The fetus and the maternal immune system: Pregnancy as a model to study peripheral T-cell tolerance

Critical Reviews in Immunology

Volumn 19, Issue 5-6, 1999, Pages 461-480

  Vacchio, Melanie S ^a   Jiang, Shi Ping ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Clonal deletion; Immune deviation; Immune privilege; Placenta; Receptor downregulation; Trophoblast

Indexed keywords

FETAL ANTIGEN; MATERNAL ANTIBODY;

ANTIGEN PRESENTING CELL; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; IMMUNOLOGICAL TOLERANCE; MOTHER FETUS RELATIONSHIP; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; REVIEW;

ANIMALS; ANTIGEN-PRESENTING CELLS; CYTOKINES; FEMALE; FETUS; HUMANS; IMMUNE TOLERANCE; MICE; PREGNANCY; T-LYMPHOCYTES;

EID: 0033386312     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (99)

1. Kruisbeek, A. M. and Amsen, D., Mechanisms under lying T-cell tolerance, Curr. Opin. Immunol., 8, 233-244, 1996.
2. Mondino, A., Khoruts, A., and Jenkins, M. K., The anatomy of T-cell activation and tolerance, Proc. Natl. Acad. Sci. U.S.A., 93, 2245-2252, 1996.
3. Kroemer, G., Mechanisms of immunological self tolerance, in Cloned Deletion of Self-Reactive T Cells Kroemer, G., Ed., R. G. Landis Co., Austin, 2, 1994, 16-50.
4. Kappler, J. W., Roehm, H., and Marrack, P., T cell tolerance by clonal elimination in the thymus, Cell 49, 273-280, 1987.
5. + thymocytes, Nature, 333, 742-745, 1988.
6. Ramsdell, F. and Fowlkes, B. J., Clonal deletion versus anergy: the role of the thymus in inducing self-tolerance, Science, 248, 1342-1348, 1990.
7. Roberts, J. L., Sharrow, S. O., and Singer, A. Clonal deletion and clonal anergy in the thymus induced by cellular elements with different radiation sensitivities, J. Exp. Med., 171, 935-940, 1990.
8. + cells, Science, 258, 653-656, 1992.
9. Nieuwenhuis, P., Stet, R. J., Wagenaar, J. P., Wubbena, A. S., Kampinga, J., and Karrenbeld, A., The transcapsular route: a new way for (self-) antigens to by-pass the blood thymus barrier? Immunol. Today, 9, 372-375, 1988.
10. Dresser, D. W., Specific inhibition of antibody production II. Paralysis induced in adult mice by small quantities of protein antigen, Immunology, 5, 378-388, 1962.
11. Singer, G. A. and Abbas, A. K., The fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice, Immunity, 1, 365-371, 1994.
12. + antigen-specific T cells after in vivo exposure to male antigen, J. Immunol., 148, 3740-3745, 1992.
13. + T cells in mice tolerant to Staphylococcus aureus enterotoxin B, Nature, 349, 245-248, 1991.
14. Rocha, B., Tanchot, C., and vonBoehmer, H., Clonal anergy blocks in vivo growth of mature T cells and can be reversed in the absence of antigen, J. Exp. Med., 177, 1517-1521, 1993.
15. Rocha, B. and vonBoehmer, H., Peripheral selection of the T cell repertoire, Science, 251, 1225-1228, 1991.
16. Zhang, L., Fung-Leung, W., and Miller, R. G., Down-regulation of CD8 on mature antigen-reactive T cells as a mechanism of peripheral tolerance, J. Immunol., 155, 3464-3471, 1995.
17. Arnold, B., Schonrich, G., and Hammerling, G. J., Multiple levels of peripheral tolerance, Immunol. Today, 14, 12-14, 1993.
18. Miller, J. F. and Flavell, R. A., T-cell tolerance and autoimmunity in transgenic models of central and peripheral tolerance, Curr. Opin. Immunol., 6, 892-899, 1994.
19. Miller, J. F. A. P., Morahan, G., Allison, J., and Hoffman, M., A transgenic approach to the study of peripheral T-cell tolerance, Immunol. Rev., 122, 103-116, 1991.
20. Vacchio, M. S. and Ashwell, J. D., Mechanisms of regulation, in T Cell Tolerance, Granstein, R. D., Ed., Basel, Karger, 1, 1994, 1-33.
21. Auphan, N., Schonrich, G., Malissen, M., Barad, M., Hammerling, G., Arnold, B., Malissen, B., and Schmitt-Verhulst, A.-M., Influence of antigen density on degree of clonal deletion in T cell receptor transgenic mice, Int. Immunol., 4, 541-547, 1992.
22. Fields, L. E. and Loh, D. Y., Organ injury associated with extrathymic induction of immune tolerance in doubly transgenic mice, Proc. Natl. Acad. Sci. U.S.A., 89, 5730-5734, 1992.
23. Heath, W. R., Allison, J., Hoffmann, M. W., Schonrich, G., Hammerling, G., Arnold, B., and Miller, J. F. A. P., Autoimmune diabetes as a consequence of locally produced interleukin-2, Nature, 359, 547-549, 1992.
24. Morahan, G., Hoffmann, M. W., and Miller, J. F. A. P., A nondeletional mechansim of peripheral tolerance in T-cell receptor transgenic mice, Proc. Natl. Acad. Sci. U.S.A., 88, 11421-11425, 1991.
25. Schonrich, G., Kalinke, U., Momburg, F., Malissen, M., Schmitt-Verhulst, A. M., Malissen, B., Hammerling, G. J., and Arnold, B., Down-regulation of T cell receptors on self-reactive T cells as a novel mechanism for extrathymic tolerance induction, Cell, 65, 293-304, 1991.
26. Ohashi, P. S., Oehen, S., Buerki, K., Pircher, H., Ohashi, C. T., Odermatt, B., Malissen, B., Zinkernagel, R. M., and Hengartner, H., Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice, Cell, 65, 305-317, 1991.
27. Von Herrath, M. G., Dockter, J., and Oldstone, M. B. A., How virus induces a rapid or slow onset insulin-dependent diabetes mellitus in a transgenic model, Immunity, 1, 231-242, 1994.
28. Jolicoeur, C., Hanahan, D., and Smith, K. M., T cell tolerance toward a transgenic B cell antigen and transcription of endogenous pancreatic genes in the thymus, Proc. Natl. Acad. Sci. U.S.A., 91, 6707-6711, 1994.
29. Yeoman, H. and Mellor, A. L., Tolerance and MHC restriction in transgenic mice expressing a MHC class I gene in erythroid cells, Int. Immunol., 4, 59-65, 1992.
30. Antonia, S. J., Geiger, T., Miller, J., and Flavell, R. A., Mechanisms of immune tolerance induction through the thymic expression of a peripheral tissue-specific protein, Int. Immunol., 7, 715-722, 1995.
31. Pugliese, A., Zeller, M., Fernandez, A. J., Zalcberg, L. J., Bertlett, R. J., Ricordi, C., Pietropaolo, M., Eisenbarth, G. S., Bennet, S. T., and Patel, D. D., The insulin gene is transcribed in the human thymus and transcription levels correlate with the allelic variation at the INS VNTR-IDDM2 susceptibility locus for type I diabetes, Nat. Gen., 15, 293-297, 1997.
32. Vafiadis, R., Bennett, S. T., Todd, J. A., Nadeau, J., Grabs, R., Goodyer, C. G., Wickramasinghe, S., Colle, E., and Polychronakos, C., Insulin expression in human thymus is modulated by INS VNTR alleles at the IDDMS locus, Nat. Gen., 15, 289-292, 1997.
33. Heath, V. L., Moore, N. C., Parnell, S. M., and Mason, D., Intrathymic expression of genes involved in organ specific autoimmune disease, J. Autoimmunol., 11, 309-318, 1998.
34. Throsby, M., Homo-Delarche, F., Chevenne, D., Goya, R., Dardenne, M., and Pleau, J. M., Pancreatic hormone expression in the murine thymus: localization in dendritic cells and macrophages, Endocrinology, 139, 2399-2406, 1998.
35. Hunziker, R. D. and Wegmann, T. G., Placental immunoregulation, Crit. Rev. Immunol., 6, 245-285, 1993.
36. Medawar, P. B., Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates, Symp. Soc. Exp. Biol., 7, 320-338, 1954.
37. Redline, R. W. and Lu, C. Y., Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta. Implications for maternal-fetal immunological relationship, Lab. Invest., 61, 27-36, 1989.
38. Hunt, J. S., Immunobiology of pregnancy, Curr. Biol., 4, 591-596, 1992.
39. Le Bouteiller, P., HLA-G: what's new? Am. J. Reprod. Immunol., 38, 146-149, 1997.
40. Chaouat, G. and Menu, E., Maternal T cell reactivity in pregnancy? Curr. Top. Microbiol. Immunol., 222, 103-126, 1997.
41. Beer, A. E., Kwak, J. Y. H., and Ruiz, J. E., The biological basis of passage of fetal cellular material into the maternal circulation, Ann. N.Y. Acad. Sci., 731, 21-35, 1994.
42. Bonney, E. A. and Matzinger, P., The maternal immune system's interaction with circulating fetal cells, J. Immunol., 158, 40-47, 1997.
43. Carbone, F. R., Kurts, C., Bennett, S. R. M., Miller, J. F. A. P., and Heath, W. R., Cross-presentation: a general mechanism for CTL immunity and tolerance, Immunol. Today, 368, 368-373, 1998.
44. Liu, Y. and Janeway, C. A., Microbial induction of costimulatory activity for CD4 T cell growth, Int. Immunol., 3, 323-332, 1991.
45. Matzinger, P., Tolerance, danger and the extended family, Ann. Rev. Immunol., 12, 991-1045, 1994.
46. Janeway, C. A., Goodnow, C. C., and Medzhitov, R., Immunological tolerance: Danger - pathogen on the premises! Curr. Biol., 5, 519-522, 1996.
47. Carter, J., Newport, A., Keeler, K. D., and Dresser, D. W., FACS analysis of changes in T and B lymphocyte populations in the blood, spleen and lymph nodes of pregnant mice, Immunology, 48, 791-797, 1983.
48. Couderc, B., Mohammad, M., Bouc, A. M., Mayer, G., and Chateaureynaud, P., Maternal alloimmunization in rat pregnancy: in vivo and in vitro studies of T-cell-dependent immunity to mating and third party alloantigens, Dev. Comp. Immunol., 16, 485-492, 1992.
49. Gambel, P. I., Cleland, A. W., and Ferguson, F. G., Alterations in thymus and spleen cell populations and immune reactivity during syngeneic pregnancy and lactation, J. Clin. Lab. Immunol., 3, 115-119, 1980.
50. Gottesman, S. R. and Stutman, O., Cellular immunity during pregnancy. I. Proliferative and cytotoxic reactivity of paraaortic lymph nodes, Am. J. Reprod. Immunol., 1, 10-17, 1980.
51. Gottesman, S. R. and Stutman, O., Cellular immunity during pregnancy. II. Response to T and B cell mitogens, Am. J. Reprod. Immunol., 1, 78-82, 1981.
52. + T cell clones during normal pregnancy, Em. J. Immunol., 26, 834-838, 1996
53. Matthiesen, L., Berg, G., Ernerudh, J., and Hakansson, L., Lymphocyte subsets and mitogen stimulation of blood lymphocytes in normal pregnancy, Am. J. Reprod. Immunol., 35, 70-79, 1996
54. Tallon, D. F., Corcoran, D. J. D., O'Dwyer, E. M., and Greally, J. F., Circulating lymphocyte subpopulations in pregnancy: a longitudinal study, J. Immunol., 132, 1784-1787, 1984.
55. Watanabe, M., Iwatani, Y., Kaneda, T., Hidaka Y., Mitsuda, N., Morimoto, Y., and Amino, N. Changes in T, B, and NK lymphocyte subsets during and after normal pregnancy, Am. J. Reprod. Immunol., 37, 368-377, 1997.
56. Tafuri, A., Alferink, J., Moller, P., Hammerling G. J., and Arnold, B., T cell awareness of paternal alloantigens during pregnancy, Science, 270, 630-633, 1995.
57. Jiang, S. P. and Vacchio, M. S., Multiple mechanisms of peripheral T cell tolerance to the fetal "allograft", J. Immunol., 160, 3086-3090, 1998.
58. The, H.-S., Kisielow, P. H., Scott, B., Kishi, H., Uematsu, Y., Bluthmann, H., and vonBoehmer, H. Thymic MHC antigens and the specificity of the αβ T cell receptor determine the CD4/CD8 phenotype of T cells, Nature, 333, 742-746, 1988.
59. Rogers, A. M., Boime, I., Connolly, J., Cook, J. R. and Russell, J. H., Maternal-fetal tolerance is maintained despite transgene-driven trophoblast expression of MHC class I and defects in Fas and its ligand. Eur. J. Immunol., 28, 3479-3487, 1998.
60. Rocha, B., Grandien, A., and Freitas, A. A., Anergy and exhaustion are independent mechanisms of peripheral T cell tolerance, J. Exp. Med., 181, 993-1003, 1995.
61. + T cell function during in vivo memory or tolerance induction, Immunity, 8, 581-590, 1998.
62. Billingham, R. E. and Hings, I. M., The H-Y antigen and its role in natural transplantation, Hum. Genet., 58, 9-17, 1981.
63. Rotzshke, O., Falk, K., Wallny, H.-J., Faathe, S., and Rammensee, H.-G., Characterization of naturally occurring minor histocompatibility peptides including H-4 and H-Y, Science, 249, 283-287, 1990
64. Scott, D. M., Ehrmann, I. E., Ellis, P. S., Bishop, C. E., Aguinik, A. I., Simpson, E., and Mitchell, M. J., Identification of a mouse male-specific trans plantation antigen, H-Y, Nature, 376, 695-698, 1995.
65. b epitope is encoded by a novel mouse Y chromosome gene, Nat. Gen., 14, 474-478, 1996.
66. Simpson, E., Scott, D., and Chandler, P., The male-specific histocompatibility antigen, H-Y: a history of transplantation, immune response genes, sex determination and expression cloning, Ann. Rev. Immunol., 15, 39-61, 1997.
67. Heath, W. R., Kurts, C., Miller, J. F. A. P., and Carbone, F. R., Cross-tolerance: a pathway for inducing tolerance to peripheral tissue antigens, J. Exp. Med., 187, 1549-1553, 1998.
68. + T cells induced by cross-presentation of self-antigens involves signaling through CD95 (Fas, Apo-1), J. Exp. Med., 188, 415-420, 1998.
69. Kurts, C., Kosaka, H., Carbone, F. R., Miller, J. F., and Heath, W. R., Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells, J. Exp. Med., 186, 239-245, 1997.
70. Kurts, C., Miller, J. F. A. P., Subramaniam, R. M., Carbone, F. R., and Heath, W. R., Major histocompatibility complex class I-restricted cross-presentation is biased towards high dose antigens and those released during cellular destruction, J. Exp. Med., 188, 409-414, 1998.
71. Albert, M. L., Sauter, B., and Bhardwaj, N., Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs, Nature, 392, 86-89, 1998.
72. Streilein, J. W., Unraveling immune privilege, Science, 270, 1158-1159, 1995.
73. Beer, A. E. and Billingham, R. E., Host responses to intra-uterine tissue, cellular and fetal allografts, J. Reprod. Fertil. Suppl., 21, 59-69, 1974.
74. Simmons, R. L. and Russell, P. S., The antigenicity of the mouse trophoblast, Ann. N.Y. Acad. Sci., 99, 717-727, 1962.
75. Bellgrau, D., Gold, D., Selawry, H., Morre, J., Franzusoff, A., and Duke, R. C., A role of CD95 ligand in preventing graft rejection, Nature, 377, 630-632, 1995.
76. Griffith, T. S., Brunner, T., Fletcher, S. M., Green, D. R., and Ferguson, T. A., Fas ligand-induced apoptosis as a mechanism of immune privilege, Science, 270, 1189-1192, 1995.
77. Crispe, I. N., Fatal interactions: fas-induced apoptosis of mature T cells, Immunity, 1, 347-349, 1994.
78. Runic, R., Lockwood, C. J., Ma, Y., Dipasquale, B., and Guller, S., Expression of fas ligand by human cytotrophoblasts: implications in placentation and fetal survival, J. Clin. Endocrinol. Metab., 81, 3119-3122, 1996.
79. Hunt, J. S., Vassmer, D., Ferguson, T. A., and Miller, L., Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus, J. Immunol., 158, 4122-4128, 1997.
80. Jerzak, M., Kasprzycka, M., Wierzbicki, P., Kotarski, J., and Gorski, A., Apoptosis of T cells in the first trimester human decidua, Am. J. Reprod. Immunol., 40, 130-135, 1998.
81. Luft, B. J. and Remington, J. S., Effect of pregnancy on resistance to Listeria monocytogenes and Toxoplasma gondii infections in mice, Infect. Immunol., 38, 1164-1171, 1982.
82. Ostensen, M., Pregnancy in psoriatic arthritis, Scand. J. Rheumatol., 17, 67-70, 1988.
83. Ostensen, M. and Husby, G., A prospective study of the effect of pregnancy on rheumatoid arthritis and ankylosing spondylitis, Arthritis Rheum., 26, 1155-1159, 1983.
84. Varner, M. W., Autoimmune disorders and pregnancy, Semin. Perinatol., 15, 238-250, 1991.
85. Holland, D., Bretscher, P., and Russell, A. S., Immunologie and inflammatory responses during pregnancy, J. Clin. Lab. Immunol., 14, 177-179, 1984.
86. Dresser, D. W., The potentiating effect of pregnancy on humoral immune responses of mice, J. Reprod. Immunol., 20, 253-266, 1991.
87. Wegmann, T. G., Lin, H., Guilbert, L., and Mosmann, T. R., Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a Th2 phenomenon? Immunol. Today, 14, 353-356, 1993.
88. Lin, H., Mosmann, T. R., Guilbert, L., Tuntipopipat, S., and Wegmann, T. G., Synthesis of T helper 2-type cytokines at the maternal-fetal interface, J. Immunol., 151, 4562-4573, 1993.
89. Krishman, L., Guilbert, L. J., Russell, A. S., Wegmann, T. G., Mossmann, T. R., and Belosevic, M., Pregnancy impairs resistance of C57B1/6 mice to Leishmania major infection and causes decreased antigen specific gamma-IFN responses and increased production of T helper 2 cytokines, J. Immunol., 156, 644-652, 1996.
90. Krishman, L., Guilbert, L. J., Wegmann, T. G., Belosevic, M., and Mossmann, T. R., T helper 1 responses against Leishmania major in pregnant C57B1/6 mice increases implantation failure and fetal resorptions, J. Immunol., 156, 653-662, 1996.
91. Chaouat, G., Meliani, A. A., Clark, D. A., Dy, M., Minkowski, M., and Wegmann, T. G., Control of fetal survival in CBAxDBA/2 mice by lymphokine therapy, J. Reprod. Fertil., 89, 447-452, 1990.
92. Chaouat, G., Meliani, A. A., Martal, J., Raghupathy, R., Elliot, J., Mosmann, T., and Wegmann, T. G., IL-10 prevents naturally occurring fetal loss in the CBAxDBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-t, J. Immunol., 154, 4621-4630, 1995.
93. Hill, J. A., Polgar, K., and Anderson, D. J., T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion, JAMA, 273, 1933-1936, 1995.
94. Piccinni, M.-P., Giudizi, M.-G., Biagiotti, R., Beloni, L., Giannarini, L., Sampognaro, S., Parronchi, P., Manetti, R., Annunziato, F., Livi, C., et al., Progesterone favors the development of human T helper cells producting Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones, J. Immunol., 155, 128-133, 1995.
95. Szekeres-Bartho, J., Faust, Z., Varga, P., Szereday, L., and Kelemen, K., The immunological pregnancy protective effect of progesterone is manifested via controlling cytokine production, Am. J. Reprod. Immunol., 35, 348-351, 1996.
96. Takeuchi, M., Alard, P., and Streilein, J. W., TGF-β promotes immune deviation by altering accessory signals of antigen-presenting cells, J. Immunol., 160, 1589-1597, 1998.
97. Munn, D. H., Zhou, M., Attwood, J. T., Bondarev I., Conway, S. J., Marshall, B., Brown, C., and Mellor A. L., Prevention of allogeneic fetal rejection by tryptophan catabolism, Science, 281, 1191-1193, 1998
98. Munn, D. H., Pressey, J., Beall, A. C., Hudes, R. and Alderson, M. R., Selective activation-induced apoptosis of peripheral T cells imposed by macrophages. A potential mechanism of antigen-specic peripheral lymphocyte deletion, J. Immunol., 156, 523-532, 1996.
99. Schrocksnadel, H., Baier-Bitterlich, G., Dapunt, O., Wachter, H., and Fuchs, D., Decreased plasma tryptophan in pregnancy, Obstet. Gynecol., 88, 47-50, 1996.