray JF, Daya S, Chaouat G: Transforming growth factor-β-related suppressor factor in mammalian pregnancy decidua. In Maternofetal Relationship: Molecular and Cellular Biology, INSERM Colloque, Vol. 212, G. Chaouat (ed). Paris, John Libby Eurotext, 1991, pp. 171-179.
41. Croy BA, Chapeau C: Evaluation of the pregnancy immunotrophism hypothesis by assessment of the reproductive performance of young adult mice of genotype scid/scid.bg/bg. J Reprod Fertil 1990; 88:231-239.
42. Chaouat G, Menu E, Clark DA, Minkowsky M, Dy M, Wegmann TG: Control of fetal survival in CBA × DBA/2 mice by lymphokine therapy. J Reprod Fertil 1990; 89:447-458.
43. Baines MG, Duclos AJ, Antecka E, Haddad EK: Decidual infiltration and activation of macrophages leads to early embryo loss. Am J Reprod Immunol 1997; 37:471-477.
44. Clark DA, Chaouat G, Arck PC, Mittruecker HW, Levy GA: The cutting edge: cytokine-dependent abortion in CBA × DBA/2 mice is mediated by the procoagulant fg12 prothrombinase. J Immunol 1998; 160:545-549.
45. + T cell-dependent suppression of natural effector cells. Cell Immunol 1994; 154:143-152.
46. Grimm EA: Human lymphokine-activated killer cells (LAK cells) as a potential therapeutic modality. Biochem Biophys Acta 1986; 865:267-269.
47. Stoppacciaro A, Meliani C, Parenza M, Mastracchio A, Bassi C, Baroni C, Parmiani G, Colombo MP: Regression of an established tumor genetically modified to release granulocyte colony-stimulating factor requires granulocyte-T cell cooperation and T cell-produced interferon. J Exp Med 1993; 178:151-161.
48. Lu CY, Redline RW, Shea CM, Dustin LB, McKay DB: Pregnancy as a natural model of allograft tolerance. Interactions between adherent macrophages and trophoblast populations. Transplantation 1989; 48:848-855.
49. Drake BL, Head JR: Murine trophoblast can be killed by lymphokine-activated killer cells. J Immunol 1989; 143:9-14.
50. King A, Loke YW: Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell Immunol 1990; 129:435-448.
51. Clark DA, Lea RG, Flanders KC, Banwatt D, Chaouat G: Role of a unique species of TGF-β in preventing rejection of the conceptus during pregnancy. In Progress in Immunology VIII, J Gergely, M Benczur, A Erdei, A Falus, Gy Fust, G Medqyesi, Gy Petranyi, E Rajnavolgyi (eds). Budapest/Heidelberg, Springer-Verlag, 1992, pp. 841-884.
52. Kinsky R, Delage G, Rosin M, Thang N, Hoffman M, Chaouat G: A murine model of NK cell mediated resorption. Am J Reprod Immunol 1990; 23:73-77.
53. Aoki K, Kajijura S, Matsumoto Y, Okada S, Yagami Y, Gleicher N: Preconceptional natural killer cell activity as a predictor of miscarriage. Lancet 1995; 135:1340-1342.
54. + leukocytes in early pregnancy predicts success or miscarriage. Am J Reprod Immunol 1995; 34:219-224.
55. Lachapelle MH, Miron P, Hemmings R, Roy DC: Endometrial T, B, and NK cells in patients with recurrent abortion: altered profile and pregnancy outcome. J Immunol 1996; 156:4227-4234.
56. Ferry BL, Sargent IL, Starkey PM, Redmann CW: Cytotoxic activity against trophoblast and choriocarcinoma cells of large granular lymphocytes from early pregnancy decidua. Cellular Immunol 1991; 132:140-149.
57. + lymphocytes on killing of natural killer-and lymphokine-activated killer-sensitive targets. Biol Reprod 1998; 58:982-987.
58. Arck PC, Troutt AB, Clark DA: Soluble receptors neutralizing TNF-α and IL-1 block stress-triggered murine abortion. Am J Reprod Immunol 1997; 37:262-266.
59. Lim KJH, Odukoya OA, Ajjan RA, Li TC, Weetman AP, Cooke ID: Profile of cytokine mRNA expression in peri-implantation endometrium. Mol Human Reprod 1998; 4:77-81.
60. Trinchieri G: Proinflammatory and immunoregulatory effects of interleukin 12. Int Rev Immunol 1998; 16:30-96.
61. Chaouat G, Meliani AA, Martal J, Raghupathy R, Elliot J, Mosmann TR, Wegmann TG: IL-10 prevents naturally occurring fetal loss in the CBA × DBA/2 mating combination and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-τ. J Immunol 1995; 154:4261-4268.
62. Raghupathy R, Tangri S: Immunodystrophism, T cells, cytokines and pregnancy failure. Am J Reprod Immunol 1996; 35:291-296.
63. Muzikova E, Clark DA: Is spontaneous resorption in the DBA/2-mated CBA/J mouse due to a defect in "seed" or in "soil"? Am J Reprod Immunol 1995; 33:81-85.
64. Ewoldsen MA, Ostlie NS, Warner CM: Killing of mouse blastocyst stage embryos by cytotoxic T lymphocytes directed to major histocompatibility complex antigens. J Immunol 1997; 138:2764-2770.
65. Searle RF, Johnson MH, Billington WD, Elson J, Clutterbuck-Jackson S: Investigation of H-2 and non-H-2 antigens on the mouse blastocyst. Transplantation 1974; 18:136-141.
66. King NJC, Drake BL, Maxwell LE, Rodger JC: Class I major histocompatibility complex antigen expression on early murine trophoblast and its induction by lymphokines in vitro. II. The role of gamma interferon in the responses of primary and secondary giant cells. J Reprod Immunol 1987; 12:13-21.
67. Simpson TJ, Globus MS: In utero fetal hematopotietic stem cell transplantation. Semin Perinatol 1985; 9:68-74.
68. Barrett MJ, Buckley RH, Schiff SE, Kidd PC, Ward EE: Accelerated development of immunity following transplantation of maternal marrow stem cells into infants with severe combined immunodeficiency and transplacentally acquired lymphoid chimerism. Clin Exp Immunol 1988; 72:118-123.
69. Zhang X, Brunner T, Carter L, Dutton RW, Rogers P, Bradley L, Sato T, Reed JC, Green D, Swain SL: Unequal death in T helper cell (Th)1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J Exp Med 1987; 185:1837-1849.
70. + T cells as cytotoxic T cells specific for maternal alloantigens. J Exp Med 1992; 176:1-7.
71. Olding LB, Papadogiannakis N, Barbieri B, Murgita RA: Suppressive cellular and molecular activities in maternofetal immune interactions: suppressor cell activity, prostaglandins, and alpha-fetoproteins. Curr Top Microbiol Immunol 1997; 222:159-187.
72. Roussev RG, Kaider BD, Coulam CB: Anti-endothelial cell antibodies - another cause for pregnancy loss? Am J Reprod Immunol 1997; 37:355.
73. Meegdes BHLM, Ingenhoes R, Peeters LLH, Exalto N: Early pregnancy wastage: relationship between chorionic vascularization and embryonic development. Fertil Steril 1985; 49:216-220.
74. Coulam CB, Stephenson M, Stern JJ, Clark DA: Immunotherapy for recurrent pregnancy loss: analysis of results from clinical trials. Am J Reprod Immunol 1996; 35:330-337.
75. Laberrere CA, Faulk WP: Immunopathology of extraembryonic tissues in normal human pregnancy. In Immunobiology of Normal and Diabetic Pregnancy, D Andreani, G Bompani, U DiMario, WP Faulk, A Galluzzo (eds). Chichester, UK, Wiley, 1990, pp. 145-186.
76. Labarrere CA: Allogeneic recognition and rejection reactions in the placenta. Am J Reprod Immunol 1989; 21:94-99.
77. Heyborne K, Fu YX, Nelson A, Farr A, O'Brien R, Born W: Recognition of trophoblasts by γδ T cells. J Immunol 1994; 153:2918-2976.
78. Ferrick DA, Gemmell-Hori L, Sydna B, Mulvania T, Pemminger JM, Kronenberg M, Mak TW: Tolerance and self-reactivity in Vγ1.1Cγ4 transgenic mice. Int Rev Immunol 1994; 11:295-304.
79. Su BC, Strand D, McDonough PG, McDonald JF: Temporal and constitutive expression of homeobox-2 gene (Hu-2), human heat shock gene (hsp-70), and oncogenes C-sis and N-myc in early human trophoblast. Am J Obstet Gynecol 1988; 159:1195-1199.
80. Yui J, Garcia-Lloret M, Wegmann TG, Guilbert LJ: Cytotoxicity of tumor necrosis factor-α and γ-interferon against primary human placental trophoblasts. Placenta 1994; 15:819-835.
81. Rand JH, Wu XX, Andree HAM, Lockwood S, Guller S, Sher J, Happel PC: Pregnancy loss in the antiphospholipid-antibody syndrome: a possible thrombogenic mechanism. N Engl J Med 1997; 337:154-160.
82. Lea RG, al-Sharelch N, Tulppati M, Critchley HO: The immunolocalization of bcl-2 at the maternal-fetal interface in healthy and failing pregnancies. Human Reprod 1997; 12:153-158.
83. Garcia-Lloret MI, Yui J, Winkler-Lowen B, Guilbert LJ: Epidermal growth factor inhibits cytokine-induced apoptosis of primary human trophoblasts. J Cell Physiol 1996; 167:324-332.
84. Ding JW, Ning Q, Liu MF, Leibowitz J, Peltekian KM, Cole EH, Fung LS, Holloway C, Marsden P, Yeger H, Phillips MJ, Levy GA: Fulminant hepatic failure in murine hepatitis virus strain 3 infection: tissue-specific expression of a novel fg12 prothrombinase. J Virol 1997; 71:9223-9230.
85. Salafia C, Maier D, Vogel C, Pezzullo J, Burns J, Silberman L: Placental and decidual histology in spontaneous abortion: detailed description and correlations with chromosome number. Obstet Gynecol 1993; 82:295-303.
86. Bratt J, Palmblad J: Cytokine-induced neutrophil-mediated injury of human endothelial cells. J Immunol 1997; 159:912-918.
87. Kaplanski G, Fabrigoule M, Boulay V, Dinarello CA, Bongrand P, Kaplanski S, Farnarier C: Thrombin-induced endothelial type II activation in vitro. J Immunol 1997; 158:5435-5441.
88. Liu L, Rogers GM: Characterization of an inducible endothelial cell prothrombin activator. Blood 1996; 88:2989-2994.
89. Lefer AM, Tsao P, Aoki N, Palladino MA Jr: Mediation of cardioprotection by transforming growth factor-β. Science 1990; 249:61-64.
90. Krishnan L, Guilbert LJ, Wegmann TG, Belosovic M, Mosmann TR: T helper response against Leishmania major in pregnant C57B1/6 mice increases implantation failure and fetal resorption: correlation with increased IFN-γ and TNF and reduced IL-10 production by placental cells. J Immunol 1996; 156:653-662.
91. Krishnan L, Guilbert LJ, Russell AS, Wegmann TG, Mosmann TR, Belosovic M: Pregnancy impairs resistance of C57B1/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-γ responses and increased production of T helper 2 cytokines. J Immunol 1996; 146:644-652.
92. Blumberg N, Heal JM: The transfusion immunomodulation theory: the Th1/Th2 paradigm and an analogy with pregnancy as a unifying mechanism. Semin Hematol 1996; 33:329-340.
93. Babcock GF, Alexander JW: The effects of blood transfusion on cytokine production by Th1 and Th2 lymphocytes in the mouse. Transplantation 1996; 61:465-468.
94. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL: Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 1994; 265:1237-1240.
95. Lin H, Mosmann TR, Guilbert L, Tuntipopopat S, Wegmann TG: Synthesis of T helper-2-type cytokines at the maternal-fetal interface. J Immunol 1993; 151:4562-4573.
96. Lea RG, Flanders KC, Harley CB, Manuel J, Banwatt D, Clark DA: Release of a TGF-β2-related suppressor factor from postimplantation murine decidual tissue can be correlated with the detection of a subpopulation of cells containing RNA for TGF-β2. J Immunol 1992; 148:778-787.
97. Delassus S, Couthino GC, Saucier C, Darche S, Kourilsky P: Differential cytokine expression in maternal blood and placenta during murine gestation. J Immunol 1994; 152:2411-2420.
98. Maeda H, Shiraishi A: TGF-β contributes to the shift towards Th2-type responses through direct and IL-10-mediated pathways in tumor-bearing mice. J Immunol 1996; 156:73-78.
99. Roth I, Corry DB, Locksley RM, Abrams JS, Litton MJ, Fisher SJ: Human placental cytotrophoblasts produce the immunosuppressive cytokine interleukin 10. J Exp Med 1996; 184:539-548.
100. Maejima M, Fujii T, Kozuma S, Okai T, Shibata Y, Taketani Y: Presence of HLA-G expressing cells modulates the ability of peripheral blood mononuclear cells to release cytokines. Am J Reprod Immunol 1997; 38:79-82.
101. Piccinni MP, Giudizi MG, Biagiotti R, Beloni L, Giannarini L, Sampognaro S, Parronchi P, Manetti F, Annunziato F, Livi C, Romagnani S, Maggi E: Progesterone favors the development of human helper T cells producing Th2-type cytokines and promotes both IL-4 and membrane CD30 expression in established Th1 cell clones. J Immunol 1995; 155:128-133.
102. Arck PC, Ferrick DA, Steele-Norwood D, Croitoru K, Clark DA: Regulation of abortion by γδ T cells. Am J Reprod Immunol 1997; 37:87-93.
103. Arck PC, Ferrick DA, Steele-Norwood D, Croitoru K, Clark DA: Murine T cell determination of pregnancy outcome: I. Effects of strain, αβ T cell receptor, γδ T cell receptor, and γδ T cell subsets. Am J Reprod Immunol 1997;37:492-502. [Erratum, Am J Reprod Immunol 1997;38:438.]
104. Clark DA, Quarrington C, Banwatt D, Manuel J, Fulop G: Spontaneous abortion in immunodeficient SCID mice. Am J Reprod Immunol 1994; 32:15-25.
105. Clark DA, Merali F, Steele-Norwood D, Hoskin D, Arck PC, Murgita R, Croitoru K, Hirte H: Decidua-associated suppressor cells in abortion-prone DBA/2-mated CBA/J mice that release bioactive transforming growth factor β2-related immunosuppressive molecules express a bone marrow-derived natural suppressor cell marker and γδ T cell receptor. Biol Reprod 1997; 57:1351-1360.
106. Chaouat G, Menu E: Maternal T cell reactivity in pregnancy? Curr Top Microbiol Immunol 1997; 222:103-126.
107. + T cells as a basis for stress-triggered substance P-mediated abortion in mice. Cell Immunol 1996; 171:226-230.
108. Clark DA, Banwatt D, Chaouat G: Effects of prostaglandin synthesis inhibitors on spontaneous and endotoxin-induced abortion in mice. J Reprod Immunol 1993; 24:29-44.
109. Clark DA, Flanders KC, Hirte H, Dasch JR, Cocker R, McAnulty RJ, Laurent GJ: Characterization of murine pregnancy decidua TGF-β. I. TGF-β2-like molecules of unusual molecular size released in bioactive form. Biol Reprod 1995; 52:1380-1388.
110. Clark DA, Drake BL, Head JR, Stedronska-Clark J, Banwatt D: Decidua associated suppressor activity and viability of individual implantation sites of allopregnant C3H mice. J Reprod Immunol 1990; 17:253-264.
111. Clark DA, Banwatt D, Chaouat G: Stress-triggered abortion in mice is prevented by alloimmunization. Am J Reprod Immunol 1993; 29:141-147.
112. Suzuki T, Hiromatsu K, Ando Y, Okamoto T, Tomoda Y, Yoshikai Y: Regulatory role of γδ T cells in uterine intraepithelial lymphocytes in maternal antifetal immune response. J Immunol 1995; 154:4476-4484.
113. Mincheva-Nilsson L, Baranov V, Yeung MM, Hammarstrom S, Hammarstrom ML: Immunomorphologic studies of human decidua-associated lymphoid cells in normal early pregnancy. J Immunol 1994; 152:2020-2032.
114. + intraepithelial lymphocytes induced by the local presence of the sheep conceptus. Am J Reprod Immunol 1997; 37:199-205.
115. Chien YH, Jores R, Crowley MP: Recognition by γδ T cells. Ann Rev Immunol 1996; 14:511-532.
116. Bluestone JA, Cron RQ, Barrett TA, Houlden B, Sperling AI, Dert A, Hendrich S, Rellham B, Matis LA: Repertoire, development and ligand specificity of murine TCRγδ cells. Immunol Rev 1991; 120:5-33.
117. Tanaka Y, Brenner MB, Bloom BR, Morita CT: Recognition of nonpeptide ligands by T cells. J Mol Med 1996; 74:223-231.
118. Weintraub BC, Jackson MR, Hedrick SM: T cells can recognize nonclassical MHC in absence of conventional antigenic peptides. J Immunol 1994; 153:3051-3058.
119. Fu YX, Roark CE, Kelly K, Drevets D, Campbell P, O'Brien R, Born W: Immune protection and control of inflammatory tissue necrosis by γδ T cells. J Immunol 1994; 153:3101-3115.
120. Hsieh B, Schrenzel MD, Mulvania T, Lepper HD, DiMolfetto-Landon L, Ferrick DA: In vivo cytokine production in murine listeriosis. J Immunol 1996; 156:232-237.
121. Schneider SL, Gollnick SO, Grande C, Pazik JE, Tomasi TB: Differential regulation of TGF-β2 by hormones in rat uterus and mammary gland. J Reprod Immunol 1996; 32:125-144.
122. Heyborne KD, Cranfill RL, Carding SR, Born WK, O'Brien RL: Characterization of γδ T lymphocytes at the maternal-fetal interface. J Immunol 1992; 149:2872-2878.
123. Clark DA, Arck PC, Steele-Norwood D, Croitoru K, Levy GA, Chaouat G: Th1/Th2 balance determines outcome of pregnancy via FGL2 prothrombinase-triggered inflammation. FASEB J 1998; 12:880.
124. Nishimura H, Emoto M, Hiromatsu K, Yamamoto S, Matsuura K, Gomi H, Ikeda T, Itohara S, Yoshikai Y: The role of gamma delta T cells in priming macrophages to produce tumor necrosis factor-alpha. Eur J Immunol 1995; 25:1465-1468.
125. Sandor M, Sperling AI, Cook GA, Weinstock JV, Lynch RG, Bluestone JA: Two waves of γδ T cells expressing different vδ genes are recruited into schistosome-induced liver granulomas. J Immunol 1995; 155:275-284.
126. McMenamin C, McKersey M, Kuhnlem P, Hunig T, Holt PG: T cells down-regulate primary IgE responses in rats to inhaled soluble protein antigens. J Immunol 1995; 154:4390-4394.
127. + T cells. Immunology 1994; 81:27-35.
128. Szekeres-Bartho J, Szekeres GY, Debre P, Andreu G, Autran B, Chaouat G: Reactivity of lymphocytes to a progesterone receptor-specific monoclonal antibody. Cell Immunol 1990; 125:273-283.
129. Szereday L, Varga P, Szekeres-Bartho J: Cytokine production by lymphocytes in pregnancy. Am J Reprod Immunol 1997; 38:418-422.
130. Szekeres-Bartho J, Kinsky R, Kapovic M, Chaouat G: Complete Freund's adjuvant treatment of pregnant females influences resorption rates in CBA × DBA/2 matings via progesterone-mediated immunomodulation. Am J Reprod Immunol 1991; 26:82-83.
131. Multhoff G, Botzler C, Jennen L, Schmidt J, Ellwart J, Issels R: Heat shock protein 72 on tumor cells: a recognition structure for natural killer cells. J Immunol 1997; 158:4341-4350.
132. King A, Hiby SE, Verma S, Burrows T, Gardner L, Loke YW: Uterine NK cells and trophoblast class I molecules. Am J Reprod Immunol 1997; 37:459-462.
133. Soderstrom K, Corliss B, Lanier LL, Philips JH: CD94/ NKG2 is the predominant inhibitory receptor involved in recognition of HLA-G by decidual and peripheral blood NK cells. J Immunol 1997; 159:1072-1075.
134. Chaouat G, Dalliot JT, Volumenie JL, Menu E, Gras G, Delage G, Mognetti B: Immune suppression and Th1/Th2 balance in pregnancy revisited: a (very) personal tribute to Tom Wegmann. Am J Reprod Immunol 1977; 37:427-434.
135. Gorczynski RM, Chen Z, Fu XM, Zeng H: Increased expression of the novel molecule OX-2 is involved in prolongation of murine renal allograft survival. Transplantation 1998; 65:1106-1114.
136. Maruyama T, Makino T, Sugi T, Matsubayashi H, Ozawa N, Nozawa S: Flow-cytometric analysis of immune cell populations in human decidua from various types of first-trimester pregnancy. Hum Immunol 1992; 34:212-218.
137. + lymphocytes from first trimester human decidua using two-color flow cytometry. Am J Reprod Immunol 1993; 29:5-16.
138. Lea RG, Underwood J, Flanders KC, Hirte H, Banwatt D, Ohno I, Michel M, Daya S, Harley C, Mowbray JF, Clark DA: A subset of patients with recurrent spontaneous abortion is deficient in transforming growth factor β-2-producing "suppressor cells" in uterine tissue near the placental attachment site. Am J Reprod Immunol 1995; 34:52-61.
139. + lymphoid cells in human first trimester pregnancy decidua as a source of novel TGF-β2-related immunosuppressive factors. Hum Reprod 1994; 9:2270-2277.
140. + cells and show selective down-regulation of alloreactivity. J Immunol 1992; 149:2203-2211.
141. Morii T, Nishikawa K, Saito S, Enomoto M, Ito A, Kurai N, shimoyama T, Ichijo M, Marita N: T-cell receptors are expressed but down-regulated on intradecidual T lymphocytes. Am J Reprod Immunol 1993; 29:1-4.
142. Hayakawa S, Shiraishi H, Saitoh S, Satoh K: Decidua as a site of extrathymic Vγ1 T-cell differentiation. Am J Reprod Immunol 1996; 35:233-238.
143. Lea RG, Flanders KC, McIntyre S, Michel M, Mowbray J, Underwood J, Baird JD, Clark DA: Uterine TGF-β2 in human normal and pathologic pregnancies. In Early Embryo Development, Uterus Preparation and Role of Cytokines in Implantation and Labour, G. Chaouat (ed). Lyon, France, Fondation Marcel Merieux, 1994, pp. 117-122.
144. Mincheva-Nilsson L, Kling M, Hammarstrom S, Nagaeva O, Sundquist KG, Hammarstrom ML, Baranov V: T cells of human early pregnancy decidua. Evidence for local proliferation, phenotypic heterogeneity, and extrathymic differentiation. J Immunol 1997; 159:3266-3277.
145. Hunt JS, Miller L, Vassmer D, Croy BA: Expression of the inducible nitric oxide synthetase gene in mouse uterine leukocytes and potential relationships with uterine function during pregnancy. Biol Reprod 1997; 57:827-836.
146. Parr EL, Chen HL, Parr MB, Hunt JS: Synthesis and localization of tumor necrosis factor-α in activated NK cells in the pregnant uterus. J Reprod Immunol 1995; 28:31-40.
147. Croy BA: Granulated metrial gland cells - interesting cells found in the pregnant uterus. Am J Reprod Immunol 1990; 23:19-21.
148. bright natural killer cells in the human early pregnancy decidua. Int Immunol 1993; 5:559-563.
149. Jokhi PP, King A, Sharkey AM, Smith SK, Loke YW: Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse-transcriptase polymerase chain reaction. J Immunol 1994; 153:4427-4435.
150. Toder V, Strassburger D, Carp H, Irlin Y, Laurie S, Pecht M, Trainin N: Nonspecific immunopotentiation and pregnancy loss: complete Freund's adjuvant reverses high fetal resorption rates in CBA × DBA/2 mouse combination. Am J Reprod Immunol 1990; 24:63-66.
151. Baines MG, Duclos AJ, de Fougerolles AR, Gendron RL: Immunological prevention of spontaneous early embryo resorption is mediated by nonspecific immunostimulation. Am J Reprod Immunol 1996; 35:34-42.
152. Chaouat G, Clark DA, Wegmann TG: Genetic aspects of the CBA × DBA/2 and B10 × B10.A models of murine pregnancy failure and its prevention by lymphocyte immunisation. In Early Pregnancy Failure: Mechanisms and Treatment, Royal College of Obstetrics and Gynaecology, RW Beard, F Sharp (eds). Ashton-under-Lyne, UK, Peacock Press, 1988, pp. 215-217.
153. Mowbray JF: Effect of immunisation with paternal cells on recurrent spontaneous abortion. In Reproductive Immunology 1986, DA Clark, BA Croy (eds). Amsterdam, Elsevier, 1986, pp. 269-276.
154. Mowbray JF, Jalali R, Chaouat G, Clark DA, Underwood J, Allen WR, Mathias S: Maternal response to paternal trophoblast antigens. Am J Reprod Immunol 1997; 37:421-426.
155. Clark DA, Chaouat G, Guenet JL, Kiger N: Local active suppression and successful vaccination against spontaneous abortion in CBA/J mice. J Reprod Immunol 1987; 10:79-85.
156. Mattsson R, Holmdahl R: Maintained allogeneic pregnancy in rats depleted of T cytotoxic/suppressor cells by OX8 monoclonal antibody treatment. J Reprod Immunol 1987; 12:23-34.
157. Sulila P, Holmdahl R, Hansson I, Bernadette F, Mattsson A, Mattsson R: An investigation of allogeneic pregnancy in multiparous mice subjected to in vivo depletion of CD8 (Ly2)-positive lymphocytes by monoclonal antibody treatment. J Reprod Immunol 1988; 14:235-246.
158. Kligman I, Jeremias J, Rozenwaks Z, Witkin SS: Cell-mediated immunity to human and Escherischia coli 60-kDa heat shock protein in women: association with a history of spontaneous abortion and endometriosis. Am J Reprod Immunol 1998; 40:32-36.
159. Hill JA, Anderson D, Polgar K: T helper 1-type cellular immunity to trophoblast in women with recurrent abortions. JAMA 1995; 273:1933-1938.
160. Bendelac A, Fearon DT: Innate immunity: innate pathways that control acquired immunity. Curr Opin Immunol 1997; 9:1-3.
161. Arck PC, Quarrington C, Mak T, Clark DA: TNF-α P55 receptor knockout mice demonstrate two distinct types of endotoxin-induced rejection of the embryo qua parasite. Am J Reprod Immunol 1997; 37:347.
162. Gill TJ III, Ho HN, Kanbour-Shakir A, Kunz HW: MHC-linked genes and their role in growth and reproduction. In Immunobiology of Reproduction, Serono Symposia USA, JS Hunt (ed). New York, Springer Verlag, 1993, pp. 170-183.
163. Chaouat G: The roots of the problem: "The Fetal Allograft". In Immunology of Pregnancy, G Chaouat (ed). Boca Raton, FL, CRC Press, 1993, pp. 11-17.
164. Potts WK, Manning CJ, Wakeland EK: Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 1991; 352:619-621.
165. Jin K, Ho HN, Speed TP, Gill TJ III: Reproductive failure and the major histocompatibility complex. Am J Hum Genet 1995; 56:1456-1467.