Advertisement

Estrogen-Mediated Immunomodulation

  • Oscar J. Pung
  • Anne N. Tucker
  • Michael I. Luster

Abstract

Early anatomic observations demonstrating that ovariectomy enhanced thymic weights while thymectomy modulated uterine weight provided an impetus for numerous studies which established a relationship between sex hormones and the immune system (see rev. by Ahlquist, 1976; Kalland, 1982; Luster et al., 1985). These studies suggested that pharmacological and to some extent physiological levels of estrogens, as well as inadvertent exposure to estrogenic compounds in the environment, may modulate immune function. Consistent with the immunological alterations, clinical and laboratory studies demonstrated that altered estrogen levels can modulate host resistance to a variety of infectious agents. Illustrative of this are the findings that estrogens precipitate a dramatic increase in Listeria monocytogenes susceptibility (Dean et al., 1980; Pung et al., 1984), impair the intestinal expulsion of adult nematode Trichinella spiralis (Dean et al., 1980; Luebke et al., 1984) and increase the susceptibility of mice to both transplantable and methylcholanthreneinduced tumors (Dean et al., 1980; Morahan et al., 1984; Kalland and Forsberg, 1981). Estradiol has also been shown to induce more intense chlamydial (Rank et al., 1982) and staphylococcal (Toivanen, 1967) infections. Pharmacological doses of diethylstilbestrol (DES), a nonsteroidal synthetic estrogen, or 176-estradiol increase the severity of experimental toxoplasmosis in mice (Pung and Luster, submitted). In other instances, estrogen treated mice are less susceptible to bacterial infection, examples being Pneumococcus Type I, Pasteurella spp. and Salmonella spp. (Nicol et al., 1964). Rodents exposed to DES are also less susceptible to the formation of transplantable lung melanoma tumors (Fugmann et al., 1983) as well as to certain plasmodial, babesial and trypanosomal infections (Cottrell et al., 1977; Kierszenbaum et al., 1974; Mankau, 1975).

Keywords

Estrogen Receptor Natural Killer Cell Activity Thymic Epithelial Cell Estramustine Phosphate Thymic Weight 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ablin, R.J., Bhatti, R.A., Guinan, P.D., and Khin, W., 1979, Modulatory effects of oestrogen on immunological responsiveness. Clin. Explt. Immunol. 38:83–91.Google Scholar
  2. Ahlquist, J., 1976, Endocrine influences on lymphatic organs, immune responses, inflammation and autoimmunity. Acta Endologica. (Supp. 206 ), 83: 1–136.Google Scholar
  3. Allen, L.S., McClure, J.E., Goldstein, A.L., Barkley, M.S., and Michael, S.D., 1984, Estrogen and thymic hormone interactions in the female mouse. J. Reprod. Immunol. 6:25–37.Google Scholar
  4. Barnes, E.W., Loudon, N.B., MacCuish, A.C., Jordan, J., and Irvine, W.J., 1974, Phytohaemagglutinin-induced lymphocyte transformation and circulating autoantibodies in women taking oral contraceptives. Lancet May 11, 898–900.Google Scholar
  5. Batchelor, J.R., 1968, Hormonal control of antibody formation, in “Regulation of the Antibody Response”, B. Cinader, ed., pp.776–295, Thomas, Springfield.Google Scholar
  6. Batra, S., and Sjogren, C., 1983, Effect of estrogen treatment on calcium uptake by the rat uterine smooth muscle. Life Sci. 32: 315–319.Google Scholar
  7. Besedovsky, H.O., and Sorkin, E., 1974, Thymus involvement in female sexual maturation. Nature 249: 356–358.Google Scholar
  8. Bick, P.H., Tucker, A.N., White, K.L., Jr., and Holsapple, M., 1984, Effects of subchronic exposure to diethylstilbestrol on humoral immune functions in female B6C3F1 mice. Immunopharmacology 7: 27–39.Google Scholar
  9. Bodel, P., Dillard, G.M., Kaplan, S.S., and Malawista, S.E., 1972, Antiinflammatory effects of estradiol on human blood leukocytes. J. Lab. Clin. Med. 80:373–384.Google Scholar
  10. Bole, G.G., Friedlaeuder, M.H., and Smith, C.K., 1969, Rheumatic symptoms and serological abnormalities induced by oral contraceptives. Lancet 1: 323–326.Google Scholar
  11. Bompiani, G., 1914, Der einfluss der sangens auf die restitutions - fahigheit des thymus nach der schwangerschaft. Zbl. Allg. Pathol. u. pathol. Anat. 25:929–935.Google Scholar
  12. Boorman, G.A., Luster, M.I., Dean, J.H., and Wilson, R.E., 1980, The effect of adult exposure to diethylstilbestrol in the mouse on macrophage function and numbers. J. Reticuloendothel. Soc. 28:547–559.Google Scholar
  13. Calandra, R.S., Naess, 0., Purvis, K., Attramadal, A., Djoseland, 0., and Hansson, V., 1978, Oestrogen receptors in the rat adrenal gland. J. Steroid Biochem. 9: 957–962.CrossRefGoogle Scholar
  14. Carter, J., 1976, The effect of progesterone, oestradiol and HCG on cell-mediated immunity in pregnant mice. J. Reprod. Fert. 46:211–216.Google Scholar
  15. Carter, S.B., 1956, The influence of sex hormones on the weight of the adrenal gland in the rat. J. Endocrin. 13:150–160.Google Scholar
  16. Chiodi, H., 1940, The relationship between the thymus and the sexual organs. Endocrinology 26: 107–116.Google Scholar
  17. Cohen, J.H.M., Danel, L., Cordier, G., Saly, S., and Revillard, J.P., 1983, Sex steroid receptors in peripheral T cells: absence of androgen receptors and restriction of estrogen receptors to OKT8-positive cells. J. Immunol. 131:2767–2771.Google Scholar
  18. Colby, H.D., and Kitay, J.I., 1974, Interaction of estradiol and ACTH in the regulation of adrenal corticosterone production in the rat. Steroids 24: 527–536.Google Scholar
  19. Cottrell, B.J., Playfair, J.H.L., and de Sousa, B., 1977, Plasmodium yoelii and Plasmodium vinckei: the effects of nonspecific immunostimulation on murine maleria. Exp. Parasitol. 43:45–53.Google Scholar
  20. Cupps, T.R., and Fauci, A.S., 1982, Corticosteroid-mediated immunoregulation in man. Immunol. Rev. 65:133–155.Google Scholar
  21. Cutler, B.S., Forbes, A.P., Ingersoll, F.M., and Scully, R.E., 1972, Endometrial carcinoma after stilbestrol therapy in gonadal dysgenesis. N. Engl. J. Med. 287:628–631.Google Scholar
  22. Dean, J.H., Boorman, G.A., Luster, M.I., Adkins, B., Lauer, L.D., and Adams, D.O., 1984, Effect of agents of environmental concern on macrophage function, in “Mononuclear Phagocyte Biology”, A. Volkman, ed., pp. 473–485, Marcell Dekker, Inc.Google Scholar
  23. Dean, J.H., Luster, M.I., Boorman, G.A., Luebke, R.W., and Lauer, L.D., 1980, The effect of adult exposure to diethylstilbestrol in the mouse: alterations in tumor susceptibility and host resistance parameters. J. Reticuloendothel. Soc. 28:571–583.Google Scholar
  24. Den Dulk, M.M.C.D., Crofton, R.W., and Van Furth, R., 1979, Origin and kinetics of Kupffer cells during an acute inflammatory response. Immunology 37: 7–18.Google Scholar
  25. Eroshenko, V.P., and Palmiter, R.D., 1980, Estrogenicity of kepone in birds and mammals, in “Estrogens in the Environment”, J.A. McLachlan, ed., pp. 305–325, Elsevier North Holland, New York.Google Scholar
  26. Fishman, J., and Martucci, C., 1980, Dissociation of biological activities in metabolites of estradiol, in “Estrogens in the Environment”, J.A. McLachlan, ed., pp. 131–145, Elsevier/North-Holland, New York.Google Scholar
  27. Fluhmann, C.F., 1932, The influence of sex hormones on the reticuloendothelial cells of the uterus and a possible application to the treatment of pelvic inflammatory conditions. Am. J. Obstet. Gynecol. 24:654–655.Google Scholar
  28. Franks, C.R., Perkins, F.T., and Bishop, D., 1975, The effect of sex hormones on the growth of Hela tumor nodules in male and female mice. Brit. J. Cancer 31:100–110.Google Scholar
  29. Fried, W., Tichlee, T., Dennenberg, I., Bacone, J., and Wang, F., 1974, Effects of estrogens on hematopoietic stem cells and on hematopoiesis of mice. J. Lab. Clin. Med. 83:807–815.Google Scholar
  30. Fruhman, G.J., 1973, Peritoneal macrophages in male and female mice. J. Reticuloendothel. Soc. 14:371–379.Google Scholar
  31. Fugmann, F.A., Aranyi, C., Barbera, P.W., Bradof, J.N., Gibbons, R.D., and Fenterro, J.D., 1983, The effect of diethylstilbestrol as measured by host resistance and tumor susceptibility assays in mice. J. Toxicol. Environ. Health 11:827–841.Google Scholar
  32. Gorlich, M., Hecker, D., and Heise, E., 1981, Comparison of estradiol receptor investigations and histochemical investigations on enzymes in human mammary cancers. J. Natl. Cancer Inst. 67:521–527.Google Scholar
  33. Grossman, C.J., Sholiton, L.J., and Nathan, P., 1979a, Rat thymic estrogen receptor. I. Preparation, location and physiochemical properties. J. Steroid Biochem. 11:1233–1240.Google Scholar
  34. Grossman, C.J., Sholiton, L.J., Blaha, G.C., and Nathan, P., 1979b, Rat thymic estrogen receptor. H. Physiological properties. J. Steroid Biochem. 11:1241–1246.Google Scholar
  35. Grossman, C.J., Sholiton, L.J., and Rosselle, G.A., 1982, Estradiol regulation of thymic lymphocyte function in the rat: mediation by serum thymc factors. J. Steroid Biochem. 16:683–690.Google Scholar
  36. Grundbacher, F.J., 1972, Human X chromosome carries quantitative genes for immunoglobulin M. Science 176: 311–312.Google Scholar
  37. Henriksen, O., and Frey, J.R., 1982, Control of expression of interleukin-2 activity. Cell. Immunol. 73:106–114.Google Scholar
  38. Herbst, A.L., Ulfelder, H., and Poskanzer, D.C., 1971, Adenocarcinoma of the vagina. Association of maternal stilboestrol therapy with tumor appearance in young women. N. Engl. J. Med. 284:878–881.Google Scholar
  39. Heslop, R.W., Krohn, P.L., and Sparrow, E.M., 1954, The effect of pregnancy on the survival of skin homografts in rabbits. J. Endocrin. 10: 325–332.CrossRefGoogle Scholar
  40. Inman, R.D., 1978, Immunologic sex differences and the female predominance in systemic lupus erythematosus. Arthritis Rheum. 21: 849–852.Google Scholar
  41. Jolly, J., and Lieure, C., 1930, Influence de la-gestation sur le thymus. C.R. Soc. Biol. 104:451–454.Google Scholar
  42. Kalland, T., 1980a, Decreased and disproportionate T-cell population in adult mice after neonatal exposure to diethylstilbestrol. Cell. Immunol. 51:55–63.Google Scholar
  43. Kalland, T., 1980b, Reduced natural killer cell activity in female mice after neonatal exposure to diethylstilbestrol. J. Immunol. 124:1297–1321.Google Scholar
  44. Kalland, T., 1982, Long-term effects on the immune system of an early life exposure to diethylstilbestrol, in “Environmental Factors in Human Growth and Development”, Banbury Report 11, pp. 217–242.Google Scholar
  45. Kalland, T., and Forsberg, J.G., 1978, Delayed hypersensitivity response to oxazolone in neonatally estrogenized mice. Cancer Lett. 4:141–146.Google Scholar
  46. Kalland, T., and Forsberg, J.G., 1981, Natural killer cell activity and tumor susceptibility in female mice treated neonatally with diethylstilbestrol. Cancer Res. 41: 5134–5140.Google Scholar
  47. Kalland, T., and Haukaas, S.A., 1981, Effect of treatment with diethylstilbestrol-polyestradiol phosphate or estramustine phosphate (Estracyt®) on natural killer cell activity in patients with prostatic cancer. Invest. Urol. 18:437–441.Google Scholar
  48. Kalland, T., Strand, 0., and Forsberg, J.G., 1979, Long-term effects of neonatal estrogen treatment on mitogen responsiveness of mouse spleen lymphocytes. J. Natl. Cancer Inst. 63: 413–421.Google Scholar
  49. Karmali, R.A., Lauder, I., and Horrobin, D.F., 1974, Prolactin and the immune response. Lancet July (II):106–107.Google Scholar
  50. Kass, E.H., 1960, Bacteriuria and pyelonephritis of pregnancy. Arch. Int. Med., 105: 194–198.Google Scholar
  51. Kato, J,1977, Steroid hormone receptors in brain, hypothalamus, and hypophysis, in “Receptors and Mechanisms of Action of Steroid Hormones”, J.R. Pasqualini, ed.,pp. 603–671, Marcel Dekker, New York.Google Scholar
  52. Katzenellenbogen, J.A., Katzenellenbogen, B.S., Tatee, T., Robertson, D.W., and Landvatter, S.W., 1980, in “Estrogens in the Environment”, J.A. McLachlan, ed., pp. 33–51, Elsevier, North Holland.Google Scholar
  53. Kelly, J.D., and Dineen, J.K., 1973, The suppression of rejection of Nippostrongylus brasilunsis in Lewis strain rats treated with ovine prolactin. Immunology 24: 551–558.Google Scholar
  54. Kelly, L.S., Brown, B.A., and Dobson, E.L., 1962, Cell division and phagocytic activity in liver reticuloendothelial cells. Proc. Soc. Exp. Biol. Med. 110:555–559.Google Scholar
  55. Kenny, J.F., and Gray, J.A., 1971, Sex differences in immunologic response: studies of antibody production by individual spleen cells after stimulus with Escherichia coli antigen. Pediat. Res. 5:246–255.Google Scholar
  56. Kenny, J.F., Pangburn, P.C., and Trail, G., 1976, Effect of estradiol on immune competence: in vivo and in vitro studies. Infect. Immun. 13:448–456.Google Scholar
  57. Kierszenbaum, F., Knecht, E., Budzko, D.B., and Pizzimenti, M.C., 1974, Phagocytosis: a defense mechanism against infection with Trypanosoma cruzi. J. Immunol. 112:1839–1844.Google Scholar
  58. Kitay, J.I., 1963, Pituitary-adrenal function in the rat after gonadectomy and gonadal hormone replacement. Endocrinology 73: 253–260.Google Scholar
  59. Kitay, J.I., Cayne, M.D., Newsom, W., and Nelson, R., 1965, Relation of the ovary to adrenal corticosterone production and adrenal enzyme activity in the rat. Endocrinology 77: 902–908.Google Scholar
  60. Kitay, J.I., Cayne, M.D., and Swygert, N.H., 1970, Influence of gonadectorny and replacement with estradiol or testosterone on formation of 5a-reduced metabolites of corticosterone by the adrenal gland of the rat. Endocrinology 87: 1257–1265.PubMedGoogle Scholar
  61. Krzych, U., Strausser, H.R., Bressler, J.P., and Goldstein, A.L., 1981, Effects of sex hormones on some T and B cell functions, evidenced by differential immune expression between male and female mice and cyclic pattern of immune responsiveness during the estrous cycle in female mice. Am. J. Repro. Immunol. 1:73–77.Google Scholar
  62. Loose, L.D., and DiLuzio, N.R., 1976, Dose related reticuloendothelial system stimulation by diethylstilbestrol. J. Reticuloendothel. Soc. 20:457–460.Google Scholar
  63. Luebke, R.W., Luster, M.I., Dean, J.H., and Hayes, H.T., 1984, Altered host resistance to Trichinella spiralis infection following subchronic exposure to diethylstilbestrol. Int. J. Immunopharmacol. in press.Google Scholar
  64. Luft, B.J., and Remington, J.S., 1982, Effect of pregnancy on resistance to Listeria monocytogenes and Toxoplasma gondii infections in mice. Infect. Immun. 38:1164–1171.Google Scholar
  65. Luster, M.I., Boorman, G.A., Dean, J.H., Lawson, L.D., Wilson, R., and Haseman, J.K., 1981, Immunological alterations in mice following adult exposure to diethylstilbestrol, in “Biological Relevance of Immunosuppression”, J.H. Dean and M.L. Padarathsingh, eds., pp. 153–175, Van Nostrand, New York.Google Scholar
  66. Luster, M.I., Boorman, G.A., Dean, J.H., Luebke, R.W., and Lawson, L.D., 1980, The effect of adult exposure to diethylstilbestrol in the mouse: alterations in immunological functions. J. Reticuloendothel. Soc., 28:561–569.Google Scholar
  67. Luster, M.I., Boorman, G.A., Korach, K.S., Dieter, M.P., and Hong, L., 1984a, Mechanisms of estrogen-induced myelotoxicity: evidence of thymic regulation. Int. J. Immunopharmacol. 6:287–297.Google Scholar
  68. Luster, M.I., Hayes, H.T., Korach, K., Tucker, A.N., Dean, J.H., Greenlee, W.F., and Boorman, G.A., 1984b, Estrogen immunosuppression is regulated through estrogenic responses in the thymus. J. Immunol., 133: 110–116.PubMedGoogle Scholar
  69. Luster, M.i., Pfeifer, R.W., and Tucker, A.N., 1985, Influence of sex hormones on immunoregulation with specific reference to natural and synthetic estrogens, in “Endocrine Toxicology”, J.A. McLachlan, K. Korach, and J. Thomas, eds., pp. 67–83, Raven Press, New York.Google Scholar
  70. MacMartin, K.E., Kennedy, K.A., Greenspan, P., Alam, S.N., Greiner, P., and Yum, J., 1978, Diethylstilbestrol: a review of its toxicity and use as a growth promotant in food producing animals. J. Environ. Pathol. Toxicol. 1:297–313.Google Scholar
  71. Mankau, S.K., 1975, Host sex and sex hormones as a factor affecting Trypanosoma lewisi population in white rats. Jap. J. Parasitol. 24:379–384.Google Scholar
  72. Mathur, S., Mathur, R.S., Goust, J.M., Williamson, H.O., and Fudenburg, H.H., 1979, Cyclic variations in white cell subpopulations in the human menstrual cycle: Correlations with progesterone and estradiol. Clin. Immunol. Immunopath. 13:246–253.Google Scholar
  73. McLachlan, J.A., and Dixon, R.L., 1976, Transplacental toxicity of diethylstilbestrol: A special problem in safety evaluation, in “Advances in Modern Toxicology”, M. Mehlman, and R.E. Shapiro, eds., Vol. 1, pp. 423–448, Hemisphere Publ. Corp., New York.Google Scholar
  74. Mendelow, D.A., and Lewis, G.C., 1969, Varicella pneumonia during pregnancy. Obstet. Gynecol. 33:98–99.Google Scholar
  75. Mendelsohn, J., Multer, M.M., and Bernheim, J.L., 1977, Inhibition of human lymphocyte stimulation by steroid hormones: Cytokinetic mechanisms. Clin. Exp. Immunol. 27:127–134.Google Scholar
  76. Mitchell, G.W., Jacobs, A.A., Haddad, V., Paul, B.B., Strauss, R.R., and Sbarra, A.J., 1970, The role of the phagocyte in host-parasite interactions. XXV. Metabolic and bactericidal activities of leukocytes from pregnant women. Am. J. Obstet. Gynecol. 108:805–813.Google Scholar
  77. Mitchell, G.W., McRipley, R.J., Selvaraj, R.J., and Sbarra, A.J., 1966, The role of the phagocyte in host-parasite interactions. IV. The phagocytic activity of leuocytes in pregnancy and its relationship to urinary tract infections. Am. J. Obstet Gynecol. 96:687–697.Google Scholar
  78. Morahan, P.S., Bradley, S.G., Menson, A.E., Duke, S., Fromtling, R.A., and Marciano-Cabral, F., 1984, Immunotoxic effects of diethylstilbestrol on host resistance: comparison with cyclophosphamide. J. Leukocyte Biol. 35: 329–341.PubMedGoogle Scholar
  79. Muller, R.E., and Wotiy, H.H., 1978, Estrogen-binding protein in mouse and rat adrenal glands. J. Biol. Chem. 253:740–745.Google Scholar
  80. Munson, A.E., Levy, J.A., Harris, L.S., and Dewy, W.L., 1976, Effects of e-tetrahydrocannabinol on the immune system, in “Pharmacology of Marihuana”, M.C. Braude, and S. Szara, eds., pp. 187–197, Raven Press, New York.Google Scholar
  81. Neill, J.D., 1980, Neuroendocrine regulation of prolactin secretion, in “Frontiers in Neuroendocrinology”, L. Martini, and W.F. Ganong, eds., 6:129–155, Raven Press, New York.Google Scholar
  82. Nicol, T., and Abou-Zikry, A., 1953, Influence of eostradiol benzoate and orchidectomy on the reticuloendothelial system. Brit. Med. J. 1:133–134.Google Scholar
  83. Nicol, T., Bilbey, D.L.J., Charles, L.M., Cordingley, J.L., and Vernon-Roberts, B., 1964, Oestrogen: the natural stimulant of body defense. J. Endocrinol. 30:277–291.Google Scholar
  84. Nicol, T., and Vernon-Roberts, B., 1965, The influence of the estrus cycle, pregnancy and ovariectomy on RES activity. J. Reticuloendothel. Soc. 2:15–29.Google Scholar
  85. Paavonen, T., Andersson, L.C., and Aldercreutz, H., 1981, Sex hormone ‘regulation of in vitro immune response. J. Exp. Med. 154:1935–1945.Google Scholar
  86. Pfaff, D.W., 1983, Impact of estrogens on hypothalamic nerve cells: ultrastructural, chemical and electrical effects. Rec. Prog. Hormone Res., 39:127–179.Google Scholar
  87. Pung75.J., Luster, M.I., Hayes, H.T., and Rader, J., 1984, Influence of steroidal and nonsteroidal sex hormones on host resistance in the mouse: Increased susceptibility to Listeria monocytogenes following exposure to estrogenic hormones. Infect. Immun. 46:301–307.Google Scholar
  88. Purtilo, D.T., Hallgren, H.M., and Yunis, E.J., 1972, Depressed maternal lymphocyte response to phytohaemagglutinin in human pregnancy. Lancet 1: 769–771.Google Scholar
  89. Rank, R.G., White, H.J., Hough, A.J., Pasley, J.N., and Barrow, A.L., 1982, Effect of estradiol on chlamydial genital infection of female guinea pigs. Infect. Immun. 38:699–705.Google Scholar
  90. Reichman, M.E., and Villee, C.A., 1978, Estradiol binding by rat thymus cytosol. J. Steroid Biochem. 9:637–641.Google Scholar
  91. Reisher, E.H., 1966, Tissue culture of bone marrow. H. Effect ofGoogle Scholar
  92. steroid hormones on hematopoiesis in vitro. Blood 27:460. Rhodes, K., Scott, A., Markham, R.L., and Monk-Jones, M.E., 1969Google Scholar
  93. Immunological sex differences. Ann. Rheum. Dis. 28:104–119. Rifkind, D., and Frey, J., 1972, Sex difference in antibody response of CFW mice to Candida Albicans. Infect. Immun. 5:695–698.Google Scholar
  94. Rifkind, D., and Frey, J.A., 1974, Influence of androgen and estrogen on delayed skin test reactivity to Candida albicans. Infect. Immun. 10:971–974.Google Scholar
  95. Santoli, D., Trichieri, G., Amijewski, C.M., and Koprowski, H., 1976, HLA-related control of spontaneous and antibody-dependent cell-mediated cytotoxicity in humans. J. Immunol. 117:765–770.Google Scholar
  96. Scheiff, J.M., and Haumont, S., 1979, The effect of oestradiol on thymic epithelial cells in the mouse. J. Clin. Lab. Immunol. 2:225–234.Google Scholar
  97. Seaman, W.F., Merigan, T.C., and Talal, N., 1979, Natural killing in estrogen-treated mice responds poorly to poly I.0 despite normal stimulation of circulating interferon. J. Immunol. 123:2903–2905.Google Scholar
  98. Sljivic, V.S., and Warr, G.W., 1974, Activity of the reticuloendothelial system and the antibody response. III. The fate of Type III pneumococcal polysaccharide and the antibody response. Immunology 27: 1009–1022.PubMedGoogle Scholar
  99. Sljivic, V.S., Clark, D.W., and Warr, G.W., 1975, Effects of estrogens and pregnancy on the distribution of sheep erythrocytes and the antibody response in mice. Clin. Exp. Immunol. 20:179–186.Google Scholar
  100. Stern, K., and Davidsohn, I., 1955, Effect of estrogen and cortisone on immune hemeoantibodies in mice of inbred strains. J. Immunol. 74:479–486.Google Scholar
  101. Stimson, W.H., 1976, Studies on the immunosuppressive properties of a pregnancy-associated alph-macroglobulin. Clin. Exp. Immunol. 25:199–206.Google Scholar
  102. Stimson, W.H., and Crilly, P.J., 1981, Effects of steroids on the secretion of immunoregulatory factors by thymic epithelial cell cultures. Immunology 44: 401–407.Google Scholar
  103. Stimson, W.H., and Hunter, I.C., 1980, Oestrogen-induced immunoregulation mediated through the thymus. J. Clin. Lab. Immunol. 4:27–33.Google Scholar
  104. Sturgis, C.C., and Bethell, F.H., 1943, Quantitative and qualitative variations in normal leukocytes. Physiol. Rev. 23:279–303.Google Scholar
  105. Suzuki, K., and Tomasi, T.B., 1979, Immune responses during pregnancy. Evidence of suppressor cells for splenic antibody response. J. Exp. Med.,150:898–908.Google Scholar
  106. Tshernitchin, A.N., 1983, Eosinophil-mediated non-genomic parameters of estrogen stimulation - a separate group of responses mediated by an independent mechanism. J. Steroid Biochem. 19:95–100.Google Scholar
  107. Terres, G., Morrison, S.L., and Habicht, G.S., 1968, A quantitative difference in the immune response between male and female mice. Proc. Soc. Exp. Biol. Med. 127:664–667.Google Scholar
  108. Toivanen, P., 1967, Enhancement of staphylococcal infection in mice by estrogens. I. Effect of timing, quantity and quality of the hormone. Ann. Med. Exp. Fenn. 45: 138–146.Google Scholar
  109. Valdimarsson, H., Mulholland, C., Fridriksdottir, V., and Coleman, D., 1983, A longitudinal study of leucocyte blood counts and lymphocyte responses in pregnancy: a marked early increase of monocyte-lymphocyte ratio. Clin. Exp. Immunol. 53:437–443.Google Scholar
  110. van Zon, A.A.J.C., Eling, W.M.C., Hermsen, C.C.R., and Koekkoek, A.A.G.M., 1982, Corticosterone regulation of effector function of malarial immunity during pregnancy. Infect. Immun. 36:484–491.Google Scholar
  111. Vaughan, J.E., and Ramirez, H., 1951, Coccidiorodomycosis as a complication of pregnancy. Calif. Med. 74:121–125.Google Scholar
  112. Vernon-Roberts, B., 1969, The effect of steroid hormones on macrophage activity. Int. Rev. Cytol. 25:133–151.Google Scholar
  113. Waltman, S.R., Burde, R.M., and Berrias, J., 1971, Prevention of cornealGoogle Scholar
  114. homograft rejection by estrogens. Transplantation 11:194–196. Washburn, T., Medearis, D., and Childs, B., 1965, Sex differences in susceptibility to infections. Pediatrics 35:57–64.Google Scholar

Copyright information

© Springer Science+Business Media New York 1986

Authors and Affiliations

  • Oscar J. Pung
    • 1
  • Anne N. Tucker
    • 1
  • Michael I. Luster
    • 1
  1. 1.National Institute of Environmental Health Sciences Systemic Toxicology Branch, TRTPResearch Triangle ParkUSA

Personalised recommendations