Macrophages in the Uterus and Placenta

  • J. S. Hunt
  • J. W. Pollard
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 181)


Macrophages are abundant in the mesenchymal and connective tissue stroma of the cycling and pregnant uterus, and constitute a significant proportion of the villous or labyrinthine mesenchymal cells in the human and murid placenta. In other contexts, the activities of these multifunctional cells are strongly influenced by regulatory molecules such as steroid hormones, polypeptide growth factors, and bioactive lipids. All of these are present at particularly high concentrations in the pregnant uterus and placenta. Thus, uterine and placental macrophages stimulated by endogenous factors could contribute to the complex cellular and molecular interactions that result in successful pregnancy.


Human Placenta Decidual Cell Endometrial Stromal Cell Mouse Uterus Uterine Epithelial Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aderem AA, Cohen DS, Wright SD, Cohn ZA (1986) Bacterial lipopolysaccharides prime macrophages for enhanced release of arachadonic acid metabolites. J Exp Med 164: 165–179.PubMedGoogle Scholar
  2. Akira S, Hirano T, Taga T, Kishimoto T (1990) Biology of multifunctional cytokines: IL 6 and related molecules (IL-1 and TNF). FASEB J 4: 2860–2867.PubMedGoogle Scholar
  3. Arceci RJ, Shanahan F, Stanley ER, Pollard JW (1989) The 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 86: 8818–8822.PubMedGoogle Scholar
  4. Assoian RK, Fleurdelys BE, Stevenson HC et al. (1987) Expression and secretion of type β transforming growth factor by activated human macrophages. Proc Natl Acad Sci USA 84: 6020–6024.PubMedGoogle Scholar
  5. Barath P, Fishbein MC, Cao J, Berenson J, Helfant RH, Forrester JS (1990) Tumor necrosis factor gene expression in human vascular intimai smooth muscle cells detected by in situ hybridization. Am J Pathol 137: 503–509.PubMedGoogle Scholar
  6. Bartocci A, Pollard JW, Stanley ER (1986) Regulation of colony-stimulating factor 1 during pregnancy. J Exp Med 164: 956–961.PubMedGoogle Scholar
  7. Beer AE, Billingham RE (1974) Host responses to intra-uterine, tissue, cellular and fetal allografts. J Reprod Fertil [Suppl] 21: 59–88.Google Scholar
  8. Beesley JE, Bomford R, Schmidt JA (1990) Ultrastructural localization of interleukin 1 in human peripheral blood monocytes; evidence for IL-1β in mitochondria. Histochem J 22: 234–244.PubMedGoogle Scholar
  9. Beissert S, Bergholz M, Waase I, Lepsien G, Schauer A, Pfizenmaier K, Kronke M (1989) Regulation of tumor necrosis factor gene expression in colorectal adenocarcinoma: in vivo analysis by in situ hybridization. Proc Natl Acad Sci USA 86: 5064–5068.PubMedGoogle Scholar
  10. Beutler B, Cerami A (1989) The biology of cachectin/TNF—primary mediator of the host response. Annu Rev Immunol 7: 625–655.PubMedGoogle Scholar
  11. Beutler B, Mahoney J, Trang NL, Pekala P, Cerami A (1985) Purification of cachectin, a lipoprotein lipase-suppressing hormone secreted by endotoxin-induced RAW 264.7 cells. J Exp Med 161: 984–995.PubMedGoogle Scholar
  12. Boocock CA, Jones GE, Stanley ER, Pollard JW (1989) Colony-stimulating factor-1 induces rapid behavioural responses in the mouse macrophage cell line, BAC1.2F5. J Cell Sci 93: 447–456.PubMedGoogle Scholar
  13. Branch DR, Turner AR, Guilbert LJ (1989) Synergistic stimulation of macrophage proliferation by the monokines tumor necrosis factor-alpha and colony-stimulating factor 1. Blood 73: 307–311.PubMedGoogle Scholar
  14. Brigstock DR, Heap RP, Brown KD (1989) Polypeptide growth factors in uterine tissues and secretions. J Reprod Fertil 85: 747–758.PubMedGoogle Scholar
  15. Bulmer JN, Johnson PM (1984) Macrophage populations in the human placenta and amniochorion. Clin Exp Immunol 57: 393–403.PubMedGoogle Scholar
  16. Bulmer JN, Johnson PM (1985) Identification of leucocytes within the human chorion laeve. J Reprod Immunol 7: 89–92.PubMedGoogle Scholar
  17. Bulmer JN, Morrison L, Smith JC (1988) Expression of class II MHC gene products by macrophages in human uteroplacental tissue. Immunology 63: 707–714.PubMedGoogle Scholar
  18. Bulmer JN, Smith J, Morrison L, Wells M (1989) Maternal and fetal cellular relationships in the human placental basal plate. Placenta 9: 237–246.Google Scholar
  19. Bulmer JN, Morrison L, Johnson PM, Meager A (1990) Immunohistochemical localization of interferons in human placental tissues in normal, ectopic, and molar pregnancy. Am J Reprod Immunol 22: 109–116.PubMedGoogle Scholar
  20. Casey ML, Cox SM, Beutler B, Milewich L, MacDonald PC (1989) Cachectin/tumor necrosis factor-α formation in human decidua. J Clin Invest 83: 430–436.PubMedGoogle Scholar
  21. Chard T (1989) Interferon in pregnancy. J Dev Physiol 11: 271–276.PubMedGoogle Scholar
  22. Chard T, Craig PH, Menabawey M, Lee C (1986) Alpha interferon in human pregnancy. Br J Obstet Gynaecol 98: 1145–1149.Google Scholar
  23. Chen H-L, Yang Y, Hu X-L, Yelavarthi KK, Fishback JL, Hunt JS (1991) Tumor necrosis factor-alpha mRNA and protein are present in human placental and uterine cells at early and late stages of gestation. Am J Pathol 139: 327–335.PubMedGoogle Scholar
  24. Chouaib S, Welte K, Mertelsmann R, Dupont B (1985) Prostaglandin E2 acts at two distinct pathways of T lymphocyte activation: inhibition of interleukin 2 production and down-regulation of transferrin receptor expression. J Immunol 135: 1172–1179.PubMedGoogle Scholar
  25. Clark DA, Falbo M, Rowley RB, Banwatt D, Stedronska-Clark J (1988) Active suppression of host-vs-graft reaction in pregnant mice. IX. Soluble suppressor activity obtained from allopregnant mouse decidua that blocks the cytolytic effector response to IL-2 is related to transforming growth factor-β. J Immunol 141: 3833–3840.PubMedGoogle Scholar
  26. Crainie M, Guibert L, Wegmann TG (1990) Expression of novel cytokine transcripts in the murine placenta. Biol Reprod 45: 999–1005.Google Scholar
  27. Cunha CR, Chung LWK, Shannon JM, Taguchi O, Fujii IT (1983) Hormone-induced morphogenesis and growth: role of mesenchymal-epithelial interactions. Rec Prog Horm Res 39: 559–598.PubMedGoogle Scholar
  28. Daiter E, Pampfer S. Yeung Y-G, Barad D, Stanley ER, Pollard JW (1992) Expression of colony stimulating factor-1 (CSF-1) in the human uterus and placenta. J Clin Endocrinol Metab 14: 850–858.Google Scholar
  29. Dayer JM, Beutler B, Cerami A (1985) Cachectin/tumor necrosis factor (TNF) stimulates collagenase and PGE2 production by human synovial cells and dermal fibroblasts. J Exp Med 162: 2163–2168.PubMedGoogle Scholar
  30. De M, Wood GW (1990) Influence of oestrogen and progesterone on macrophage distribution in the mouse uterus. J Endocrinol 126: 417–424.PubMedGoogle Scholar
  31. Dijkstra CD, Dopp EA, Joling P, Draal G (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54: 589–599.PubMedGoogle Scholar
  32. Dinarello CA (1988) Biology of interleukin-1. FASEB J 2: 108–115.PubMedGoogle Scholar
  33. Elias JA, Gustilo K, Baeder W, Freundlich B (1987) Synergistic stimulation of fibroblast prostaglandin production by recombinant interleukin 1 and tumor necrosis factor. J Immunol 138: 3812–3816.PubMedGoogle Scholar
  34. Evans DB, Bunning RA, Russell RG (1989) The effects of recombinant human granulocyte-macrophages colony-stimulating factor (rhGM-CSF) on human osteoblast-like cells. Biochem Biophys Res Commun 160: 588–595.PubMedGoogle Scholar
  35. Finn CA, Pope M (1986) Control of leucocyte infiltration into the decidualized mouse uterus. J Endocrinol 110: 93–96.PubMedGoogle Scholar
  36. Flynn A, Finke JH, Hilfiker ML (1982) Placental mononuclear phagocytes as a source of interleukin-1. Science 218: 475–477.PubMedGoogle Scholar
  37. Fowler AK, Reed CD, Giron DJ (1980) Identification of an interferon in murine placentas. Nature 286: 266–267.PubMedGoogle Scholar
  38. Fox H (1978) The development and structure of the placenta. Major Prob Pathol 7: 1–37.Google Scholar
  39. Frolik CA, Dart LL, Meyers CA, Smith DM, Sporn MB (1983) Purification and initial characterization of a type β transforming growth factor from human placenta. Proc Natl Acad Sci USA 80: 3676–3680.PubMedGoogle Scholar
  40. Goldstein J, Braverman M, Salafia C, Buckley P (1988) The phenotype of human placental macrophages and its variation with gestational age. Am J Pathol 133: 648–659.PubMedGoogle Scholar
  41. Hamilton JA, Stanley ER, Burgess AW, Shadduck RK (1980) Stimulation of macrophage plasminogen activator by colony stimulating factors. J Cell Physiol 103: 435–445.PubMedGoogle Scholar
  42. Hancock RJ, Faruki S (1986) Assessment of immune responses to H-Y antigen in naturally inseminated and sperm-injected mice using cell-mediated cytotoxicity assays. J Reprod Immunol 9: 187–194.PubMedGoogle Scholar
  43. Haskill S, Johnson C, Eierman D, Becker S, Warren K (1988) Adherence induces selective mRNA expression of monocyte mediators and proto-oncogenes. J Immunol 140: 1690–1694.PubMedGoogle Scholar
  44. Head JR, Gaede SD (1986) la antigen expression in the rat uterus. J Reprod Immunol 9: 137–141.PubMedGoogle Scholar
  45. Heine UI, Munoz EF, Flanders KC et al. (1987) Role of transforming growth factor-β in the development of the mouse embryo. J Cell Biol 105: 2861–2876.PubMedGoogle Scholar
  46. Hill DJ (1989) Growth factors and their cellular actions. J Reprod Fertil 85: 723–734.PubMedGoogle Scholar
  47. Hu X-L, Yang Y, Hunt JS (1992) Differential distribution of interleukin-1α and interleukin-1β proteins in human placentas. J Reprod Immunol (in press).Google Scholar
  48. Hume DA, Robinson AP, McPherson GG, Gordon S (1983) The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80. J Exp Med 158: 1522–1536.PubMedGoogle Scholar
  49. Hunt JS (1989a) Cytokine networks in the uteroplacental unit: macrophages as pivotal regulatory cells. J Reprod Immunol 16: 1–17.PubMedGoogle Scholar
  50. Hunt JS (1989b) Macrophages in human uteroplacental tissues. Am J Reprod Immunol 21: 119–122.PubMedGoogle Scholar
  51. Hunt JS (1990) Current topic: the role of macrophages in the uterine response to pregnancy. Placenta 11: 467–475.PubMedGoogle Scholar
  52. Hunt JS (1991) Prostaglandins, immunoregulation, and macrophage function. In: Coulam C, Mclntyre JA, Faulk WP (eds) Immunologic obstetrics. W.W. Norton, New York (in press).Google Scholar
  53. Hunt JS, King CR Jr, Wood GW (1984a) Evaluation of human chorionic trophoblasts and placental macrophages as stimulators of maternal lymphocyte proliferation in vitro. J Reprod Immunol 6: 377–391.PubMedGoogle Scholar
  54. Hunt JS, Manning LS, Wood GW (1984b) Macrophages in murine uterus are immunosuppressive. Cell Immunol 85: 499–510.PubMedGoogle Scholar
  55. Hunt JS, Manning LS, Mitchell D, Selanders JR, Wood GW (1985) Localization and characterization of macrophages in murine uterus. J Leukocyte Biol 38: 255–265.PubMedGoogle Scholar
  56. Hunt JS, Soares MJ, Lei M-G, Smith RN, Wheaton D, Atherton RA, Morrison DC (1989) Products of lipopolysaccharide-activated macrophages (tumor necrosis factor-α, transforming growth factor-β) but not lipopolysaccharide modify DNA synthesis by rat trophoblast cells exhibiting the 80 kDa lipolysaccharide-binding protein. J Immunol 143: 1606–1613.PubMedGoogle Scholar
  57. Hunt JS, Atherton RA, Pace JL (1990) Differential responses of rat trophoblast cells and embryonic fibroblasts to cytokines that regulate proliferation and class IMHC antigen expression. J Immunol 145: 184–189.PubMedGoogle Scholar
  58. Jaattela M, Kuusela P, Saksela E (1988) Demonstration of tumor necrosis factor in human amniotic fluids and supernatants of placental and decidual tissues. Lab Invest 58: 48–52.PubMedGoogle Scholar
  59. Kabawat SE, Mostoufi-Zadeh M, Driscoll SG, Bhan AK (1985) Implantation site in normal pregnancy. Am J Pathol 118: 76–84.PubMedGoogle Scholar
  60. Kameda T, Matsuzaki N, Sawai K et al. (1990) Production of interleukin-6 by normal human trophoblast. Placenta 11: 205–213.PubMedGoogle Scholar
  61. Kato K, Yokoi T, Takano N, Kanegane H, Yachie A, Miyawaki T, Taniguchi N (1990) Detection by in situ hybridization and phenotypic characterization of cells expressing IL-6 mRNA in human stimulated blood. J Immunol 144: 1317–1322.PubMedGoogle Scholar
  62. Kaushansky K, Broudy VC, Harlan JM, Adamson JW (1988) Tumour necrosis factor-α and tumour necrosis factor-β (lymphotoxin) stimulate the production of granulocyte-macrophage colony-stimulating factor, macrophage colony stimulating factor, and IL-1 in vivo. J Immunol 141: 3410–3415.PubMedGoogle Scholar
  63. Keshav S, Lawson L, Chung LP, Stein M, Perry VH, Gordon S (1990) Tumour necrosis factor mRNA localized to Paneth cells of normal murine intestinal epithelium by in situ hybridization. J Exp Med 171: 327–332.PubMedGoogle Scholar
  64. Khong TY (1987) Immunohistologic study of the leukocytic infiltrate in maternal uterine tissues in normal and preeclamptic pregnancies at term. Am J Reprod Immunol 15: 1–8.Google Scholar
  65. King A, Wellings V, Gardner L, Loke YW (1989) Immunocytochemical characterization of the unusual large granular lymphocytes in human endometrium throughout the menstrual cycle. Hum Immunol 24: 195–205.PubMedGoogle Scholar
  66. Klein JO, Remington JS (1990) Current concepts of infections of the fetus and newborn infant. In: Remington JS, Klein JO (eds) Infectious diseases of the fetus and newborn infant, W.B. Saunders, Philadelphia.Google Scholar
  67. Kojima S, Tadenuma H, Inada Y, Saito Y (1989) Enhancement of plasminogen activator activity in cultured endothelial cells by granulocyte colony-stimulating factor. J Cell Physiol 138: 192–196.PubMedGoogle Scholar
  68. Laguens G, Goni JM Jr, Laguens M, Goni JM, Laguens R (1990) Demonstration and characterization of HLA-DR positive cells in the stroma of human endometrium. J Reprod Immunol 18: 179–186.PubMedGoogle Scholar
  69. Lala PK, Kennedy TG, Parhar RS (1988) Suppression of lymphocyte alloreactivity by early gestational human decidua. II. Characterization of the suppressor mechanisms. Cell Immunol 116: 411–422.PubMedGoogle Scholar
  70. Lande IJ (1986) Systemic immunity developing from intrauterine antigen exposure in the nonpregnant rat. J Reprod Immunol 9: 57–66.PubMedGoogle Scholar
  71. Le J, Vilcek J (1987) Biology of disease. Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities. Lab Invest 56: 234–248.PubMedGoogle Scholar
  72. Lessin DL, Hunt JS, King CR Jr, Wood GW (1988) Antigen expression by cells near the maternal-fetal interface. Am J Reprod Immunol Microbiol 16: 1–7.PubMedGoogle Scholar
  73. Lewis SH, Reynolds-Kohler C, Fox HE, Nelson JA (1990) HIV-1 in trophoblastic and villous Hofbauer cells and haematological precursors in eight-week fetuses. Lancet 335: 565–568.PubMedGoogle Scholar
  74. Loke YW, Eremin O, Ashby J, Day S (1982) Characterization of the phagocytic cells isolated from the human placenta. J Reticuloendothel Soc 31: 317–324.PubMedGoogle Scholar
  75. Main EK, Strizki J, Schochet P (1987) Placental production of immunoregulatory factors: trophoblast is a source of interleukin-1. Trophoblast Res 2: 149–160.Google Scholar
  76. Martin L, Finn CA, Trinder G (1973) DNA synthesis in the endometrium of progesterone treated mice. J Endocrinol 56: 303–307.PubMedGoogle Scholar
  77. Matthews CJ, Searle RF (1987) The role of prostaglandins in the immunosuppressive effects of supernatants from adherent cells of murine decidual tissue. J Reprod Immunol 12: 109–124.PubMedGoogle Scholar
  78. Matthews CJ, Adams AM, Searle RF (1985) Detection of macrophages and the characterization of Fc receptor bearing cells in the mouse decidua, placenta and yolk sac using the macrophage-specific monoclonal antibody F4/80. J Reprod Immunol 7: 315–323.PubMedGoogle Scholar
  79. McGregor JA, French JI, Lawellin D, Todd JK (1988) Preterm birth and infection: pathogenic possibilities. Am J Reprod Immunol Microbiol 16: 123–132.PubMedGoogle Scholar
  80. Meagher R, Amsden A, Hunt J, Soares M, Sogor L, Smith RN (1990) Placental CSF-like activity. Exp Hematol 18: 448–451.PubMedGoogle Scholar
  81. Ming WJ, Bersani L, Mantovani A (1987) Tumour necrosis factor-alpha is chemotactic for monocytes and polymorphonuclear leukocytes. J Immunol 138: 1469–1474.PubMedGoogle Scholar
  82. Moskalewski S, Ptak W, Strzyzewska J (1974) Macrophages in mouse placenta. I. Morphological and functional identification. J Reticuloendothel Soc 16: 9–14.PubMedGoogle Scholar
  83. Moskalewski S, Ptak W, Czarnik Z (1975) Demonstration of cells with IgG receptor in human placenta. Biol Neonate 26: 268–272.PubMedGoogle Scholar
  84. Motro B, Ahuva I, Sachs L, Keshet E (1990) Pattern of interleukin-6 gene expression in vivo suggests a role for this cytokine in angiogenesis. Proc Natl Acad Sci USA 87: 3092–3096.PubMedGoogle Scholar
  85. Mues B, Langer D, Zwadlo G, Sorg C (1989) Phenotypic characterization of macrophages in human term placenta. Immunology 67: 303–307.PubMedGoogle Scholar
  86. Muller R, Slamon DJ, Adamson ED, Tremblay JM, Muller D, Cline MJ, Verma IM (1983) Transcription of c-onc genes c-ras Ki and c-fms during mouse development. Mol Cell Biol 3: 1062–1069.PubMedGoogle Scholar
  87. Nash AD, Uren S, Hawes CS, Boyle W (1989) Application of a novel immunization protocol to the production of monoclonal antibodies specific for macrophages in human placenta. Immunology 68: 332–340.PubMedGoogle Scholar
  88. Nathan CF (1987) Secretory products of macrophages. J Clin Invest 79: 319–326.PubMedGoogle Scholar
  89. Nelson BJ, Ralph P, Green SJ, Nacy CA (1991) Differential susceptibility of activated macrophage cytotoxic effector reactions to the suppressive effects of transforming growth factor-β1. J Immunol 146: 1849–1857.PubMedGoogle Scholar
  90. Nicol T (1935) The female reproductive system in the guinea pig: intravitam staining; fat production; influence of hormones. Trans R Soc Edinb 58: 449–483.Google Scholar
  91. Okazaki T, Casey ML, Okita JR, MacDonald PC, Johnston JM (1981) Initiation of human parturition. XII. Biosynthesis and metabolism of prostaglandins in human fetal membranes and uterine decidua. Am J Obstet Gynecol 139: 373–381.PubMedGoogle Scholar
  92. Oksenberg JR, Mor-Yosef S, Ezra Y, Brautbar C (1988) Antigen presenting cells in human decidual tissue: III. Role of accessory cells in activation of suppressor cells. Am J Reprod Immunol Microbiol 16: 151–158.PubMedGoogle Scholar
  93. Parhar RS, Kennedy TG, Lala PK (1988) Suppression of lymphocyte alloreactivity by early gestational human decidua. I. Characterization of suppressor molecules. Cell Immunol 116: 392–410.PubMedGoogle Scholar
  94. Parr EL, Young LHY, Parr MB, Young JD-E (1990) Granulated metrial gland cells of pregnant mouse uterus are natural killer-like cells that contain perforin and serine esterases. J Immunol 145: 2365–2372.PubMedGoogle Scholar
  95. Pollard JW (1990) 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 88: 721–731.PubMedGoogle Scholar
  96. Pollard JW, Bartocci A, Arceci R, Orlofsky A, Ladner MB, Stanley ER (1987) Apparent role of the macrophage growth factor, CSF-1, in placental development. Nature 330: 484–487.PubMedGoogle Scholar
  97. Pollard JW, Hunt JS, Wiktor-Jedrzejczak W, Stanley ER (1991a) A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev Biol 148: 273–283.PubMedGoogle Scholar
  98. Pollard JW, Pampfer S, Daiter E, Barad D, Areci RJ (1991b) Colony stimulating factor-1 in the mouse and human uteroplacental unit. In: Schonberg DW (ed) Growth factors in reproduction. Plenum, New York, p 219–229.Google Scholar
  99. Rambaldi A, Young DC, Griffin JD (1987) Expression of the M-CSF (CSF-1) gene by human monocytes. Blood 69: 1409–1413.PubMedGoogle Scholar
  100. Redline RW, Lu CY (1988) Specific defects in the anti-listerial immune response in discrete regions of the murine uterus and placenta account for susceptibility to infection. J Immunol 140: 3947–3955.PubMedGoogle Scholar
  101. Redline RW, Lu CY (1989) Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta. Lab Invest 61: 27–36.PubMedGoogle Scholar
  102. Redline RW, McKay DB, Vazquez MA, Papaioannou VE, Lu CY (1990) Macrophage functions are regulated by the substratum of murine decidual stromal cells. J Clin Invest 85: 1951–1958.PubMedGoogle Scholar
  103. Regenstreif LJ, Rossant J (1989) Expression of the c-fms proto-oncogene and of the cytokine, CSF-1 during mouse embryogenesis. Dev Biol 133: 284–294.PubMedGoogle Scholar
  104. Renz H, Gong J-H, Schmidt A, Nain M, Gemsa D (1988) Release of tumor necrosis factor-α from macrophages. Enhancement and suppression are dose-dependently regulated by prosta-glandin E2 and cyclic nucleotides. J Immunol 141: 2388–2393.PubMedGoogle Scholar
  105. Rizzino A (1988) Transforming growth factor-β: multiple effects on cell differentiation and extracellular matrices. Dev Biol 130: 411–422.PubMedGoogle Scholar
  106. Robbins DS, Shirazi Y, Drysdale BE, Leiberman A, Shin HS, Shin ML (1987) Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes. J Immunol 139: 2593–2597.PubMedGoogle Scholar
  107. Robertson SA, Seamark RF (1990) Granulocyte macrophage colony stimulating factor (GM-CSF) in the murine reproductive tract: stimulation by seminal factors. Reprod Fertil Dev 2: 359–368.PubMedGoogle Scholar
  108. Romero R, Emamian M, Wan M, Quintero R, Hobbins JC, Mitchell M (1987) Prostaglandin concentrations in amniotic fluid of women with intra-amniotic infections and preterm labor. Am J Obstet Gynecol 157: 1461–1467.PubMedGoogle Scholar
  109. Romero R, Brody DT, Oyarzun E, Mazor M, Wu YK, Hobbins JC, Durum SK (1989a) Infection and labor. III. lnterleukin-1: a signal for the onset of parturition. Am J Obstet Gynecol 160: 1117–1123.PubMedGoogle Scholar
  110. Romero R, Manogue KR, Mitchell MD, Wu YK, Oyarzun E, Hobbins JC, Cerami A (1989b) Infection and labor. IV. Cachectin-tumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am J Obstet Gynecol 161: 336–341.PubMedGoogle Scholar
  111. Romero R, Avila C, Santhanam U, Sehgal PB (1990) Amniotic fluid and interleukin-6 in preterm labor: association with infection. J Clin Invest 85: 1392–1400.PubMedGoogle Scholar
  112. Russell SW, Pace JL (1987) The effects of interferons on macrophages and their precursors. Vet Immunol Immunopathol 15: 129–165.PubMedGoogle Scholar
  113. Simmen FA, Simmen RC (1991) Peptide growth factors and proto-oncogenes in mammalian conceptus development. Biol Reprod 44: 1–5.PubMedGoogle Scholar
  114. Sminia T, Jeurissen SHM (1986) The macrophage population of the gastro-intestinal tract of the rat. Immunobiology 172: 72–80.PubMedGoogle Scholar
  115. Sokol S, Wong GG, Melton DA (1990) A mouse macrophage factor induces head structures and organizes a body axis in Xenopus. Science 249: 561–564.PubMedGoogle Scholar
  116. Sporn MB, Roberts AB (1989) Transforming growth factor-β. Multiple actions and potential clinical applications. JAMA 262: 938–941.PubMedGoogle Scholar
  117. Starkey PM, Turley I, Gordon S (1987) The mouse macrophage-specific glycoprotein defined by monoclonal antibody F4/80: characterization, biosynthesis and demonstration of a rat analogue. Immunology 60: 117–122.PubMedGoogle Scholar
  118. Sugarman BJ, Aggarwal BB, Hass PE, Figari IS, Palladino MA, Shepard HM (1985) Recombinant human tumor necrosis factor-α: effects on proliferation of normal and transformed cells in vitro. Science 230: 943–945.PubMedGoogle Scholar
  119. Tabibzadeh SS (1990) Proliferative activity of lymphoid cells in human endometrium throughout the menstrual cycle. J Clin Endocrinol Metabol 70: 437–443.Google Scholar
  120. Tabibzadeh SS, Santhanam U, Sehgal PB, May LT (1988) Cytokine-induced production of IFN-β/IL-6 by freshly explanted human endometrial stromal cells. J Immunol 142: 3134–3139.Google Scholar
  121. Tachi C, Tachi S (1989) Role of macrophages in the maternal recognition of pregnancy. J Reprod Fertil [Supp] 37: 63–68.Google Scholar
  122. Tachi C, Tachi S, Knyszynski A, Linder HR (1981) Possible involvement of macrophages in embryo-maternal relationships during ovum implantation in the rat. J Exp Zool 217: 81–92.PubMedGoogle Scholar
  123. Takacs L, Kovacs EJ, Smith MR, Young HA, Durum SK (1988) Detection of IL-1α and IL-1β gene expression by in situ hybridization. J Immunol 141: 3081–3095.PubMedGoogle Scholar
  124. Tamada H, McMaster MT, Flanders KC, Andrews GK, Dey SK (1990) Cell type-specific expression of TGF-β1 in the mouse uterus during the periimplantation period. Mol Endocrinol 4: 965–972.PubMedGoogle Scholar
  125. Tamatani T, Tsunoda H, Iwasaki H, Kaneko M, Hashimoto T, Onozaki K (1988) Existence of both IL-1α and β in normal amniotic fluid: unique high molecular weight form of IL-1β. Immunology 65: 337–342.PubMedGoogle Scholar
  126. Taniguchi T (1988) Regulation of cytokine gene expression. Annu Rev Immunol 6: 439–464.PubMedGoogle Scholar
  127. Tawfik OW, Hunt JS, Wood GW (1986a) Implication of prostaglandin E2 in soluble factor-mediated immune suppression by murine decidual cells. Am J Reprod Immunol Microbiol 12: 111–117.PubMedGoogle Scholar
  128. Tawfik OW, Hunt JS, Wood GW (1986b) Partial characterization of uterine cells responsible for suppression of murine maternal anti-fetal immune responses. J Reprod Immunol 9: 213–224.PubMedGoogle Scholar
  129. Toth FD, Juhl C, Norskov-Lauritsen N, Mosborg-Petersen P, Ebbesen P (1990) Interferon production by cultured human trophoblasts induced with double stranded polyribonucleotide. J Reprod Immunol 17: 217–227.PubMedGoogle Scholar
  130. Tushinski RJ, Oliver IT, Guilbert LJ, Tynan PW, Warner JR, Stanley ER (1982) Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell 28: 71–81.PubMedGoogle Scholar
  131. Ulich TR, Guo K, del Castillo J (1989) Endotoxin-induced cytokine gene expression in vivo. Am J Pathol 134: 11–14.PubMedGoogle Scholar
  132. Umeda T, Hara T, Niijima T (1983) Cytotoxic effect of tumor necrosis factor on human lymphocytes and specific binding of the factor to the target cells. Cell Mol Biol 29: 349–352.PubMedGoogle Scholar
  133. Uzumaki H, Okabe T, Sasaki N et al. (1989) Identification and characterization of receptors for granulocyte colony-stimulating factor on human placenta and trophoblastic cells. Proc Natl Acad Sci USA 86: 9323–9326.PubMedGoogle Scholar
  134. Van Damme J, Van Beeumen J, Decock B, Van Snick J, De Ley M, Billiau F (1988) Separation and comparison of two monokines with LAF activity (interleukin-1β and hybridoma growth factor): identification of leukocyte-derived HGF as interleukin-6. J Immunol 140: 1534–1541.PubMedGoogle Scholar
  135. Van Rood JJ, Eernisse JG, Van Leeuwen A (1958) Leucocyte antibodies in sera from pregnant women. Nature 181: 1735–1736.Google Scholar
  136. Van Snick J (1990) Interleukin-6: an overview. Annu Rev Immunol 8: 253–278.PubMedGoogle Scholar
  137. Wahl SM, Hunt DA, Wakefield LM, McCartney-Francis N, Wahl LM, Roberts AB, Sporn MR (1987) Transforming growth factor type β induces monocyte chemotaxis and growth factor production. Proc Natl Acad Sci USA 84: 5788–5792.PubMedGoogle Scholar
  138. Wahl SM, Hunt DA, Wong HL et al. (1988) Transforming growth factor-β is a potent immunosup-pressive agent that inhibits IL-1-dependent lymphocyte proliferation. J Immunol 140: 3026–3032.PubMedGoogle Scholar
  139. Wahl SM, McCartney-Francis N, Mergenhagen SE (1989) Inflammatory and immunomodulatory roles of TGF-β. Immunol Today 10: 258–261.PubMedGoogle Scholar
  140. Wang JM, Colella S, Allavena P, Mantovani A (1987) Chemotactic activity of human recombinant granulocyte-macrophage colony stimulating factor. Immunology 60: 439–444.PubMedGoogle Scholar
  141. Wang JM, Griffin JD, Rambaldi A, Chen ZG, Mantovani A (1988) Induction of monocyte migration by recombinant macrophage colony-stimulating factor. J Immunol 141: 575–579.PubMedGoogle Scholar
  142. Wiktor-Jedrzejczak W, Ahmed A, Szczylik C, Skelly RR (1982) Hematological characterization of congenital osteopetrosis in op/op mouse. J Exp Med 156: 1516–1527.PubMedGoogle Scholar
  143. Wiktor-Jedrzejczak W, Bartocci A, Fermate AW, Ahmed-Ansari A, Snell KW, Pollard JW, Stanley ER (1990) Total absence of colony stimulating factor-1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci USA 87: 4828–4832.PubMedGoogle Scholar
  144. Wiktor-Jedrzejczak W, Urbanowska E, Aukerman SL et al. (1991) Correction by CSF-1 of defects in the osteopetrotic op/op mouse suggest local, developmental and humoral requirements for this growth factor. Exp Hematol 19: 1049–1054.PubMedGoogle Scholar
  145. Wood GW (1980) Immunohistological identification of macrophages in murine placentae, yolk sac membranes and pregnant uteri. Placenta 1: 309–318.PubMedGoogle Scholar
  146. Wood GW, King CR Jr (1982) Trapping antigen-antibody complexes within the human placenta. Cell Immunol 69: 347–362.PubMedGoogle Scholar
  147. Wood GW, Reynard J, Krishnan E, Racela L (1978) Immunobiology of the human placenta. II. Localization of macrophages, in vivo bound IgG and C3. Cell Immunol 35: 205–216.PubMedGoogle Scholar
  148. Yang CP, De Pinho SG, Greenberger LM, Arceci RJ, Horwitz SB (1989) Progesterone interacts with P-glycoprotein in multidrug-resistant cells and in the endometrium of gravid uterus. J Biol Chem 264: 782–788.PubMedGoogle Scholar
  149. Yelavarthi KK, Chen H-L, Yang Y, Cowley BD, Fishback JL, Hunt JS (1991) Tumor necrosis factor-alpha mRNA and protein in rat uterine and placental cells. J Immunol 146: 3840–3848.PubMedGoogle Scholar
  150. Yoshida H, Hayashi S-I, Kunisada T et al. (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345: 442–444.PubMedGoogle Scholar
  151. Zheng Y, Zhou Z-Z, Lyttle CR, Teuscher C (1988) Immunohistochemical characterization of the esterogen-stimulated leukocyte influx in the immature rat uterus. J Leukocyte Biol 44: 27–32.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1992

Authors and Affiliations

  • J. S. Hunt
    • 1
  • J. W. Pollard
    • 2
  1. 1.Department of Pathology and OncologyUniversity of Kansas Medical CenterKansas City, KansasUSA
  2. 2.Department of Developmental Biology and Cancer and Department of Obstetrics and GynecologyAlbert Einstein College of MedicineBronx, New YorkUSA

Personalised recommendations