Sex Steroid Receptors in Immune Cells



Lymphocytes and myeloid cells express estrogen, progesterone, and androgen receptors, and studies show that sex steroid hormones directly modulate their activation, lifespan, and functional response during innate and adaptive immunity. Hematopoietic progenitors also express estrogen and androgen receptors, and profound effects of sex hormones on development of lymphoid and myeloid cells have been reported. The sex steroid receptors act as nuclear transcription factors, via multiple ligand-dependent or ligand-independent mechanisms. Sex steroid receptors also mediate rapid signaling events that synergize with membrane receptor signaling. The basis of sex-based differences in immunity will be clarified by determination of the potentially diverse molecular mechanisms by which sex steroid receptor signaling regulates immune cell development and function.


Estrogen Receptor Androgen Receptor Progesterone Receptor Hematopoietic Progenitor Estrogen Receptor Expression 
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.



The authors thank Dr. John Knight for expert editorial assistance.


  1. Aboudkhil S, Bureau JP, Garrelly L, Vago P (1991) Effects of castration, Depo-testosterone and cyproterone acetate on lymphocyte T subsets in mouse thymus and spleen. Scand J Immunol 34:647–653PubMedCrossRefGoogle Scholar
  2. Acconcia F, Ascenzi P, Bocedi A, Spisni E, Tomasi V, Trentalance A, Visca P, Marino M (2005) Palmitoylation-dependent estrogen receptor alpha membrane localization: regulation by 17beta-estradiol. Mol Biol Cell 16:231–237PubMedCrossRefGoogle Scholar
  3. Adams JS (2005) “Bound” to work: the free hormone hypothesis revisited. Cell 122:647–649PubMedCrossRefGoogle Scholar
  4. Ahmadi K, McCruden AB (2006) Macrophage may responses to androgen via its receptor. Med Sci Monit 12:BR15–BR20PubMedGoogle Scholar
  5. Ahmed SA (2000) The immune system as a potential target for environmental estrogens (endocrine disrupters): a new emerging field. Toxicology 150:191–206PubMedCrossRefGoogle Scholar
  6. Ahmed SA, Penhale WJ, Talal N (1985) Sex hormones, immune responses, and autoimmune diseases. Mechanisms of sex hormone action. Am J Pathol 121:531–551Google Scholar
  7. Angele MK, Ayala A, Cioffi WG, Bland KI, Chaudry IH (1998) Testosterone: the culprit for producing splenocyte immune depression after trauma hemorrhage. Am J Physiol 274:C1530–C1536PubMedGoogle Scholar
  8. Angele MK, Schwacha MG, Ayala A, Chaudry IH (2000) Effect of gender and sex hormones on immune responses following shock. Shock 14:81–90PubMedCrossRefGoogle Scholar
  9. Arruvito L, Giulianelli S, Flores AC, Paladino N, Barboza M, Lanari C, Fainboim L (2008) NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J Immunol 180:5746–5753PubMedGoogle Scholar
  10. Askanase AD, Buyon JP (2002) Reproductive health in SLE. Best Pract Res Clin Rheumatol 16:265–280PubMedCrossRefGoogle Scholar
  11. Bamberger CM, Else T, Bamberger AM, Beil FU, Schulte HM (1999) Dissociative glucocorticoid activity of medroxyprogesterone acetate in normal human lymphocytes. J Clin Endocrinol Metab 84:4055–4061PubMedCrossRefGoogle Scholar
  12. Barkhem T, Carlsson B, Nilsson Y, Enmark E, Gustafsson J, Nilsson S (1998) Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol 54:105–112PubMedGoogle Scholar
  13. Benten WP, Wunderlich F, Herrmann R, Kuhn-Velten WN (1993) Testosterone-induced compared with oestradiol-induced immunosuppression against Plasmodium chabaudi malaria. J Endocrinol 139:487–494PubMedCrossRefGoogle Scholar
  14. Benten WP, Lieberherr M, Sekeris CE, Wunderlich F (1997) Testosterone induces Ca2+ influx via non-genomic surface receptors in activated T cells. FEBS Lett 407:211–214PubMedCrossRefGoogle Scholar
  15. Benten WP, Lieberherr M, Giese G, Wrehlke C, Stamm O, Sekeris CE, Mossmann H, Wunderlich F (1999a) Functional testosterone receptors in plasma membranes of T cells. Faseb J 13:123–133PubMedGoogle Scholar
  16. Benten WP, Lieberherr M, Stamm O, Wrehlke C, Guo Z, Wunderlich F (1999b) Testosterone signaling through internalizable surface receptors in androgen receptor-free macrophages. Mol Biol Cell 10:3113–3123PubMedGoogle Scholar
  17. Benten WP, Becker A, Schmitt-Wrede HP, Wunderlich F (2002a) Developmental regulation of intracellular and surface androgen receptors in T cells. Steroids 67:925–931PubMedCrossRefGoogle Scholar
  18. Benten WP, Stephan C, Wunderlich F (2002b) B cells express intracellular but not surface receptors for testosterone and estradiol. Steroids 67:647–654PubMedCrossRefGoogle Scholar
  19. Benten WP, Guo Z, Krucken J, Wunderlich F (2004) Rapid effects of androgens in macrophages. Steroids 69:585–590PubMedCrossRefGoogle Scholar
  20. Bhasin S, Storer TW, Javanbakht M, Berman N, Yarasheski KE, Phillips J, Dike M, Sinha-Hikim I, Shen R, Hays RD, Beall G (2000) Testosterone replacement and resistance exercise in HIV-infected men with weight loss and low testosterone levels. Jama 283:763–770PubMedCrossRefGoogle Scholar
  21. Bhat-Nakshatri P, Campbell RA, Patel NM, Newton TR, King AJ, Marshall MS, Ali S, Nakshatri H (2004) Tumour necrosis factor and PI3-kinase control oestrogen receptor alpha protein level and its transrepression function. Br J Cancer 90:853–859PubMedCrossRefGoogle Scholar
  22. Bjornstrom L, Sjoberg M (2002) Signal transducers and activators of transcription as downstream targets of nongenomic estrogen receptor actions. Mol Endocrinol 16:2202–2214PubMedCrossRefGoogle Scholar
  23. Blondeau JP, Baulieu EE (1984) Progesterone receptor characterized by photoaffinity labelling in the plasma membrane of Xenopus laevis oocytes. Biochem J 219:785–792PubMedGoogle Scholar
  24. Boonyaratanakornkit V, McGowan E, Sherman L, Mancini MA, Cheskis BJ, Edwards DP (2007) The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol Endocrinol 21:359–375PubMedCrossRefGoogle Scholar
  25. Brinkmann AO, Trapman J (2000) Genetic analysis of androgen receptors in development and disease. Adv Pharmacol 47:317–341PubMedCrossRefGoogle Scholar
  26. Brinkmann AO, Faber PW, van Rooij HC, Kuiper GG, Ris C, Klaassen P, van der Korput JA, Voorhorst MM, van Laar JH, Mulder E et al (1989) The human androgen receptor: domain structure, genomic organization and regulation of expression. J Steroid Biochem 34:307–310PubMedCrossRefGoogle Scholar
  27. Burger HG (2002) Androgen production in women. Fertil Steril 77(Suppl 4):S3–S5PubMedCrossRefGoogle Scholar
  28. Butts CL, Shukair SA, Duncan KM, Bowers E, Horn C, Belyavskaya E, Tonelli L, Sternberg EM (2007a) Progesterone inhibits mature rat dendritic cells in a receptor-mediated fashion. Int Immunol 19:287–296PubMedCrossRefGoogle Scholar
  29. Butts CL, Shukair SA, Duncan KM, Harris CW, Belyavskaya E, Sternberg EM (2007b) Evaluation of steroid hormone receptor protein expression in intact cells using flow cytometry. Nucl Recept Signal 5:e007PubMedGoogle Scholar
  30. Bynoe MS, Grimaldi CM, Diamond B (2000) Estrogen up-regulates Bcl-2 and blocks tolerance induction of naive B cells. Proc Natl Acad Sci U S A 97:2703–278PubMedCrossRefGoogle Scholar
  31. Cadepond F, Ulmann A, Baulieu EE (1997) RU486 (mifepristone): mechanisms of action and clinical uses. Annu Rev Med 48:129–156PubMedCrossRefGoogle Scholar
  32. Calippe B, Douin-Echinard V, Laffargue M, Laurell H, Rana-Poussine V, Pipy B, Guery JC, Bayard F, Arnal JF, Gourdy P (2008) Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to tlr4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J Immunol 180:7980–7988PubMedGoogle Scholar
  33. Carreras E, Turner S, Paharkova-Vatchkova V, Mao A, Dascher C, Kovats S (2008) Estradiol acts directly on bone marrow myeloid progenitors to differentially regulate GM-CSF or Flt3 Ligand mediated dendritic cell differentiation. J. Immunol. 180:727–738PubMedGoogle Scholar
  34. Carson-Jurica MA, Schrader WT, O’Malley BW (1990) Steroid receptor family: structure and functions. Endocr Rev 11:201–220PubMedCrossRefGoogle Scholar
  35. Castles CG, Oesterreich S, Hansen R, Fuqua SA (1997) Auto-regulation of the estrogen receptor promoter. J Steroid Biochem Mol Biol 62:155–163PubMedCrossRefGoogle Scholar
  36. Cenni B, Picard D (1999) Ligand-independent Activation of Steroid Receptors: New Roles for Old Players. Trends Endocrinol Metab 10:41–46PubMedCrossRefGoogle Scholar
  37. Chang CS, Kokontis J, Liao ST (1988a) Molecular cloning of human and rat complementary DNA encoding androgen receptors. Science 240:324–326PubMedCrossRefGoogle Scholar
  38. Chang CS, Kokontis J, Liao ST (1988b) Structural analysis of complementary DNA and amino acid sequences of human and rat androgen receptors. Proc Natl Acad Sci USA 85:7211–7215PubMedCrossRefGoogle Scholar
  39. Chang EC, Frasor J, Komm B, Katzenellenbogen BS (2006) Impact of estrogen receptor beta on gene networks regulated by estrogen receptor alpha in breast cancer cells. Endocrinology 147:4831–4842PubMedCrossRefGoogle Scholar
  40. Chao TC, Van Alten PJ, Greager JA, Walter RJ (1995) Steroid sex hormones regulate the release of tumor necrosis factor by macrophages. Cell Immunol 160:43–49PubMedCrossRefGoogle Scholar
  41. Chen T, Wang LH, Farrar WL (2000) Interleukin 6 activates androgen receptor-mediated gene expression through a signal transducer and activator of transcription 3-dependent pathway in LNCaP prostate cancer cells. Cancer Res 60:2132–2135PubMedGoogle Scholar
  42. Cheng J, Watkins SC, Walker WH (2007) Testosterone activates mitogen-activated protein kinase via Src kinase and the epidermal growth factor receptor in sertoli cells. Endocrinology 148:2066–2074PubMedCrossRefGoogle Scholar
  43. Chien EJ, Liao CF, Chang CP, Pu HF, Lu LM, Shie MC, Hsieh DJ, Hsu MT (2007) The non-genomic effects on Na+/H + -exchange 1 by progesterone and 20alpha-hydroxyprogesterone in human T cells. J Cell Physiol 211:544–550PubMedCrossRefGoogle Scholar
  44. Chopra DP, Menard RE, Januszewski J, Mattingly RR (2004) TNF-alpha-mediated apoptosis in normal human prostate epithelial cells and tumor cell lines. Cancer Lett 203:145–154PubMedCrossRefGoogle Scholar
  45. Couse JF, Korach KS (1999) Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20:358–417PubMedCrossRefGoogle Scholar
  46. Couse JF, Curtis SW, Washburn TF, Lindzey J, Golding TS, Lubahn DB, Smithies O, Korach KS (1995) Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Mol Endocrinol 9:1441–1454PubMedCrossRefGoogle Scholar
  47. Culig Z (2004) Androgen receptor cross-talk with cell signalling pathways. Growth Factors 22:179–184PubMedCrossRefGoogle Scholar
  48. Culig Z, Hobisch A, Cronauer MV, Radmayr C, Trapman J, Hittmair A, Bartsch G, Klocker H (1994) Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-I, keratinocyte growth factor, and epidermal growth factor. Cancer Res 54:5474–5478PubMedGoogle Scholar
  49. Curran EM, Berghaus LJ, Vernetti NJ, Saporita AJ, Lubahn DB, Estes DM (2001) Natural killer cells express estrogen receptor-alpha and estrogen receptor-beta and can respond to estrogen via a non-estrogen receptor-alpha-mediated pathway. Cell Immunol 214:12–20PubMedCrossRefGoogle Scholar
  50. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, Straub RH (2004) Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus Lupus 13:635–638Google Scholar
  51. Cvoro A, Tzagarakis-Foster C, Tatomer D, Paruthiyil S, Fox MS, Leitman DC (2006) Distinct roles of unliganded and liganded estrogen receptors in transcriptional repression. Mol Cell 21:555–564PubMedCrossRefGoogle Scholar
  52. Cvoro A, Tatomer D, Tee MK, Zogovic T, Harris HA, Leitman DC (2008) Selective estrogen receptor-beta agonists repress transcription of proinflammatory genes. J Immunol 180:630–636PubMedGoogle Scholar
  53. Da Silva JA (1995) Sex hormones, glucocorticoids and autoimmunity: facts and hypotheses. Ann Rheum Dis 54:6–16PubMedCrossRefGoogle Scholar
  54. Dai R, Phillips RA, Ahmed SA (2007) Despite inhibition of nuclear localization of NF-kappa B p65, c-Rel, and RelB, 17-beta estradiol up-regulates NF-kappa B signaling in mouse splenocytes: the potential role of Bcl-3. J Immunol 179:1776–1783PubMedGoogle Scholar
  55. Darne C, Veyssiere G, Jean C (1998) Phorbol ester causes ligand-independent activation of the androgen receptor. Eur J Biochem 256:541–549PubMedCrossRefGoogle Scholar
  56. Davison SL, Bell R (2006) Androgen physiology. Semin Reprod Med 24:71–77PubMedCrossRefGoogle Scholar
  57. Davison SL, Bell R, Donath S, Montalto JG, Davis SR (2005) Androgen levels in adult females: changes with age, menopause, and oophorectomy. J Clin Endocrinol Metab 90:3847–3853PubMedCrossRefGoogle Scholar
  58. Dayan M, Zinger H, Kalush F, Mor G, Amir-Zaltzman Y, Kohen F, Sthoeger Z, Mozes E (1997) The beneficial effects of treatment with tamoxifen and anti-oestradiol antibody on experimental systemic lupus erythematosus are associated with cytokine modulations. Immunology 90:101–108PubMedCrossRefGoogle Scholar
  59. De Bosscher K, Vanden Berghe W, Haegeman G (2006) Cross-talk between nuclear receptors and nuclear factor kappaB. Oncogene 25:6868–6886PubMedCrossRefGoogle Scholar
  60. Denner LA, Weigel NL, Maxwell BL, Schrader WT, O’Malley BW (1990) Regulation of progesterone receptor-mediated transcription by phosphorylation. Science 250:1740–1743PubMedCrossRefGoogle Scholar
  61. Dhandapani KM, Wade FM, Mahesh VB, Brann DW (2005) Astrocyte-derived transforming growth factor-{beta} mediates the neuroprotective effects of 17{beta}-estradiol: involvement of nonclassical genomic signaling pathways. Endocrinology 146:2749–2759PubMedCrossRefGoogle Scholar
  62. Dorner G, Eckert R, Hinz G (1980) Androgen-dependent sexual dimorphism of the immune system. Endokrinologie 76:112–114PubMedGoogle Scholar
  63. Dosiou C, Hamilton AE, Pang Y, Overgaard MT, Tulac S, Dong J, Thomas P, Giudice LC (2008) Expression of membrane progesterone receptors on human T lymphocytes and Jurkat cells and activation of G-proteins by progesterone. J Endocrinol 196:67–77PubMedCrossRefGoogle Scholar
  64. Douin-Echinard V, Laffont S, Seillet C, Delpy L, Krust A, Chambon P, Gourdy P, Arnal JF, Guery JC (2008) Estrogen receptor alpha, but not beta, is required for optimal dendritic cell differentiation and CD40-induced cytokine production. J Immunol 180:3661–3669PubMedGoogle Scholar
  65. Dunn JF, Nisula BC, Rodbard D (1981) Transport of steroid hormones: binding of 21 endogenous steroids to both testosterone-binding globulin and corticosteroid-binding globulin in human plasma. J Clin Endocrinol Metab 53:58–68PubMedCrossRefGoogle Scholar
  66. Dutertre M, Smith CL (2000) Molecular mechanisms of selective estrogen receptor modulator (SERM) action. J Pharmacol Exp Ther 295:431–47PubMedGoogle Scholar
  67. Edwards DP (2005) Regulation of signal transduction pathways by estrogen and progesterone. Annu Rev Physiol 67:335–376PubMedCrossRefGoogle Scholar
  68. Ehring GR, Kerschbaum HH, Eder C, Neben AL, Fanger CM, Khoury RM, Negulescu PA, Cahalan MD (1998) A nongenomic mechanism for progesterone-mediated immunosuppression: inhibition of K + channels, Ca2+ signaling, and gene expression in T lymphocytes. J Exp Med 188:1593–1602PubMedCrossRefGoogle Scholar
  69. Ellis TM, Moser MT, Le PT, Flanigan RC, Kwon ED (2001) Alterations in peripheral B cells and B cell progenitors following androgen ablation in mice. Int Immunol 13:553–558PubMedCrossRefGoogle Scholar
  70. Er F, Michels G, Gassanov N, Rivero F, Hoppe UC (2004) Testosterone induces cytoprotection by activating ATP-sensitive K + channels in the cardiac mitochondrial inner membrane. Circulation 110:3100–3107PubMedCrossRefGoogle Scholar
  71. Erlandsson MC, Ohlsson C, Gustafsson JA, Carlsten H (2001) Role of oestrogen receptors alpha and beta in immune organ development and in oestrogen-mediated effects on thymus. Immunology 103:17–25PubMedCrossRefGoogle Scholar
  72. Estrada M, Espinosa A, Muller M, Jaimovich E (2003) Testosterone stimulates intracellular calcium release and mitogen-activated protein kinases via a G protein-coupled receptor in skeletal muscle cells. Endocrinology 144:3586–3597PubMedCrossRefGoogle Scholar
  73. Evans RM (1988) The steroid and thyroid hormone receptor superfamily. Science 240:889–895PubMedCrossRefGoogle Scholar
  74. Faulds MH, Pettersson K, Gustafsson JA, Haldosen LA (2001) Cross-talk between ERs and signal transducer and activator of transcription 5 is E2 dependent and involves two functionally separate mechanisms. Mol Endocrinol 15:1929–1940PubMedCrossRefGoogle Scholar
  75. Foradori CD, Weiser MJ, Handa RJ (2008) Non-genomic actions of androgens. Front Neuroendocrinol 29:169–181PubMedGoogle Scholar
  76. Foster HL, Small JD, Fox JG (1983) Normative biology, immunology and husbandry. Academic Press Inc., Orlando, FLGoogle Scholar
  77. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS (2003) Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 144:4562–4574PubMedCrossRefGoogle Scholar
  78. Freeman MR, Cinar B, Lu ML (2005) Membrane rafts as potential sites of nongenomic hormonal signaling in prostate cancer. Trends Endocrinol Metab 16:273–279PubMedCrossRefGoogle Scholar
  79. Frey-Wettstein M, Craddock CG (1970) Testosterone-induced depletion of thymus and marrow lymphocytes as related to lymphopoiesis and hematopoiesis. Blood 35:257–271PubMedGoogle Scholar
  80. Gao W, Dalton JT (2007) Expanding the therapeutic use of androgens via selective androgen receptor modulators (SARMs). Drug Discov Today 12:241–248PubMedCrossRefGoogle Scholar
  81. Gao T, McPhaul MJ (1998) Functional activities of the A and B forms of the human androgen receptor in response to androgen receptor agonists and antagonists. Mol Endocrinol 12:654–663PubMedCrossRefGoogle Scholar
  82. Gao Y, Qian WP, Dark K, Toraldo G, Lin AS, Guldberg RE, Flavell RA, Weitzmann MN, Pacifici R (2004) Estrogen prevents bone loss through transforming growth factor beta signaling in T cells. Proc Natl Acad Sci USA 101:16618–16623PubMedCrossRefGoogle Scholar
  83. Gao W, Bohl CE, Dalton JT (2005) Chemistry and structural biology of androgen receptor. Chem Rev 105:3352–3370PubMedCrossRefGoogle Scholar
  84. Ghisletti S, Meda C, Maggi A, Vegeto E (2005) 17beta-estradiol inhibits inflammatory gene expression by controlling NF-kappaB intracellular localization. Mol Cell Biol 25:2957–2968PubMedCrossRefGoogle Scholar
  85. Gilmore TD (2006) Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25:6680–6684PubMedCrossRefGoogle Scholar
  86. Gilmore W, Weiner LP, Correale J (1997) Effect of estradiol on cytokine secretion by proteolipid protein-specific T cell clones isolated from multiple sclerosis patients and normal control subjects. J Immunol 158:446–451PubMedGoogle Scholar
  87. Goldberg GL, Alpdogan O, Muriglan SJ, Hammett MV, Milton MK, Eng JM, Hubbard VM, Kochman A, Willis LM, Greenberg AS, Tjoe KH, Sutherland JS, Chidgey A, van den Brink MR, Boyd RL (2007) Enhanced immune reconstitution by sex steroid ablation following allogeneic hemopoietic stem cell transplantation. J Immunol 178:7473–7484PubMedGoogle Scholar
  88. Gonzalez-Flores O, Shu J, Camacho-Arroyo I, Etgen AM (2004) Regulation of lordosis by cyclic 3’, 5’-guanosine monophosphate, progesterone, and its 5alpha-reduced metabolites involves mitogen-activated protein kinase. Endocrinology 145:5560–5567PubMedCrossRefGoogle Scholar
  89. Gourdy P, Araujo LM, Zhu R, Garmy-Susini B, Diem S, Laurell H, Leite-de-Moraes M, Dy M, Arnal JF, Bayard F, Herbelin A (2005) Relevance of sexual dimorphism to regulatory T cells: estradiol promotes IFN-gamma production by invariant natural killer T cells. Blood 105:2415–2420PubMedCrossRefGoogle Scholar
  90. Graham JD, Clarke CL (1997) Physiological action of progesterone in target tissues. Endocr Rev 18:502–519PubMedCrossRefGoogle Scholar
  91. Granger DA, Booth A, Johnson DR (2000) Human aggression and enumerative measures of immunity. Psychosom Med 62:583–590PubMedGoogle Scholar
  92. Grimaldi CM, Michael DJ, Diamond B (2001) Cutting edge: expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J Immunol 167:1886–190PubMedGoogle Scholar
  93. Grimaldi CM, Cleary J, Dagtas AS, Moussai D, Diamond B (2002) Estrogen alters thresholds for B cell apoptosis and activation. J Clin Invest 109:1625–133PubMedGoogle Scholar
  94. Grimaldi CM, Jeganathan V, Diamond B (2006) Hormonal regulation of B cell development: 17 beta-estradiol impairs negative selection of high-affinity DNA-reactive B cells at more than one developmental checkpoint. J Immunol 176:2703–2710PubMedGoogle Scholar
  95. Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257–261PubMedCrossRefGoogle Scholar
  96. Guo Z, Benten WP, Krucken J, Wunderlich F (2002) Nongenomic testosterone calcium signaling. Genotropic actions in androgen receptor-free macrophages. J Biol Chem 277:29600–29607Google Scholar
  97. Hammes A, Andreassen TK, Spoelgen R, Raila J, Hubner N, Schulz H, Metzger J, Schweigert FJ, Luppa PB, Nykjaer A, Willnow TE (2005) Role of endocytosis in cellular uptake of sex steroids. Cell 122:751–762PubMedCrossRefGoogle Scholar
  98. Harkonen PL, Vaananen HK (2006) Monocyte-macrophage system as a target for estrogen and selective estrogen receptor modulators. Ann N Y Acad Sci 1089:218–227PubMedCrossRefGoogle Scholar
  99. Harman BC, Miller JP, Nikbakht N, Gerstein R, Allman D (2006) Mouse plasmacytoid dendritic cells derive exclusively from estrogen-resistant myeloid progenitors. Blood 108:878–885PubMedCrossRefGoogle Scholar
  100. Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenellenbogen JA, Katzenellenbogen BS (2003) Activities of estrogen receptor alpha- and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol 206:13–22PubMedCrossRefGoogle Scholar
  101. Heinlein CA, Chang C (2002a) Androgen receptor (AR) coregulators: an overview. Endocr Rev 23:175–200PubMedCrossRefGoogle Scholar
  102. Heinlein CA, Chang C (2002b) The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions. Mol Endocrinol 16:2181–2187PubMedCrossRefGoogle Scholar
  103. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M, Gustafsson JA (2007) Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87:905–931PubMedCrossRefGoogle Scholar
  104. Heng TS, Goldberg GL, Gray DH, Sutherland JS, Chidgey AP, Boyd RL (2005) Effects of castration on thymocyte development in two different models of thymic involution. J Immunol 175:2982–2993PubMedGoogle Scholar
  105. Hobisch A, Eder IE, Putz T, Horninger W, Bartsch G, Klocker H, Culig Z (1998) Interleukin-6 regulates prostate-specific protein expression in prostate carcinoma cells by activation of the androgen receptor. Cancer Res 58:4640–4645PubMedGoogle Scholar
  106. Hughes GC, Thomas S, Li C, Kaja MK, Clark EA (2008) Cutting edge: progesterone regulates IFN-alpha production by plasmacytoid dendritic cells. J Immunol 180:2029–2033PubMedGoogle Scholar
  107. Igarashi H, Kouro T, Yokota T, Comp PC, Kincade PW (2001) Age and stage dependency of estrogen receptor expression by lymphocyte precursors. Proc Natl Acad Sci U S A 98:15131–15136PubMedCrossRefGoogle Scholar
  108. Ikeuchi T, Todo T, Kobayashi T, Nagahama Y (1999) cDNA cloning of a novel androgen receptor subtype. J Biol Chem 274:25205–25209PubMedCrossRefGoogle Scholar
  109. Islander U, Erlandsson MC, Hasseus B, Jonsson CA, Ohlsson C, Gustafsson JA, Dahlgren U, Carlsten H (2003) Influence of oestrogen receptor alpha and beta on the immune system in aged female mice. Immunology 110:149–157PubMedCrossRefGoogle Scholar
  110. Jenster G, van der Korput HA, Trapman J, Brinkmann AO (1995) Identification of two transcription activation units in the N-terminal domain of the human androgen receptor. J Biol Chem 270:7341–7346PubMedCrossRefGoogle Scholar
  111. Jones LA, Anthony JP, Henriquez FL, Lyons RE, Nickdel MB, Carter KC, Alexander J, Roberts CW (2008) Toll-like receptor-4-mediated macrophage activation is differentially regulated by progesterone via the glucocorticoid and progesterone receptors. Immunology 125(1):59–69PubMedCrossRefGoogle Scholar
  112. Jordan VC, Gapstur S, Morrow M (2001) Selective estrogen receptor modulation and reduction in risk of breast cancer, osteoporosis, and coronary heart disease. J Natl Cancer Inst 93:1449–1457PubMedCrossRefGoogle Scholar
  113. Kaarbo M, Klokk TI, Saatcioglu F (2007) Androgen signaling and its interactions with other signaling pathways in prostate cancer. Bioessays 29:1227–1238PubMedCrossRefGoogle Scholar
  114. Kalaitzidis D, Gilmore TD (2005) Transcription factor cross-talk: the estrogen receptor and NF-kappaB. Trends Endocrinol Metab 16:46–52PubMedCrossRefGoogle Scholar
  115. Kamath AT, Henri S, Battye F, Tough DF, Shortman K (2002) Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 100:1734–1741PubMedGoogle Scholar
  116. Kampa M, Papakonstanti EA, Hatzoglou A, Stathopoulos EN, Stournaras C, Castanas E (2002) The human prostate cancer cell line LNCaP bears functional membrane testosterone receptors that increase PSA secretion and modify actin cytoskeleton. Faseb J 16:1429–1431PubMedGoogle Scholar
  117. Karpuzoglu E, Fenaux JB, Phillips RA, Lengi AJ, Elvinger F, Ansar Ahmed S (2006) Estrogen up-regulates inducible nitric oxide synthase, nitric oxide, and cyclooxygenase-2 in splenocytes activated with T cell stimulants: role of interferon-gamma. Endocrinology 147:662–671PubMedCrossRefGoogle Scholar
  118. Kaushic C, Ashkar AA, Reid LA, Rosenthal KL (2003) Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J Virol 77:4558–4565PubMedCrossRefGoogle Scholar
  119. Kawasaki T, Choudhry MA, Suzuki T, Schwacha MG, Bland KI, Chaudry IH (2008) 17beta-Estradiol’s salutary effects on splenic dendritic cell functions following trauma-hemorrhage are mediated via estrogen receptor-alpha. Mol Immunol 45:376–385PubMedCrossRefGoogle Scholar
  120. Kazeto Y, Goto-Kazeto R, Thomas P, Trant JM (2005) Molecular characterization of three forms of putative membrane-bound progestin receptors and their tissue-distribution in channel catfish, Ictalurus punctatus. J Mol Endocrinol 34:781–791PubMedCrossRefGoogle Scholar
  121. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Matsuyama T, Ishimaru T (2005) Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis. Hum Reprod 20:2004–2013PubMedCrossRefGoogle Scholar
  122. Kian Tee M, Rogatsky I, Tzagarakis-Foster C, Cvoro A, An J, Christy RJ, Yamamoto KR, Leitman DC (2004) Estradiol and selective estrogen receptor modulators differentially regulate target genes with estrogen receptors alpha and beta. Mol Biol Cell 15:1262–1272PubMedCrossRefGoogle Scholar
  123. Kincade PW, Medina KL, Payne KJ, Rossi MI, Tudor KS, Yamashita Y, Kouro T (2000) Early B-lymphocyte precursors and their regulation by sex steroids. Immunol Rev 175:128–37PubMedCrossRefGoogle Scholar
  124. Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264PubMedCrossRefGoogle Scholar
  125. Klein SL, Wisniewski AB, Marson AL, Glass GE, Gearhart JP (2002) Early exposure to genistein exerts long-lasting effects on the endocrine and immune systems in rats. Mol Med 8:742–749PubMedGoogle Scholar
  126. Komi J, Lassila O (2000) Nonsteroidal anti-estrogens inhibit the functional differentiation of human monocyte-derived dendritic cells. Blood 95:2875–282PubMedGoogle Scholar
  127. Komi J, Mottonen M, Luukkainen R, Lassila O (2001) Non-steroidal anti-oestrogens inhibit the differentiation of synovial macrophages into dendritic cells. Rheumatology (Oxford) 40:185–191CrossRefGoogle Scholar
  128. Konoplya EF, Popoff EH (1992) Identification of the classical androgen receptor in male rat liver and prostate cell plasma membranes. Int J Biochem 24:1979–1983PubMedCrossRefGoogle Scholar
  129. Kontula K, Paavonen T, Luukkainen T, Andersson LC (1983) Binding of progestins to the glucocorticoid receptor. Correlation to their glucocorticoid-like effects on in vitro functions of human mononuclear leukocytes. Biochem Pharmacol 32:1511–1518Google Scholar
  130. Kostellow AB, Weinstein SP, Morrill GA (1982) Specific binding of progesterone to the cell surface and its role in the meiotic divisions in Rana oocytes. Biochim Biophys Acta 720:356–363PubMedCrossRefGoogle Scholar
  131. Kousteni S, Bellido T, Plotkin LI, O’Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719–730PubMedGoogle Scholar
  132. Kovacs EJ (2005) Aging, traumatic injury, and estrogen treatment. Exp Gerontol 40:549–555PubMedCrossRefGoogle Scholar
  133. Kovacs WJ, Olsen NJ (1987) Androgen receptors in human thymocytes. J Immunol 139:490–493PubMedGoogle Scholar
  134. Koyama Y, Nagao S, Ohashi K, Takahashi H, Marunouchi T (1987) Sex differences in the densities of epidermal Langerhans cells of the mouse. J Invest Dermatol 88:541–544PubMedCrossRefGoogle Scholar
  135. Koyama Y, Nagao S, Ohashi K, Takahashi H, Marunouchi T (1989) Effect of systemic and topical application of testosterone propionate on the density of epidermal Langerhans cells in the mouse. J Invest Dermatol 92:86–90PubMedCrossRefGoogle Scholar
  136. Kuiper GG, Faber PW, van Rooij HC, van der Korput JA, Ris-Stalpers C, Klaassen P, Trapman J, Brinkmann AO (1989) Structural organization of the human androgen receptor gene. J Mol Endocrinol 2:R1–4PubMedCrossRefGoogle Scholar
  137. Kurtis JD, Mtalib R, Onyango FK, Duffy PE (2001) Human resistance to Plasmodium falciparum increases during puberty and is predicted by dehydroepiandrosterone sulfate levels. Infect Immun 69:123–128PubMedCrossRefGoogle Scholar
  138. Lambert KC, Curran EM, Judy BM, Lubahn DB, Estes DM (2004) Estrogen receptor-alpha deficiency promotes increased TNF-alpha secretion and bacterial killing by murine macrophages in response to microbial stimuli in vitro. J Leukoc Biol 75:1166–1172PubMedCrossRefGoogle Scholar
  139. Lange CA, Shen T, Horwitz KB (2000) Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26 S proteasome. Proc Natl Acad Sci USA 97:1032–1037PubMedCrossRefGoogle Scholar
  140. Leung KC, Doyle N, Ballesteros M, Sjogren K, Watts CK, Low TH, Leong GM, Ross RJ, Ho KK (2003) Estrogen inhibits GH signaling by suppressing GH-induced JAK2 phosphorylation, an effect mediated by SOCS-2. Proc Natl Acad Sci USA 100:1016–1021PubMedCrossRefGoogle Scholar
  141. Levin ER (2002) Cellular functions of plasma membrane estrogen receptors. Steroids 67:471–475PubMedCrossRefGoogle Scholar
  142. Li L, Ren CH, Tahir SA, Ren C, Thompson TC (2003) Caveolin-1 maintains activated Akt in prostate cancer cells through scaffolding domain binding site interactions with and inhibition of serine/threonine protein phosphatases PP1 and PP2A. Mol Cell Biol 23:9389–9404PubMedCrossRefGoogle Scholar
  143. Liegibel UM, Sommer U, Boercsoek I, Hilscher U, Bierhaus A, Schweikert HU, Nawroth P, Kasperk C (2003) Androgen receptor isoforms AR-A and AR-B display functional differences in cultured human bone cells and genital skin fibroblasts. Steroids 68:1179–1187PubMedCrossRefGoogle Scholar
  144. Lin CY, Vega VB, Thomsen JS, Zhang T, Kong SL, Xie M, Chiu KP, Lipovich L, Barnett DH, Stossi F, Yeo A, George J, Kuznetsov VA, Lee YK, Charn TH, Palanisamy N, Miller LD, Cheung E, Katzenellenbogen BS, Ruan Y, Bourque G, Wei CL, Liu ET (2007) Whole-genome cartography of estrogen receptor alpha binding sites. PLoS Genet 3:e87PubMedCrossRefGoogle Scholar
  145. Liu MM, Albanese C, Anderson CM, Hilty K, Webb P, Uht RM, Price RHJ, Pestell RG, Kushner PJ (2002) Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J Biol Chem 277:24353–24360PubMedCrossRefGoogle Scholar
  146. Liu HB, Loo KK, Palaszynski K, Ashouri J, Lubahn DB, Voskuhl RR (2003) Estrogen receptor alpha mediates estrogen’s immune protection in autoimmune disease. J Immunol 171:6936–6940PubMedGoogle Scholar
  147. Liu L, Benten WP, Wang L, Hao X, Li Q, Zhang H, Guo D, Wang Y, Wunderlich F, Qiao Z (2005) Modulation of Leishmania donovani infection and cell viability by testosterone in bone marrow-derived macrophages: signaling via surface binding sites. Steroids 70:604–614PubMedCrossRefGoogle Scholar
  148. Liva SM, Voskuhl RR (2001) Testosterone acts directly on CD4+ T lymphocytes to increase IL-10 production. J Immunol 167:2060–2067PubMedGoogle Scholar
  149. Losel RM, Falkenstein E, Feuring M, Schultz A, Tillmann HC, Rossol-Haseroth K, Wehling M (2003) Nongenomic steroid action: controversies, questions, and answers. Physiol Rev 83:965–1016PubMedGoogle Scholar
  150. Lubahn DB, Joseph DR, Sullivan PM, Willard HF, French FS, Wilson EM (1988) Cloning of human androgen receptor complementary DNA and localization to the X chromosome. Science 240:327–330PubMedCrossRefGoogle Scholar
  151. Lutz LB, Jamnongjit M, Yang WH, Jahani D, Gill A, Hammes SR (2003) Selective modulation of genomic and nongenomic androgen responses by androgen receptor ligands. Mol Endocrinol 17:1106–1116PubMedCrossRefGoogle Scholar
  152. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA Jr, Shyamala G, Conneely OM, O’Malley BW (1995) Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266–2278PubMedCrossRefGoogle Scholar
  153. Mansour I, Reznikoff-Etievant MF, Netter A (1994) No evidence for the expression of the progesterone receptor on peripheral blood lymphocytes during pregnancy. Hum Reprod 9:1546–1549PubMedGoogle Scholar
  154. Mantalaris A, Panoskaltsis N, Sakai Y, Bourne P, Chang C, Messing EM, Wu JH (2001) Localization of androgen receptor expression in human bone marrow. J Pathol 193:361–366PubMedCrossRefGoogle Scholar
  155. Mao A, Paharkova-Vatchkova V, Hardy J, Miller MM, Kovats S (2005) Estrogen selectively promotes the differentiation of dendritic cells with characteristics of Langerhans cells. J Immunol 175:5146–5151PubMedGoogle Scholar
  156. Maret A, Coudert JD, Garidou L, Foucras G, Gourdy P, Krust A, Dupont S, Chambon P, Druet P, Bayard F, Guery JC (2003) Estradiol enhances primary antigen-specific CD4 T cell responses and Th1 development in vivo. Essential role of estrogen receptor alpha expression in hematopoietic cells. Eur J Immunol 33:512–521Google Scholar
  157. Marino M, Ascenzi P, Acconcia F (2006a) S-palmitoylation modulates estrogen receptor alpha localization and functions. Steroids 71:298–303PubMedCrossRefGoogle Scholar
  158. Marino M, Galluzzo P, Ascenzi P (2006b) Estrogen signaling multiple pathways to impact gene transcription. Curr Genomics 7:497–508PubMedCrossRefGoogle Scholar
  159. Marriott I, Huet-Hudson YM (2006) Sexual dimorphism in innate immune responses to infectious organisms. Immunol Res 34:177–192PubMedCrossRefGoogle Scholar
  160. Matsuda T, Yamamoto T, Muraguchi A, Saatcioglu F (2001a) Cross-talk between transforming growth factor-beta and estrogen receptor signaling through Smad3. J Biol Chem 276:42908–42914PubMedCrossRefGoogle Scholar
  161. Matsuda T, Junicho A, Yamamoto T, Kishi H, Korkmaz K, Saatcioglu F, Fuse H, Muraguchi A (2001b) Cross-talk between signal transducer and activator of transcription 3 and androgen receptor signaling in prostate carcinoma cells. Biochem Biophys Res Commun 283:179–187PubMedCrossRefGoogle Scholar
  162. Matsumoto T, Takeyama K, Sato T, Kato S (2005) Study of androgen receptor functions by genetic models. J Biochem 138:105–110PubMedCrossRefGoogle Scholar
  163. Matsumoto T, Shiina H, Kawano H, Sato T, Kato S (2008) Androgen receptor functions in male and female physiology. J Steroid Biochem Mol Biol 109:236–241PubMedCrossRefGoogle Scholar
  164. Matthews J, Wihlen B, Tujague M, Wan J, Strom A, Gustafsson JA (2006) Estrogen receptor (ER) beta modulates ERalpha-mediated transcriptional activation by altering the recruitment of c-Fos and c-Jun to estrogen-responsive promoters. Mol Endocrinol 20:534–543PubMedCrossRefGoogle Scholar
  165. McClain MA, Gatson NN, Powell ND, Papenfuss TL, Gienapp IE, Song F, Shawler TM, Kithcart A, Whitacre CC (2007) Pregnancy suppresses experimental autoimmune encephalomyelitis through immunoregulatory cytokine production. J Immunol 179:8146–8152PubMedGoogle Scholar
  166. McDonnell DP (2004) The molecular determinants of estrogen receptor pharmacology. Maturitas 48(Suppl 1):S7–S12PubMedCrossRefGoogle Scholar
  167. McEwan IJ (2004) Molecular mechanisms of androgen receptor-mediated gene regulation: structure-function analysis of the AF-1 domain. Endocr Relat Cancer 11:281–293PubMedCrossRefGoogle Scholar
  168. McKay LI, Cidlowski JA (1999) Molecular control of immune/inflammatory responses: interactions between nuclear factor-kappa B and steroid receptor-signaling pathways. Endocr Rev 20:435–59PubMedCrossRefGoogle Scholar
  169. Medina KL, Kincade PW (1994) Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc Natl Acad Sci USA 91:5382–536PubMedCrossRefGoogle Scholar
  170. Medina KL, Strasser A, Kincade PW (2000) Estrogen influences the differentiation, proliferation, and survival of early B-lineage precursors. Blood 95:2059–267PubMedGoogle Scholar
  171. Medina KL, Garrett KP, Thompson LF, Rossi MI, Payne KJ, Kincade PW (2001) Identification of very early lymphoid precursors in bone marrow and their regulation by estrogen. Nat Immunol 2:718–24PubMedCrossRefGoogle Scholar
  172. Mendel CM (1989) The free hormone hypothesis: a physiologically based mathematical model. Endocr Rev 10:232–274PubMedCrossRefGoogle Scholar
  173. Meyer ME, Pornon A, Ji JW, Bocquel MT, Chambon P, Gronemeyer H (1990) Agonistic and antagonistic activities of RU486 on the functions of the human progesterone receptor. EMBO J 9:3923–3932PubMedGoogle Scholar
  174. Meyer C, Schmid R, Scriba PC, Wehling M (1996) Purification and partial sequencing of high-affinity progesterone-binding site(s) from porcine liver membranes. Eur J Biochem 239:726–731PubMedCrossRefGoogle Scholar
  175. Michels G, Hoppe UC (2008) Rapid actions of androgens. Front Neuroendocrinol 29:182–198PubMedCrossRefGoogle Scholar
  176. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018PubMedCrossRefGoogle Scholar
  177. Mor G, Sapi E, Abrahams VM, Rutherford T, Song J, Hao XY, Muzaffar S, Kohen F (2003) Interaction of the estrogen receptors with the Fas ligand promoter in human monocytes. J Immunol 170:114–122PubMedGoogle Scholar
  178. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM (2000) Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289:1751–1754PubMedCrossRefGoogle Scholar
  179. Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM (2003) Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci USA 100:9744–9749PubMedCrossRefGoogle Scholar
  180. Nakajima Y, DelliPizzi AM, Mallouh C, Ferreri NR (1996) TNF-mediated cytotoxicity and resistance in human prostate cancer cell lines. Prostate 29:296–302PubMedCrossRefGoogle Scholar
  181. Nakamura T, Imai Y, Matsumoto T, Sato S, Takeuchi K, Igarashi K, Harada Y, Azuma Y, Krust A, Yamamoto Y, Nishina H, Takeda S, Takayanagi H, Metzger D, Kanno J, Takaoka K, Martin TJ, Chambon P, Kato S (2007) Estrogen Prevents Bone Loss via Estrogen Receptor alpha and Induction of Fas Ligand in Osteoclasts. Cell 130:811–823PubMedCrossRefGoogle Scholar
  182. Nakhla AM, Leonard J, Hryb DJ, Rosner W (1999) Sex hormone-binding globulin receptor signal transduction proceeds via a G protein. Steroids 64:213–216PubMedCrossRefGoogle Scholar
  183. Nalbandian G, Kovats S (2005) Understanding sex biases in immunity: effects of estrogen on the differentiation and function of antigen-presenting cells. Immunol Res 31:91–106PubMedCrossRefGoogle Scholar
  184. Nalbandian G, Paharkova-Vatchkova V, Mao A, Nale S, Kovats S (2005) The selective estrogen receptor modulators, tamoxifen and raloxifene, impair dendritic cell differentiation and activation. J Immunol 175:2666–2675PubMedGoogle Scholar
  185. Nazareth LV, Weigel NL (1996) Activation of the human androgen receptor through a protein kinase A signaling pathway. J Biol Chem 271:19900–19907PubMedCrossRefGoogle Scholar
  186. Oettel M (2003) Testosterone metabolism, dose-response relationships and receptor polymorphisms: selected pharmacological/toxicological considerations on benefits versus risks of testosterone therapy in men. Aging Male 6:230–256PubMedCrossRefGoogle Scholar
  187. Oettel M, Mukhopadhyay AK (2004) Progesterone: the forgotten hormone in men? Aging Male 7:236–257PubMedCrossRefGoogle Scholar
  188. O’Lone R, Frith MC, Karlsson EK, Hansen U (2004) Genomic targets of nuclear estrogen receptors. Mol Endocrinol 18:1859–1875PubMedCrossRefGoogle Scholar
  189. Olsen NJ, Kovacs WJ (2001) Effects of androgens on T and B lymphocyte development. Immunol Res 23:281–288PubMedCrossRefGoogle Scholar
  190. Olsen NJ, Watson MB, Henderson GS, Kovacs WJ (1991) Androgen deprivation induces phenotypic and functional changes in the thymus of adult male mice. Endocrinology 129:2471–2476PubMedCrossRefGoogle Scholar
  191. Olsen NJ, Viselli SM, Fan J, Kovacs WJ (1998) Androgens accelerate thymocyte apoptosis. Endocrinology 139:748–752PubMedCrossRefGoogle Scholar
  192. Olsen NJ, Gu X, Kovacs WJ (2001a) Bone marrow stromal cells mediate androgenic suppression of B lymphocyte development. J Clin Invest 108:1697–1704PubMedGoogle Scholar
  193. Olsen NJ, Olson G, Viselli SM, Gu X, Kovacs WJ (2001b) Androgen receptors in thymic epithelium modulate thymus size and thymocyte development. Endocrinology 142:1278–1283PubMedCrossRefGoogle Scholar
  194. Paharkova-Vatchkova V, Maldonado R, Kovats S (2004) Estrogen preferentially promotes the differentiation of CD11c + CD11b(intermediate) dendritic cells from bone marrow precursors. J Immunol 172:1426–1436PubMedGoogle Scholar
  195. Palvimo JJ, Reinikainen P, Ikonen T, Kallio PJ, Moilanen A, Janne OA (1996) Mutual transcriptional interference between RelA and androgen receptor. J Biol Chem 271:24151–24156PubMedCrossRefGoogle Scholar
  196. Pedram A, Razandi M, Sainson RC, Kim JK, Hughes CC, Levin ER (2007) A conserved mechanism for steroid receptor translocation to the plasma membrane. J Biol Chem 282:22278–22288PubMedCrossRefGoogle Scholar
  197. Pelayo R, Welner R, Perry SS, Huang J, Baba Y, Yokota T, Kincade PW (2005) Lymphoid progenitors and primary routes to becoming cells of the immune system. Curr Opin Immunol 17:100–107PubMedCrossRefGoogle Scholar
  198. Pernis AB (2007) Estrogen and CD4+ T cells. Curr Opin Rheumatol 19:414–420PubMedCrossRefGoogle Scholar
  199. Peterziel H, Mink S, Schonert A, Becker M, Klocker H, Cato AC (1999) Rapid signalling by androgen receptor in prostate cancer cells. Oncogene 18:6322–6329PubMedCrossRefGoogle Scholar
  200. Phiel KL, Henderson RA, Adelman SJ, Elloso MM (2005) Differential estrogen receptor gene expression in human peripheral blood mononuclear cell populations. Immunol Lett 97:107–113PubMedCrossRefGoogle Scholar
  201. Polanczyk M, Zamora A, Subramanian S, Matejuk A, Hess DL, Blankenhorn EP, Teuscher C, Vandenbark AA, Offner H (2003) The protective effect of 17beta-estradiol on experimental autoimmune encephalomyelitis is mediated through estrogen receptor-alpha. Am J Pathol 163:1599–1605PubMedGoogle Scholar
  202. Polanczyk M, Yellayi S, Zamora A, Subramanian S, Tovey M, Vandenbark AA, Offner H, Zachary JF, Fillmore PD, Blankenhorn EP, Gustafsson JA, Teuscher C (2004) Estrogen receptor-1 (Esr1) and -2 (Esr2) regulate the severity of clinical experimental allergic encephalomyelitis in male mice. Am J Pathol 164:1915–1924PubMedGoogle Scholar
  203. Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306–360PubMedCrossRefGoogle Scholar
  204. Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, Hathaway HJ (2008) Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 70:165–190PubMedCrossRefGoogle Scholar
  205. Qiu M, Lange CA (2003) MAP kinases couple multiple functions of human progesterone receptors: degradation, transcriptional synergy, and nuclear association. J Steroid Biochem Mol Biol 85:147–157PubMedCrossRefGoogle Scholar
  206. Qiu M, Olsen A, Faivre E, Horwitz KB, Lange CA (2003) Mitogen-activated protein kinase regulates nuclear association of human progesterone receptors. Mol Endocrinol 17:628–642PubMedCrossRefGoogle Scholar
  207. Radojevic K, Arsenovic-Ranin N, Kosec D, Pesic V, Pilipovic I, Perisic M, Plecas-Solarovic B, Leposavic G (2007) Neonatal castration affects intrathymic kinetics of T-cell differentiation and the spleen T-cell level. J Endocrinol 192:669–682PubMedCrossRefGoogle Scholar
  208. Rao KV, Peralta WD, Greene GL, Fox CF (1987) Cellular progesterone receptor phosphorylation in response to ligands activating protein kinases. Biochem Biophys Res Commun 146:1357–1365PubMedCrossRefGoogle Scholar
  209. Ren MQ, Kuhn G, Wegner J, Chen J (2001) Isoflavones, substances with multi-biological and clinical properties. Eur J Nutr 40:135–146PubMedCrossRefGoogle Scholar
  210. Rosner W, Hryb DJ, Khan MS, Nakhla AM, Romas NA (1999) Androgen and estrogen signaling at the cell membrane via G-proteins and cyclic adenosine monophosphate. Steroids 64:100–106PubMedCrossRefGoogle Scholar
  211. Roubenoff R, Grinspoon S, Skolnik PR, Tchetgen E, Abad L, Spiegelman D, Knox T, Gorbach S (2002) Role of cytokines and testosterone in regulating lean body mass and resting energy expenditure in HIV-infected men. Am J Physiol Endocrinol Metab 283:E138–45PubMedGoogle Scholar
  212. Russell DW, Berman DM, Bryant JT, Cala KM, Davis DL, Landrum CP, Prihoda JS, Silver RI, Thigpen AE, Wigley WC (1994) The molecular genetics of steroid 5 alpha-reductases. Recent Prog Horm Res 49:275–284PubMedGoogle Scholar
  213. Sader MA, McGrath KC, Hill MD, Bradstock KF, Jimenez M, Handelsman DJ, Celermajer DS, Death AK (2005) Androgen receptor gene expression in leucocytes is hormonally regulated: implications for gender differences in disease pathogenesis. Clin Endocrinol (Oxf) 62:56–63CrossRefGoogle Scholar
  214. Saino N, Bolzern AM, Moller AP (1997) Immunocompetence, ornamentation, and viability of male barn swallows (Hirundo rustica). Proc Natl Acad Sci USA 94:549–552PubMedCrossRefGoogle Scholar
  215. Sartorius CA, Melville MY, Hovland AR, Tung L, Takimoto GS, Horwitz KB (1994) A third transactivation function (AF3) of human progesterone receptors located in the unique N-terminal segment of the B-isoform. Mol Endocrinol 8:1347–1360PubMedCrossRefGoogle Scholar
  216. Schulman C, Lunenfeld B (2002) The ageing male. World J Urol 20:4–10PubMedCrossRefGoogle Scholar
  217. Schuurs AH, Verheul HA (1990) Effects of gender and sex steroids on the immune response. J Steroid Biochem 35:157–172PubMedCrossRefGoogle Scholar
  218. Selman PJ, Mol JA, Rutteman GR, van Garderen E, Rijnberk A (1994) Progestin-induced growth hormone excess in the dog originates in the mammary gland. Endocrinology 134:287–292PubMedCrossRefGoogle Scholar
  219. Shang Y, Brown M (2002) Molecular determinants for the tissue specificity of SERMs. Science 295:2465–248PubMedCrossRefGoogle Scholar
  220. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M (2000) Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843–852PubMedCrossRefGoogle Scholar
  221. Shang Y, Myers M, Brown M (2002) Formation of the androgen receptor transcription complex. Mol Cell 9:601–610PubMedCrossRefGoogle Scholar
  222. Shim GJ, Wang L, Andersson S, Nagy N, Kis LL, Zhang Q, Makela S, Warner M, Gustafsson JA (2003) Disruption of the estrogen receptor beta gene in mice causes myeloproliferative disease resembling chronic myeloid leukemia with lymphoid blast crisis. Proc Natl Acad Sci USA 100:6694–6699PubMedCrossRefGoogle Scholar
  223. Shim GJ, Kis LL, Warner M, Gustafsson JA (2004) Autoimmune glomerulonephritis with spontaneous formation of splenic germinal centers in mice lacking the estrogen receptor alpha gene. Proc Natl Acad Sci USA 101:1720–1724PubMedCrossRefGoogle Scholar
  224. Shortman K, Naik SH (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7:19–30PubMedCrossRefGoogle Scholar
  225. Shuai K, Liu B (2005) Regulation of gene-activation pathways by PIAS proteins in the immune system. Nat Rev Immunol 5:593–605PubMedCrossRefGoogle Scholar
  226. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK (2000) Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538–541PubMedCrossRefGoogle Scholar
  227. Singh AB, Hsia S, Alaupovic P, Sinha-Hikim I, Woodhouse L, Buchanan TA, Shen R, Bross R, Berman N, Bhasin S (2002) The effects of varying doses of T on insulin sensitivity, plasma lipids, apolipoproteins, and C-reactive protein in healthy young men. J Clin Endocrinol Metab 87:136–143PubMedCrossRefGoogle Scholar
  228. Sinkevicius KW, Burdette JE, Woloszyn K, Hewitt SC, Hamilton K, Sugg SL, Temple KA, Wondisford FE, Korach KS, Woodruff TK, Greene GL (2008) An estrogen receptor-alpha knock-in mutation provides evidence of ligand-independent signaling and allows modulation of ligand-induced pathways in vivo. Endocrinology 149:2970–2979PubMedCrossRefGoogle Scholar
  229. Siracusa MC, Overstreet MG, Housseau F, Scott AL, Klein SL (2008) 17{beta}-Estradiol Alters the Activity of Conventional and IFN-Producing Killer Dendritic Cells. J Immunol 180:1423–1431PubMedGoogle Scholar
  230. Smith CL, O’Malley BW (2004) Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr Rev 25:45–71PubMedCrossRefGoogle Scholar
  231. Smithson G, Beamer WG, Shultz KL, Christianson SW, Shultz LD, Kincade PW (1994) Increased B lymphopoiesis in genetically sex steroid-deficient hypogonadal (hpg) mice. J Exp Med 180:717–20PubMedCrossRefGoogle Scholar
  232. Smithson G, Couse JF, Lubahn DB, Korach KS, Kincade PW (1998) The role of estrogen receptors and androgen receptors in sex steroid regulation of B lymphopoiesis. J Immunol 161:27–34PubMedGoogle Scholar
  233. Sobel ES, Gianini J, Butfiloski EJ, Croker BP, Schiffenbauer J, Roberts SM (2005) Acceleration of autoimmunity by organochlorine pesticides in (NZB x NZW)F1 mice. Environ Health Perspect 113:323–328PubMedCrossRefGoogle Scholar
  234. Soucy G, Boivin G, Labrie F, Rivest S (2005) Estradiol is required for a proper immune response to bacterial and viral pathogens in the female brain. J Immunol 174:6391–6398PubMedGoogle Scholar
  235. Sperry TS, Thomas P (1999) Characterization of two nuclear androgen receptors in Atlantic croaker: comparison of their biochemical properties and binding specificities. Endocrinology 140:1602–1611PubMedCrossRefGoogle Scholar
  236. Spitz IM (2003) Progesterone antagonists and progesterone receptor modulators: an overview. Steroids 68:981–993PubMedCrossRefGoogle Scholar
  237. Spitz IM (2006) Progesterone receptor antagonists. Curr Opin Investig Drugs 7:882–890PubMedGoogle Scholar
  238. Staples JE, Gasiewicz TA, Fiore NC, Lubahn DB, Korach KS, Silverstone AE (1999) Estrogen receptor alpha is necessary in thymic development and estradiol-induced thymic alterations. J Immunol 163:4168–4174PubMedGoogle Scholar
  239. Sthoeger ZM, Zinger H, Mozes E (2003) Beneficial effects of the anti-oestrogen tamoxifen on systemic lupus erythematosus of (NZBxNZW)F1 female mice are associated with specific reduction of IgG3 autoantibodies. Ann Rheum Dis 62:341–346PubMedCrossRefGoogle Scholar
  240. Stites DP, Siiteri PK (1983) Steroids as immunosuppressants in pregnancy. Immunol Rev 75:117–138PubMedCrossRefGoogle Scholar
  241. Stossi F, Barnett DH, Frasor J, Komm B, Lyttle CR, Katzenellenbogen BS (2004) Transcriptional profiling of estrogen-regulated gene expression via estrogen receptor (ER) alpha or ERbeta in human osteosarcoma cells: distinct and common target genes for these receptors. Endocrinology 145:3473–3486PubMedCrossRefGoogle Scholar
  242. Straub RH (2007) The complex role of estrogens in inflammation. Endocr Rev 28:521–574PubMedCrossRefGoogle Scholar
  243. Subramanian M, Shaha C (2007) Up-regulation of Bcl-2 through ERK phosphorylation is associated with human macrophage survival in an estrogen microenvironment. J Immunol 179:2330–2338PubMedGoogle Scholar
  244. Suh J, Payvandi F, Edelstein LC, Amenta PS, Zong WX, Gelinas C, Rabson AB (2002) Mechanisms of constitutive NF-kappaB activation in human prostate cancer cells. Prostate 52:183–200PubMedCrossRefGoogle Scholar
  245. Supakar PC, Jung MH, Song CS, Chatterjee B, Roy AK (1995) Nuclear factor kappa B functions as a negative regulator for the rat androgen receptor gene and NF-kappa B activity increases during the age-dependent desensitization of the liver. J Biol Chem The Journal of biological chemistry 270:837–842Google Scholar
  246. Sutherland JS, Goldberg GL, Hammett MV, Uldrich AP, Berzins SP, Heng TS, Blazar BR, Millar JL, Malin MA, Chidgey AP, Boyd RL (2005) Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol 175:2741–2753Google Scholar
  247. Szekeres-Bartho J, Szekeres G, Debre P, Autran B, Chaouat G (1990) Reactivity of lymphocytes to a progesterone receptor-specific monoclonal antibody. Cell Immunol 125:273–283PubMedCrossRefGoogle Scholar
  248. Takahashi T, Eitzman B, Bossert NL, Walmer D, Sparrow K, Flanders KC, McLachlan J, Nelson KG (1994) Transforming growth factors beta 1, beta 2, and beta 3 messenger RNA and protein expression in mouse uterus and vagina during estrogen-induced growth: a comparison to other estrogen-regulated genes. Cell Growth Differ 5:919–935PubMedGoogle Scholar
  249. Takeda H, Chodak G, Mutchnik S, Nakamoto T, Chang C (1990) Immunohistochemical localization of androgen receptors with mono- and polyclonal antibodies to androgen receptor. J Endocrinol 126:17–25PubMedCrossRefGoogle Scholar
  250. Takeo J, Yamashita S (1999) Two distinct isoforms of cDNA encoding rainbow trout androgen receptors. J Biol Chem 274:5674–5680PubMedCrossRefGoogle Scholar
  251. Taniguchi F, Couse JF, Rodriguez KF, Emmen JM, Poirier D, Korach KS (2007) Estrogen receptor-alpha mediates an intraovarian negative feedback loop on thecal cell steroidogenesis via modulation of Cyp17a1 (cytochrome P450, steroid 17alpha-hydroxylase/17, 20 lyase) expression. FASEB J 21:586–595PubMedCrossRefGoogle Scholar
  252. Thomas P (2008) Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front Neuroendocrinol 29:292–312PubMedCrossRefGoogle Scholar
  253. Thurmond TS, Murante FG, Staples JE, Silverstone AE, Korach KS, Gasiewicz TA (2000) Role of estrogen receptor alpha in hematopoietic stem cell development and B lymphocyte maturation in the male mouse. Endocrinology 141:2309–2318PubMedCrossRefGoogle Scholar
  254. Tibbetts TA, Conneely OM, O’Malley BW (1999) Progesterone via its receptor antagonizes the pro-inflammatory activity of estrogen in the mouse uterus. Biol Reprod 60:1158–1165PubMedCrossRefGoogle Scholar
  255. Tilley WD, Marcelli M, Wilson JD, McPhaul MJ (1989) Characterization and expression of a cDNA encoding the human androgen receptor. Proc Natl Acad Sci USA 86:327–331PubMedCrossRefGoogle Scholar
  256. Trapman J, Klaassen P, Kuiper GG, van der Korput JA, Faber PW, van Rooij HC, Geurts van Kessel A, Voorhorst MM, Mulder E, Brinkmann AO (1988) Cloning, structure and expression of a cDNA encoding the human androgen receptor. Biochem Biophys Res Commun 153:241–248PubMedCrossRefGoogle Scholar
  257. Tseng L, Tang M, Wang Z, Mazella J (2003) Progesterone receptor (hPR) upregulates the fibronectin promoter activity in human decidual fibroblasts. DNA Cell Biol 22:633–640PubMedCrossRefGoogle Scholar
  258. Ueda T, Bruchovsky N, Sadar MD (2002) Activation of the androgen receptor N-terminal domain by interleukin-6 via MAPK and STAT3 signal transduction pathways. J Biol Chem 277:7076–7085PubMedCrossRefGoogle Scholar
  259. Vegeto E, Pollio G, Pellicciari C, Maggi A (1999) Estrogen and progesterone induction of survival of monoblastoid cells undergoing TNF-alpha-induced apoptosis. FASEB J 13:793–803PubMedGoogle Scholar
  260. Vicencio JM, Ibarra C, Estrada M, Chiong M, Soto D, Parra V, Diaz-Araya G, Jaimovich E, Lavandero S (2006) Testosterone induces an intracellular calcium increase by a nongenomic mechanism in cultured rat cardiac myocytes. Endocrinology 147:1386–1395PubMedCrossRefGoogle Scholar
  261. Viselli SM, Olsen NJ, Shults K, Steizer G, Kovacs WJ (1995) Immunochemical and flow cytometric analysis of androgen receptor expression in thymocytes. Mol Cell Endocrinol 109:19–26PubMedCrossRefGoogle Scholar
  262. Viselli SM, Reese KR, Fan J, Kovacs WJ, Olsen NJ (1997) Androgens alter B cell development in normal male mice. Cell Immunol 182:99–104PubMedCrossRefGoogle Scholar
  263. Walker WH, Cheng J (2005) FSH and testosterone signaling in Sertoli cells. Reproduction 130:15–28PubMedCrossRefGoogle Scholar
  264. Walmer DK, Wrona MA, Hughes CL, Nelson KG (1992) Lactoferrin expression in the mouse reproductive tract during the natural estrous cycle: correlation with circulating estradiol and progesterone. Endocrinology 131:1458–1466PubMedCrossRefGoogle Scholar
  265. Wang LH, Yang XY, Mihalic K, Xiao W, Li D, Farrar WL (2001) Activation of estrogen receptor blocks interleukin-6-inducible cell growth of human multiple myeloma involving molecular cross-talk between estrogen receptor and STAT3 mediated by co-regulator PIAS3. J Biol Chem 276:31839–31844PubMedCrossRefGoogle Scholar
  266. Wang F, Roberts SM, Butfiloski EJ, Morel L, Sobel ES (2007) Acceleration of autoimmunity by organochlorine pesticides: a comparison of splenic B-cell effects of chlordecone and estradiol in (NZBxNZW)F1 mice. Toxicol Sci 99:141–152PubMedCrossRefGoogle Scholar
  267. Warner M, Gustafsson JA (2006) Nongenomic effects of estrogen: why all the uncertainty? Steroids 71:91–95PubMedCrossRefGoogle Scholar
  268. Welner RS, Pelayo R, Garrett KP, Chen X, Perry SS, Sun XH, Kee BL, Kincade PW (2007) Interferon-producing killer dendritic cells (IKDCs) arise via a unique differentiation pathway from primitive c-kitHiCD62L + lymphoid progenitors. Blood 109:4825–4931PubMedCrossRefGoogle Scholar
  269. Whitacre CC, Reingold SC, O’Looney PA (1999) A gender gap in autoimmunity. Science 283:1277–1278PubMedCrossRefGoogle Scholar
  270. Williams C, Edvardsson K, Lewandowski SA, Strom A, Gustafsson JA (2008) A genome-wide study of the repressive effects of estrogen receptor beta on estrogen receptor alpha signaling in breast cancer cells. Oncogene 27:1019–1032PubMedCrossRefGoogle Scholar
  271. Wilson CM, McPhaul MJ (1994) A and B forms of the androgen receptor are present in human genital skin fibroblasts. Proc Natl Acad Sci USA 91:1234–1238PubMedCrossRefGoogle Scholar
  272. Wilson CA, Mrose SA, Thomas DW (1995) Enhanced production of B lymphocytes after castration. Blood Blood 85:1535–1539Google Scholar
  273. Windmill KF, Meade BJ, Lee VW (1993) Effect of prepubertal gonadectomy and sex steroid treatment on the growth and lymphocyte populations of the rat thymus. Reprod Fertil Dev 5:73–81PubMedCrossRefGoogle Scholar
  274. Winneker RC, Fensome A, Wrobel JE, Zhang Z, Zhang P (2005) Nonsteroidal progesterone receptor modulators: structure activity relationships. Semin Reprod Med 23:46–57PubMedCrossRefGoogle Scholar
  275. Wunderlich F, Benten WP, Lieberherr M, Guo Z, Stamm O, Wrehlke C, Sekeris CE, Mossmann H (2002) Testosterone signaling in T cells and macrophages. Steroids 67:535–538PubMedCrossRefGoogle Scholar
  276. Yamamoto T, Matsuda T, Junicho A, Kishi H, Saatcioglu F, Muraguchi A (2000) Cross-talk between signal transducer and activator of transcription 3 and estrogen receptor signaling. FEBS Lett 486:143–148PubMedCrossRefGoogle Scholar
  277. Yamamoto T, Sato N, Sekine Y, Yumioka T, Imoto S, Junicho A, Fuse H, Matsuda T (2003) Molecular interactions between STAT3 and protein inhibitor of activated STAT3, and androgen receptor. Biochem Biophys Res Commun 306:610–615PubMedCrossRefGoogle Scholar
  278. Yao M, Nguyen TV, Pike CJ (2007) Estrogen regulates Bcl-w and Bim expression: role in protection against beta-amyloid peptide-induced neuronal death. J Neurosci 27:1422–1433PubMedCrossRefGoogle Scholar
  279. Yeh S, Tsai MY, Xu Q, Mu XM, Lardy H, Huang KE, Lin H, Yeh SD, Altuwaijri S, Zhou X, Xing L, Boyce BF, Hung MC, Zhang S, Gan L, Chang C (2002) Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci USA 99:13498–13503PubMedCrossRefGoogle Scholar
  280. Zhang Y, Beck CA, Poletti A, Edwards DP, Weigel NL (1995) Identification of a group of Ser-Pro motif hormone-inducible phosphorylation sites in the human progesterone receptor. Mol Endocrinol 9:1029–1040PubMedCrossRefGoogle Scholar
  281. Zhou ZX, Sar M, Simental JA, Lane MV, Wilson EM (1994) A ligand-dependent bipartite nuclear targeting signal in the human androgen receptor. Requirement for the DNA-binding domain and modulation by NH2-terminal and carboxyl-terminal sequences. J Biol Chem 269:13115–13123PubMedGoogle Scholar
  282. Zhu Y, Rice CD, Pang Y, Pace M, Thomas P (2003) Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc Natl Acad Sci USA 100:2231–2236PubMedCrossRefGoogle Scholar
  283. Zoller AL, Kersh GJ (2006) Estrogen induces thymic atrophy by eliminating early thymic progenitors and inhibiting proliferation of beta-selected thymocytes. J Immunol 176:7371–7378PubMedGoogle Scholar
  284. Zoller AL, Schnell FJ, Kersh GJ (2007) Murine pregnancy leads to reduced proliferation of maternal thymocytes and decreased thymic emigration. Immunology 121:207–215PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Arthritis and Immunology Research ProgramOklahoma Medical Research FoundationOklahoma CityUSA

Personalised recommendations