Seminars in Fetal & Neonatal Medicine
Volume 11, Issue 5 , Pages 279-295 , October 2006

Immunology of normal pregnancy

References 

  1. Fugmann SD, Lee AI, Shockett PE, Villey IJ, Schatz DG. The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Annu Rev Immunol. 2000;18:495–527
  2. Aagaard-Tillery KM, Jelinek DF. Inhibition of human B lymphocyte cell cycle progression and differentiation by rapamycin. Cell Immunol. 1994;156:493–507
  3. Aagaard-Tillery KM, Jelinek DF. Phosphatidylinositol 3-kinase activation in normal human B lymphocytes. J Immunol. 1996;156:4543–4554
  4. Aagaard-Tillery KM, Jelinek DF. A role for phosphatidylinositol 3-kinase in generating T cell help for B cell growth and differentiation. J Immunol. 1996;157:2769–2778
  5. Metcalf D. The molecular control of cell division, differentiation commitment and maturation in haemopoietic cells. Nature. 1989;339:27–30
  6. Nunez C, Nishimoto N, Gartland GL, Billips LG, Burrows PD, Kubagawa H, et al. B cells are generated throughout life in humans. J Immunol. 1996;156:866–872
  7. Peault B. In-vitro models of stroma-dependent lymphopoiesis. Semin Immunol. 1995;7:169–175
  8. Tarlinton D. B-cell differentiation in the bone marrow and the periphery. Immunol Rev. 1994;137:203–229
  9. Jerne N. The natural-selection theory of antibody formation. Proc Natl Acad Sci USA. 1955;4:849
  10. Burnet M. The clonal selection theory of acquired immunity. Nashville, TN: Vanderbuilt University Press; 1959;p 209.
  11. Tonegawa S. Somatic generation of antibody diversity. Nature. 1983;302:575–581
  12. Nemazee D, Buerki K. Clonal deletion of autoreactive B lymphocytes in bone marrow chimeras. Proc Natl Acad Sci USA. 1989;86:8039–8043
  13. Aagaard-Tillery KM, Jelinek DF. Differential activation of a calcium-dependent endonuclease in human B lymphocytes. Role in ionomycin-induced apoptosis. J Immunol. 1995;155:3297–3307
  14. Allen RC, Armitage RJ, Conley ME, Rosenblatt H, Jenkins NA, Copeland NG, et al. CD40 ligand gene defects responsible for X-linked hyper-IgM syndrome. Science. 1993;259:990–993
  15. Aruffo A, Farrington M, Hollenbaugh D, Li X, Milatovich A, Nonoyama S, et al. The CD40 ligand, gp39, is defective in activated T cells from patients with X-linked hyper-IgM syndrome. Cell. 1993;72:291–300
  16. Robey E, Schlissel M. Lymphocyte development. Curr Opin Immunol. 2003;15:155–157
  17. Von Boehmer H, Aifantis I, Gounari F, Azogui O, Haughn L, Apostolou I, et al. Thymic selection revisited: how essential is it?. Immunol Rev. 2003;191:62–78
  18. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986;136:2348–2357
  19. Hansen T, Sachs D. The major histocompatibility complex. In:  Paul W editors. Fundamental immunology. New York: Raven Press; 1989;p. 445–488
  20. Zika E, Ting JP. Epigenetic control of MHC-II: interplay between CIITA and histone-modifying enzymes. Curr Opin Immunol. 2005;17:58–64
  21. Magner WJ, Kazim AL, Stewart C, Romano MA, Catalano G, Grande C, et al. Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors. J Immunol. 2000;165:7017–7024
  22. Acuto O, Cantrell D. T cell activation and the cytoskeleton. Annu Rev Immunol. 2000;18:165–184
  23. Clements JL, Boerth NJ, Lee JR, Koretzky GA. Integration of T cell receptor-dependent signaling pathways by adapter proteins. Annu Rev Immunol. 1999;17:89–108
  24. 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
  25. Thomas IK, Erickson KL. Gestational immunosuppression is mediated by specific Lyt 2+ T cells. Immunology. 1986;57:201–206
  26. Mincheva-Nilsson L, Hammarstrom S, Hammarstrom ML. Human decidual leukocytes from early pregnancy contain high numbers of gamma delta+ cells and show selective down-regulation of alloreactivity. J Immunol. 1992;149:2203–2211
  27. Ditzian-Kadanoff R, GAron J, Verp MS, Zilberstein M. Gamma delta T cells in human decidua. Am J Obstet Gynecol. 1993;168:831–836
  28. Heyborne KD, Cranfill RL, Carding SR, Born WK, O'Brien RL. Characterization of gamma delta T lymphocytes at the maternal–fetal interface. J Immunol. 1992;149:2872–2878
  29. Bonney EA, Pudney J, Anderson DJ, Hill JA. Gamma-delta T cells in midgestation human placental villi. Gynecol Obstet Invest. 2000;50:153–157
  30. Barakonyi A, Polgar B, Szekeres-Bartho J. The role of gamma/delta T-cell receptor-positive cells in pregnancy: part II. Am J Reprod Immunol. 1999;42:83–87
  31. Heyborne K, Fu YX, Nelson A, Farr A, O'Brien R, Born W. Recognition of trophoblasts by gamma delta T cells. J Immunol. 1994;153:2918–2926
  32. Heyborne KD, Silver RM. Immunology of postimplantation pregnancy. In:  Bronson RA,  Alexander NJ,  Anderson OJ, et al. editor. Reproductive immunology. Cambridge, MA: Blackwell Scientific Publications; 1996;p. 383–412
  33. Nahmias AJ, Kourtis AP. The great balancing acts. The pregnant woman, placenta, fetus, and infectious agents. Clin Perinatol. 1997;24:497–521
  34. Murray DL, Imagawa DT, Okada DM, St Geme JW. Antibody response to monovalent A/New Jersey/8/76 influenza vaccine in pregnant women. J Clin Microbiol. 1979;10:184–187
  35. Jones WR, Hawes CS, Kemp AS. Studies on cell-mediated immunity in human pregnancy. In:  Wegmann TG,  Gill TJ editor. Immunology of reproduction. New York: Oxford University Press; 1983;p. 363–380
  36. Stiehm ER, Fudenberg HH. Serum levels of immune globulins in health and disease: a survey. Pediatrics. 1966;37:715–727
  37. Ballow M, Cates KL, Rowe JC, Goetz C, Desbonnet C. Development of the immune system in very low birth weight (less than 1500 g) premature infants: concentrations of plasma immunoglobulins and patterns of infections. Pediatr Res. 1986;20:899–904
  38. Baker CJ, Edwards MS, Kasper DL. Role of antibody to native type III polysaccharide of group B Streptococcus in infant infection. Pediatrics. 1981;68:544–549
  39. Morell A, Sidiropoulos D, Herrmann U, Romano MA, Catalano G, Grande C, et al. IgG subclasses and antibodies to group B streptococci in preterm neonates after intravenous infusion of immunoglobulin to the mothers. Pediatr Infect Dis. 1986;5(Suppl. 3):S195–S197
  40. Griffiths-Chu S, Patterson JA, Berger CL, Edelson RL, Chu AC. Characterization of immature T cell subpopulations in neonatal blood. Blood. 1984;64:296–300
  41. Solinger AM. Immature T lymphocytes in human neonatal blood. Cell Immunol. 1985;92:115–122
  42. Harris DT, Schumacher MJ, Locascio J, Besencon FJ, Olson GB, DeLuca D, et al. Phenotypic and functional immaturity of human umbilical cord blood T lymphocytes. Proc Natl Acad Sci USA. 1992;89:10006–10010
  43. Wilson CB, Westall J, Johnston L, Lewis DB, Dower SK, Alpert AR. Decreased production of interferon-gamma by human neonatal cells. Intrinsic and regulatory deficiencies. J Clin Invest. 1986;77:860–867
  44. Granberg C, Hirvonen T. Cell-mediated lympholysis by fetal and neonatal lymphocytes in sheep and man. Cell Immunol. 1980;51:13–22
  45. Sullender WM, Miller JL, Yasukawa LL, Bradley JS, Black SB, Yeager AS, et al. Humoral and cell-mediated immunity in neonates with herpes simplex virus infection. J Infect Dis. 1987;155:28–37[Erratum: J Infect Dis 1987;155:838]
  46. Rai R, Sacks G, Trew G. Natural killer cells and reproductive failure - theory, practice and prejudice. Hum Reprod. 2005;20:1123–1126
  47. Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood. 2001;97:3146–3151
  48. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med. 2003;198:1201–1212
  49. Parham P. NK cells and trophoblasts: partners in pregnancy. J Exp Med. 2004;200:951–955
  50. Szekeres-Bartho J. Immunological relationship between the mother and the fetus. Int Rev Immunol. 2002;21:471–495
  51. Hunt JS, Jadhav L, Chu W, Geraghty DE, Ober C. Soluble HLA-G circulates in maternal blood during pregnancy. Am J Obstet Gynecol. 2000;183:682–688
  52. Lila N, Rouas-Freiss N, Dausset J, Carpentier A, Carosella ED. Soluble HLA-G protein secreted by allo-specific CD4+ T cells suppresses the allo-proliferative response: a CD4+ T cell regulatory mechanism. Proc Natl Acad Sci USA. 2001;98:12150–12155
  53. Kanai T, Fujii T, Unno N, Yamashita T, Hyodo H, Miki A, et al. Human leukocyte antigen-G-expressing cells differently modulate the release of cytokines from mononuclear cells present in the decidua versus peripheral blood. Am J Reprod Immunol. 2001;45:94–99
  54. Hunt JS, Fishback JL, Chumbley G, Loke YW. Identification of class I MHC mRNA in human first trimester trophoblast cells by in situ hybridization. J Immunol. 1990;144:4420–4425
  55. Yelavarthi KK, Fishback JL, Hunt JS. Analysis of HLA-G mRNA in human placental and extraplacental membrane cells by in situ hybridization. J Immunol. 1991;146:2847–2854
  56. Sunderland CA, Redman CW, Stirrat GM. HLA A, B, C antigens are expressed on nonvillous trophoblast of the early human placenta. J Immunol. 1981;127:2614–2615
  57. Lata JA, Tuan RS, Shepley KJ, Mulligan MM, Jackson LG, Smith JB. Localization of major histocompatibility complex class I and II mRNA in human first-trimester chorionic villi by in situ hybridization. J Exp Med. 1992;175:1027–1032
  58. Hunt JS, Fishback JL, Andrews GK, Wood GW. Expression of class I HLA genes by trophoblast cells. Analysis by in situ hybridization. J Immunol. 1988;140:1293–1299
  59. Hviid TV, Hylenius S, Lindhard A, Christianson OB. Association between human leukocyte antigen-G genotype and success of in vitro fertilization and pregnancy outcome. Tissue Antigens. 2004;64:66–69
  60. Rosa F, Hatat D, Abadie A, Fellous M. Regulation of histocompatibility antigens by interferon. Ann Inst Pasteur Immunol. 1985;136C:103–119
  61. Collins T, Lapierre LA, Fiers W, Strominger JL, Pober JS. Recombinant human tumor necrosis factor increases mRNA levels and surface expression of HLA-A,B antigens in vascular endothelial cells and dermal fibroblasts in vitro. Proc Natl Acad Sci USA. 1986;83:446–450
  62. Zuckermann F, Head JR. Expression of MHC antigens on murine trophoblast and their modulation by interferon. J Immunol. 1986;137:846–853
  63. King A, Hiby SE, Gardner L, Joseph S, Bowen JM, Verma S, et al. Recognition of trophoblast HLA class I molecules by decidual NK cell receptors - a review. Placenta. 2000;21(Suppl. A):S81–S85
  64. Holbrook KA. Structural and biochemical organogenesis of skin and cutaneous appendages in the fetus and neonate. In:  Polin RA,  Fox WW editor. Fetal and neonatal physiology. Philadelphia: WB Saunders; 1992;p. 527–553
  65. Fauser AA, Messner HA. Granuloerythropoietic colonies in human bone marrow, peripheral blood, and cord blood. Blood. 1978;52:1243–1248
  66. Messner HA, Fauser AA. Culture studies of human pluripotent hemopoietic progenitors. Blut. 1980;41:327–333
  67. Messner HA, Izaquirre CA, Jamal N. Identification of T lymphocytes in human mixed hemopoietic colonies. Blood. 1981;58:402–405
  68. Kelemen E, Janossa M. Macrophages are the first differentiated blood cells formed in human embryonic liver. Exp Hematol. 1980;8:996–1000
  69. Beelen RHJ, van Rees EP, Bos HJ. Ontogeny of antigen-presenting cells. In:  Chaouat G editors. The immunology of the fetus. Boca Raton, FL: CRC Press; 1990;p. 110–133
  70. Stiehm ER. Fetal defense mechanisms. Am J Dis Child. 1975;129:438–443
  71. Klein RB, Fischer TJ, GArd SE, Biberstein M, Rich KC, Stiehm ER. Decreased mononuclear and polymorphonuclear chemotaxis in human newborns, infants, and young children. Pediatrics. 1977;60:467–472
  72. Li Y, Ohls RK, Christensen RD. Effects of recombinant granulocyte-macrophage colony stimulating factor on the capacity of mononuclear cells from preterm infants to generate interleukin-6 and granulocyte colony-stimulating factor. Int J Pediatr Hematol Oncol. 1996;3:63–66
  73. Forestier F, Daffos F, Galacteros F, Bardakjian J, Rainaut M, Beuzard Y. Hematological values of 163 normal fetuses between 18 and 30 weeks of gestation. Pediatr Res. 1986;20:342–346
  74. Shigeoka AO, Santos JI, Hill HR. Functional analysis of neutrophil granulocytes from healthy, infected, and stressed neonates. J Pediatr. 1979;95:454–460
  75. Anderson DC, Hughes BJ, Smith CW. Abnormal mobility of neonatal polymorphonuclear leukocytes. Relationship to impaired redistribution of surface adhesion sites by chemotactic factor or colchicine. J Clin Invest. 1981;68:863–874
  76. Anderson DC, Freeman KB, Hughes BJ, Buffone GJ. Secretory determinants of impaired adherence and motility of neonatal PMNs. Pediatr Res. 1985;19:257A
  77. Uksila J, Lassila O, Hirvonen T, Toivanen P. Development of natural killer cell function in the human fetus. J Immunol. 1983;130:153–156
  78. Berry SM, Fine N, Bichalski JA, Cotton DB, Dombrowski MP, Kaplan J. Circulating lymphocyte subsets in second- and third-trimester fetuses: comparison with newborns and adults. Am J Obstet Gynecol. 1992;167:895–900
  79. Lubens RG, GArd SE, Soderberg-Warner M, Stiehm ER. Lectin-dependent T-lymphocyte and natural killer cytotoxic deficiencies in human newborns. Cell Immunol. 1982;74:40–53
  80. Harrison CJ, Waner JL. Natural killer cell activity in infants and children excreting cytomegalovirus. J Infect Dis. 1985;151:301–307
  81. Faulk WP, Temple A. Distribution of beta2 microglobulin and HLA in chorionic villi of human placentae. Nature. 1976;262:799–802
  82. Bulmer JN, Johnson PM. Antigen expression by trophoblast populations in the human placenta and their possible immunobiological relevance. Placenta. 1985;6:127–140
  83. Redman CW, McMichael AL, Stirrat GM, Sunderland CA, Ting A. Class I major histocompatability complex antigens on extravillus trophoblast. Immunology. 1984;52:457–468
  84. Hsi BL, Yeh CJ, Faulk WP. Class I antigens of the major histocompatibility complex on cytotrophoblast of human chorion laeve. Immunology. 1984;52:621–629
  85. Hunt JS, Lessin DL, King CR. Ontogeny and distribution of cells expressing HLA-B locus-specific determinants in the placenta and extraplacental membranes. J Reprod Immunol. 1989;15:21–30
  86. Shukla H, Swaroop A, Srivastava R, Weissman SM. The mRNA of a human class I gene HLA G/HLA 6.0 exhibits a restricted pattern of expression. Nucleic Acids Res. 1990;18:2189
  87. Houlihan JM, Biro PA, Fergar-Payne A, Simpson KL, Holmes CH. Evidence for the expression of non-HLA-A,-B,-C class I genes in the human fetal liver. J Immunol. 1992;149:668–675
  88. Kirszenbaum M, Moreau P, Gluckman E, Dausset J, Carosella E. An alternatively spliced form of HLA-G mRNA in human trophoblasts and evidence for the presence of HLA-G transcript in adult lymphocytes. Proc Natl Acad Sci USA. 1994;91:4209–4213
  89. Grusby MJ, Auchincloss H, Lee R, et al. Mice lacking major histocompatibility complex class I and class II molecules. Proc Natl Acad Sci USA. 1993;90:3913–3917
  90. Hunt JS, Vassmer D, Ferguson TA, 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. 1997;158:4122–4128
  91. Runic R, Lockwood CJ, MA Y, Dipasquale B, Guller S. Expression of Fas ligand by human cytotrophoblasts: implications in placentation and fetal survival. J Clin Endocrinol Metab. 1996;81:3119–3122
  92. Bamberger AM, Schulte HM, Thuneke I, Erdmann I, Bamberger CM, Asa SL. Expression of the apoptosis-inducing Fas ligand (FasL) in human first and third trimester placenta and choriocarcinoma cells. J Clin Endocrinol Metab. 1997;82:3173–3175
  93. Kauma SW, Huff TF, Hayes N, Nilkaeo A. Placental Fas ligand expression is a mechanism for maternal immune tolerance to the fetus. J Clin Endocrinol Metab. 1999;84:2188–2194
  94. Hammer A, Blaschitz A, Daxbock C, Walcher W, Dohr G. Fas and Fas-ligand are expressed in the uteroplacental unit of first-trimester pregnancy. Am J Reprod Immunol. 1999;41:41–51
  95. Li W, Whaley CD, Bonnevier JL, Mondino A, Martin ME, Aagaard-Tillery KM, et al. CD28 signaling augments Elk-1-dependent transcription at the c-fos gene during antigen stimulation. J Immunol. 2001;167:827–835
  96. Lenschow DJ, Zeng Y, Thistlethwaite JR, et al. Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4lg. Science. 1992;257:789–792
  97. Kaufman KA, Bowen JA, Tsai AF, Bluestone JA, Hunt JS, Ober C. The CTLA-4 gene is expressed in placental fibroblasts. Mol Hum Reprod. 1999;5:84–87
  98. Chambers CA, Cado D, Truong T, Allison JP. Thymocyte development is normal in CTLA-4-deficient mice. Proc Natl Acad Sci USA. 1997;94:9296–9301
  99. Bulmer JN, Johnson PM, Bulmer D. Leukocyte populations in human decidua and endometrium. In:  Gill TJ,  Wegmann TG,  Nisbet-Brown E editor. Immunoregulation and fetal survival. New York: Oxford University Press; 1987;p. 223–247
  100. Starkey PM, Sargent IL, Redman CW. Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology. 1988;65:129–134
  101. Zheng LM, Ojcius DM, Young JD. Role of granulated metrial gland cells in the immunology of pregnancy. Am J Reprod Immunol. 1991;25:72–76
  102. Kammerer U, Marzusch K, Krober S, Ruck P, Handgretinger R, Dietl J. A subset of CD56+ large granular lymphocytes in first-trimester human decidua are proliferating cells. Fertil Steril. 1999;71:74–79
  103. Kodama T, Hara T, Okamoto E, Kusunoki Y, Ohama K. Characteristic changes of large granular lymphocytes that strongly express CD56 in endometrium during the menstrual cycle and early pregnancy. Hum Reprod. 1998;13:1036–1043
  104. King A, Birkby C, Loke YW. Early human decidual cells exhibit NK activity against the K562 cell line but not against first trimester trophoblast. Cell Immunol. 1989;118:337–344
  105. Redman CWG, Ferry BL, Jackson MC. Immune cell populations in human early pregnancy decidua. In:  Wegmann TF,  Gill TJ,  Nisbet-Brown E editor. Molecular and cellular immunobiology of the maternal–fetal interface. New York: Oxford University Press; 1991;p. 110–136
  106. Guimond MJ, Luross JA, Wang B, Terhorst C, Danial S, Croy BA. Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol Reprod. 1997;56:169–179
  107. Guimon MJ, Wang B, Croy BA. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med. 1998;187:217–223
  108. Guimond M, Wang B, Croy BA. Immune competence involving the natural killer cell lineage promotes placental growth. Placenta. 1999;20:441–450
  109. Bulmer JN, Sunderland CA. Immunohistological characterization of lymphoid cell populations in the early human placental bed. Immunology. 1984;52:349–357
  110. Redline RW, Lu CY. Role of local immunosuppression in murine fetoplacental listeriosis. J Clin Invest. 1987;79:1234–1241
  111. Redline RW, McKay DB, Vazquez MA, Papaioannou VE, Lu CY. Macrophage functions are regulated by the substratum of murine decidual stromal cells. J Clin Invest. 1990;85:1951–1958
  112. Chang MD, Pollard JW, Khalili H, Goyert SM, Diamond B. Mouse placental macrophages have a decreased ability to present antigen. Proc Natl Acad Sci USA. 1993;90:462–466
  113. Castellucci M, Kosanke G, Verdenelli F, Huppertz B, Kaufman P. Villous sprouting: fundamental mechanisms of human placental development. Hum Reprod Update. 2000;6:485–494
  114. Anderson DJ, Hill JA, Haimovici F, Berkowitz RS. Adverse effects of immune cell products in pregnancy. In:  Wegmann TF,  Gill TJ,  Nisbet-Brown E editor. Molecular and cellular immunobiology of the maternal–fetal interface. New York: Oxford University Press; 1991;p. 207–236
  115. Paterson WG, Grant KA. Advanced intraligamentous pregnancy. Report of a case, review of the literature and a discussion of the biological implications. Obstet Gynecol Surv. 1975;30:715–726
  116. Steven DH, Morris G. Development of the fetal membranes. In:  Steven DH editors. Comparative placentation: essays in structure and function. New York: Academic Press; 1975;p. 58–61
  117. Berkowitz RS, Hill JA, Kurtz CB, Anderson DJ. Effects of products of activated leukocytes (lymphokines and monokines) on the growth of malignant trophoblast cells in vitro. Am J Obstet Gynecol. 1988;158:199–203
  118. Yui J, Garcia-Lloret MI, Wegmann TG, Berkowitz RS. In:  Soares MJ,  Handwerger S,  Talamantes F editor. Disruption of trophoblast monolayers by TNF-alpha and IFN-gamma and antagonism by GM-CSF. Boston, USA: Serono Symposia; 1993;p. 174–179
  119. Drake BL, Head JR. Murine trophoblast cells are not killed by tumor necrosis factor-alpha. J Reprod Immunol. 1990;17:93–99
  120. Hill JA, Haimovici F, Anderson DJ. Products of activated lymphocytes and macrophages inhibit mouse embryo development in vitro. J Immunol. 1987;139:2250–2254
  121. Hill JA, Polgar K, Harlow BL, Anderson DJ. Evidence of embryo- and trophoblast-toxic cellular immune response(s) in women with recurrent spontaneous abortion. Am J Obstet Gynecol. 1992;166:1044–1052
  122. Hill JA, Polgar K, Anderson DJ. T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. J Am Med Assoc. 1995;273:1933–1936
  123. Silen ML, Firpo A, Morgello S, Lowry SF, Francus T. Interleukin-1 alpha and tumor necrosis factor alpha cause placental injury in the rat. Am J Pathol. 1989;135:239–244
  124. Romero R, Mazor M, Tartakovsky B. Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol. 1991;165:969–971
  125. Silver RM, Edwin SS, Umar F, Dudley DJ, Branch DW, Mitchell MD. Bacterial lipopolysaccharide-mediated murine fetal death: the role of interleukin-1. Am J Obstet Gynecol. 1997;176:544–549
  126. Tezabwala BU, Johnson PM, Rees RC. Inhibition of pregnancy viability in mice following IL-2 administration. Immunology. 1989;67:115–119
  127. Chaouat G, menu E, Clark DA, Dy M, Minkowski M, Wegmann TG. Control of fetal survival in CBA x DBA/2 mice by lymphokine therapy. J Reprod Fertil. 1990;89:447–458
  128. Lala PK, Scodras LM, Graham CH, Lysiak JJ, Parhar RS. 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. 1990;127:368–381
  129. Silver RM, Lohner WS, DAynes RA, Mitchell MD, Branch DW. Lipopolysaccharide-induced fetal death: the role of tumor-necrosis factor alpha. Biol Reprod. 1994;50:1108–1112
  130. Bone RC. The pathogenesis of sepsis. Ann Intern Med. 1991;115:457–469
  131. Benyo DF, Miles TM, Conrad KP. Hypoxia stimulates cytokine production by villous explants from the human placenta. J Clin Endocrinol Metab. 1997;82:1582–1588
  132. Munn D, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 1998;281:1191–1193
  133. Mellor AL, Sivakumar J, Chandler P, Smith K, Molina H, Mao D, et al. Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol. 2001;2:64–68
  134. Kamimura S, Eguchi K, Yonezawa M, Sekiba K. Localization and developmental change of indoleamine 2,3-dioxygenase activity in the human placenta. Acta Med Okayama. 1991;45:135–139
  135. Sedlmayr P, Blaschitz A, Wintersteiger R, Semlitsch M, Hammer A, MacKenzie CR, et al. Localization of indoleamine 2,3-dioxygenase in human female reproductive organs and the placenta. Mol Hum Reprod. 2002;8:385–391
  136. Kudo Y, Boyd CA, Sargent IL, Redman CW. Modulation of indoleamine 2,3-dioxygenase by interferon-gamma in human placental chorionic villi. Mol Hum Reprod. 2000;6:369–374
  137. Kudo Y, Boyd CA, Sargent IL, Redman CW. Tryptophan degradation by human placental indoleamine 2,3-dioxygenase regulates lymphocyte proliferation. J Physiol. 2001;535:207–215
  138. Santoso DI, Rogers P, Wallace EM, Manuelpillai U, Walker D, Subakir SB. Localization of indoleamine 2,3-dioxygenase and 4-hydroxynonenal in normal and pre-eclamptic placentae. Placenta. 2002;23:373–379
  139. Gendron RL, Baines MG. Infiltrating decidual natural killer cells are associated with spontaneous abortion in mice. Cell Immunol. 1988;113:261–267
  140. de Fougerolles AR, Baines MG. Modulation of the natural killer cell activity in pregnant mice alters the spontaneous abortion rate. J Reprod Immunol. 1987;11:147–153
  141. Zuckermann FA, Head JR. Susceptibility of mouse trophoblast to antibody and complement-mediated damage. Transplant Proc. 1985;17:925–930
  142. Zuckermann F, Head JR. Possible mechanism of non-rejection of the feto-placental allogaft: trophoblast resistance to lysis by cellular immune effectors. Transplant Proc. 1987;19:554–556
  143. Clark DA, Chaouat G. Characterization of the cellular basis for the inhibition of cytolytic effector cells by murine placenta. Cell Immunol. 1986;102:43–51
  144. 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
  145. Athanassakis I, Bleackley RC, Paetkau V, Guilbert L, Barr PJ, Wegmann TG. The immunostimulatory effect of T cells and T cell lymphokines on murine fetally derived placental cells. J Immunol. 1987;138:37–44
  146. Armstrong DT, Chaouat G. Effects of lymphokines and immune complexes on murine placental cell growth in vitro. Biol Reprod. 1989;40:466–474
  147. Robertson S, Lavranos T, Seamark RF. In vitro models of the maternal–fetal interface. In:  Wegmann TF,  Gill TJ,  Nisbet-Brown E editor. Molecular and cellular immunobiology of the maternal–fetal interface. New York: Oxford University Press; 1991;p. 191–220
  148. Bartocci A, Pollard JW, Stanley ER. Regulation of colony-stimulating factor 1 during pregnancy. J Exp Med. 1986;164:956–961
  149. Pollard JW, BArtocci A, Areci R, Orlofsky A, Ladner MB, Stanley ER. Apparent role of the macrophage growth factor, CSF-1, in placental development. Nature. 1987;330:484–486
  150. Arceci RJ, Shanahan F, Stanley ER, Pollard JW. Temporal expression and location of colony-stimulating factor 1 (CSF-1) and its receptor in the female reproductive tract are consistent with CSF-1-regulated placental development. Proc Natl Acad Sci USA. 1989;86:8818–8822
  151. Wegmann TG, Athanassakis I, Guilbert L, Branch D, Dy M, Menu E, et al. The role of M-CSF and GM-CSF in fostering placental growth, fetal growth, and fetal survival. Transplant Proc. 1989;21:566–568
  152. Fishman P, Falach-Vaknine E, Zigelman R, Bakimer R, Sredni B, Djaldetti M, et al. Prevention of fetal loss in experimental antiphospholipid syndrome by in vivo administration of recombinant interleukin-3. J Clin Invest. 1993;91:1834–1837
  153. Coutifaris C, Kao LC, Sehdev HM, Chin U, Babalola GO, Blaschuk OW, et al. E-cadherin expression during the differentiation of human trophoblasts. Development. 1991;113:767–777
  154. Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest. 1992;89:210–222
  155. Feinberg RF, Kliman HJ, Lockwood CJ. Is oncofetal fibronectin a trophoblast glue for human implantation?. Am J Pathol. 1991;138:537–543
  156. Dustin ML, Springer TA. Role of lymphocyte adhesion receptors in transient interactions and cell locomotion. Annu Rev Immunol. 1991;9:27–66
  157. Ohlsson R, Glaser A, Holmgren L, Franklin G. The molecular biology of placental development. In:  Redman CW,  Sargent IL,  Starkey PM editor. The human placenta. Oxford: Blackwell Scientific Publications; 1993;p. 33
  158. Choi SJ, Park JY, Lee YK, Choi HI, Lee YS, Koh CM, et al. Effects of cytokines on VEGF expression and secretion by human first trimester trophoblast cell line. Am J Reprod Immunol. 2002;48:70–76
  159. Sridama V, Pacini F, Yang S-L, Moawad A, Reilly M, DeGroot LJ. Decreased levels of helper T cells: a possible cause of immunodeficiency in pregnancy. N Engl J Med. 1982;307(6):352–356
  160. Dodson MG, Kerman RH, Lange CF, Stefani SS, O'Leary JA. T and B cells in pregnancy. Obstet Gynecol. 1977;49(3):299–302
  161. Siegel I, Gleicher N. Changes in peripheral mononuclear cells in pregnancy. Am J Reprod Immunol. 1981;1(3):154–155
  162. Moore MP, Carter NP, Redman CW. Lymphocyte subsets in normal and pre-eclamptic pregnancies. Br J Obstet Gynaecol. 1983;90(4):326–331
  163. Bardeguez AD, McNerney R, Frieri M, Verma UL, Tejani N. Cellular immunity in preeclampsia: alterations in T-lymphocyte subpopulations during early pregnancy. Obstet Gynecol. 1991;77(6):859–862
  164. Coulam CB. T-lymphocyte subsets during pregnancy and the menstrual cycle. Am J Reprod Immunol. 1983;4(2):88–90
  165. Lucivero G, Selvaggi A, Dell'osso A, Antonaci S, Iannone A, Bettocchi S, et al. Mononuclear cell subpopulations during normal pregnancy: I. Analysis of cell surface markers using conventional techniques and monoclonal antibodies. Am J Reprod Immunol. 1983;4(3):142–145
  166. Tallon DF, Corcoran DJD, O'Dwyer EM, Greally JF. Circulating lymphocyte subpopulations in pregnancy: a longitudinal study. J Immunol. 1984;132(4):1784–1787
  167. Gill TJ, Repetti CF. Immunologic and genetic factors influencing reproduction. A review. Am J Pathol. 1979;95(2):465–570
  168. Beer A. Immunology of reproduction. In:  Samter M,  Austen KF,  Claman HN editor. Immunological diseases. Boston: Little, Brown and Co; 1988;p. 329
  169. Gehrz RC, Christianson WR, Linner KM, Conroy MM, McCue SA, Balfour HH. A longitudinal analysis of lymphocyte proliferative responses to mitogens and antigens during human pregnancy. Am J Obstet Gynecol. 1981;140(6):665–670
  170. Petrucco OM, Seamark RF, Holmes K, Forbes IJ, Symons RG, et al. Changes in lymphocyte function during pregnancy. Br J Obstet Gynaecol. 1976;83(3):245–250
  171. Vaquer S, de la Hera A, Jorda J, Martinez C, Escudero M, Alvarez-Mon M. Diminished natural killer activity in pregnancy: modulation by interleukin 2 and interferon gamma. Scand J Immunol. 1987;26(6):691–698
  172. Toder V, Nebel L, Gleicher N. Studies of natural killer cells in pregnancy. I. Analysis at the single cell level. J Clin Lab Immunol. 1984;14(3):123–127
  173. Margoulis GV, Buckley RH, Younger JB. Serum immunoglobulin concentrations during normal pregnancy. Am J Obstet Gynecol. 1971;109:971
  174. Gonik B, Loo LS, West S, Kohl S. Natural killer cell cytotoxicity and antibody-dependent cellular cytotoxicity to herpes simplex virus-infected cells in human pregnancy. Am J Reprod Immunol Microbiol. 1987;13(1):23–26
  175. Kovar IZ, Riches PG. C3 and C4 complement components and acute phase proteins in late pregnancy and parturition. J Clin Pathol. 1988;41(6):650–652
  176. Johnson U, Gustavii B. Complement components in normal pregnancy. Acta Pathol Microbiol Immunol Scand [C]. 1987;95(3):97–99

PII: S1744-165X(06)00045-X

doi: 10.1016/j.siny.2006.04.003

Seminars in Fetal & Neonatal Medicine
Volume 11, Issue 5 , Pages 279-295 , October 2006

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