Sex steroids as inflammatory regulators

Journal of Steroid Biochemistry and Molecular Biology

Volumn 120, Issue 2-3, 2010, Pages 105-115

  Gilliver, Stephen C ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Atherosclerosis; Inflammation; Sex steroids; Wound healing

Indexed keywords

ANDROGEN; CONJUGATED ESTROGEN; CONJUGATED ESTROGEN PLUS MEDROXYPROGESTERONE ACETATE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FLUTAMIDE; GESTAGEN; LEVONORGESTREL; MEDROXYPROGESTERONE; MEDROXYPROGESTERONE ACETATE; NORETHISTERONE; NORETHISTERONE ACETATE; PROGESTERONE; SEX HORMONE; STEROID 5ALPHA REDUCTASE INHIBITOR; TESTOSTERONE UNDECANOATE;

ARTICLE; CELL FUNCTION; CLINICAL TRIAL; DIABETIC FOOT; DNA POLYMORPHISM; HUMAN; INFLAMMATION; INFLAMMATORY CELL; INFLAMMATORY DISEASE; MACROPHAGE; MEDIATOR RELEASE; MENOPAUSE; NONHUMAN; RECEPTOR GENE; WOUND HEALING;

EID: 77952955740     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2009.12.015     Document Type: Review

References (188)

1. Offner P.J., Moore E.E., Biffl W.L. Male gender is a risk factor for major infections after surgery. Arch. Surg. 1999, 134(9):935-938.
2. Verthelyi D. Sex hormones as immunomodulators in health and disease. Int. Immunopharmacol. 2001, 1(6):983-993.
3. Enosawa S., Hirasawa K. Sex-associated differences in the survival of skin grafts in rats. Enhancement of cyclosporine immunosuppression in male compared with female recipients. Transplantation 1989, 47(6):933-937.
4. McCashland T.M., Brand R., Lyden E., de Garmo P.P. Gender differences in colorectal polyps and tumors. Am. J. Gastroenterol. 2001, 96(3):882-886.
5. Woldrich J.M., Mallin K., Ritchey J., Carroll P.R., Kane C.J. Sex differences in renal cell cancer presentation and survival: an analysis of the National Cancer Database, 1993-2004. J. Urol. 2008, 179(5):1709-1713.
6. Bosch F.X., Ribes J., Díaz M., Cléries R. Primary liver cancer: worldwide incidence and trends. Gastroenterology 2004, 127(5 Suppl. 1):S5-S16.
7. Koçar I.H., Yesilova Z., Ozata M., Turan M., Sengül A., Ozdemir I. The effect of testosterone replacement treatment on immunological features of patients with Klinefelter's syndrome. Clin. Exp. Immunol. 2000, 121(3):448-452.
8. Nikolaevich K.N., Ivanovich S.J., Victorovich S.S. Major reproduction hormones as regulators of cell-to-cell interactions in humoral immune responses. Brain Behav. Immun. 1991, 5(2):149-161.
9. Beynon H.L., Garbett N.D., Barnes P.J. Severe premenstrual exacerbations of asthma: effect of intramuscular progesterone. Lancet 1988, 2(8607):370-372.
10. Malkin C.J., Pugh P.J., Jones R.D., Jones T.H., Channer K.S. Testosterone as a protective factor against atherosclerosis-immunomodulation and influence upon plaque development and stability. J. Endocrinol. 2003, 178(3):373-380.
11. Mikkola T.S., Clarkson T.B. Estrogen replacement therapy, atherosclerosis, and vascular function. Cardiovasc. Res. 2002, 53(3):605-619.
12. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28(5):521-574.
13. Feldman H.A., Longcope C., Derby C.A., Johannes C.B., Araujo A.B., Coviello A.D., Bremner W.J., McKinlay J.B. Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J. Clin. Endocrinol. Metab. 2002, 87(2):589-598.
14. Benten W.P., Lieberherr M., Stamm O., Wrehlke C., Guo Z., Wunderlich F. Testosterone signaling through internalizable surface receptors in androgen receptor-free macrophages. Mol. Biol. Cell 1999, 10(10):3113-3123.
15. Benten W.P., Becker A., Schmitt-Wrede H.P., Wunderlich F. Developmental regulation of intracellular and surface androgen receptors in T cells. Steroids 2002, 67(11):925-931.
16. Aerts J.L., Christiaens M.R., Vandekerckhove P. Evaluation of progesterone receptor expression in eosinophils using real-time quantitative PCR. Biochim. Biophys. Acta 2002, 1571(3):167-172.
17. Molloy E.J., O'Neill A.J., Grantham J.J., Sheridan-Pereira M., Fitzpatrick J.M., Webb D.W., Watson R.W. Sex-specific alterations in neutrophil apoptosis: the role of estradiol and progesterone. Blood 2003, 102(7):2653-2659.
18. Békési G., Kakucs R., Várbíró S., Rácz K., Sprintz D., Fehér J., Székács B. In vitro effects of different steroid hormones on superoxide anion production of human neutrophil granulocytes. Steroids 2000, 65(12):889-894.
19. Chiang K., Parthasarathy S., Santanam N. Estrogen, neutrophils and oxidation. Life Sci. 2004, 75(20):2425-2438.
20. Bekesi G., Tulassay Z., Racz K., Feher J., Szekacs B., Kakucs R., Dinya E., Riss E., Magyar Z., Rigo J. The effect of estrogens on superoxide anion generation by human neutrophil granulocytes: possible consequences of the antioxidant defense. Gynecol. Endocrinol. 2007, 23(8):451-454.
21. García-Durán M., de Frutos T., Díaz-Recasens J., García-Gálvez G., Jiménez A., Montón M., Farré J., Sánchez de Miguel L., González-Fernández F., Arriero M.D., Rico L., García R., Casado S., López-Farré A. Estrogen stimulates neuronal nitric oxide synthase protein expression in human neutrophils. Circ. Res. 1999, 85(11):1020-1026.
22. Durán M.G., Gálvez G.G., de Frutos T., Díaz Recaséns J., Casado S., López Farré A. 17β-Estradiol-stimulated nitric oxide production by neutrophils: effect on platelet activation. Obstet. Gynecol. 2000, 95(2):284-290.
23. Martinoli C., Zocchi E., Querzola F., Damiani G., Zaccheo D. Progesterone enhances reactive oxygen intermediates production by cultured human monocytes. Boll. Soc. Ital. Biol. Sper. 1984, 60(10):1871-1877.
24. Jain S.K., Kannan K., Prouty L., Jain S.K. Progesterone, but not 17β-estradiol, increases TNF-α secretion in U937 monocytes. Cytokine 2004, 26(3):102-105.
25. Peltier M.R., Tee S.C., Smulian J.C. Effect of progesterone on proinflammatory cytokine production by monocytes stimulated with pathogens associated with preterm birth. Am. J. Reprod. Immunol. 2008, 60(4):346-353.
26. Morishita M., Miyagi M., Iwamoto Y.Y. Effects of sex hormones on production of interleukin-1 by human peripheral monocytes. J. Periodontol. 1999, 70(7):757-760.
27. Miyagi M., Morishita M., Iwamoto Y. Effects of sex hormones on production of prostaglandin E2 by human peripheral monocytes. J. Periodontol. 1993, 64(11):1075-1078.
28. Pioli P.A., Jensen A.L., Weaver L.K., Amiel E., Shen Z., Shen L., Wira C.R., Guyre P.M. Estradiol attenuates lipopolysaccharide-induced CXC chemokine ligand 8 production by human peripheral blood monocytes. J. Immunol. 2007, 179(9):6284-6290.
29. Yamada K., Hayashi T., Kuzuya M., Naito M., Asai K., Iguchi A. Physiological concentration of 17β-estradiol inhibits chemotaxis of human monocytes in response to monocyte chemotactic protein 1. Artery 1996, 22(1):24-35.
30. Janis K., Hoeltke J., Nazareth M., Fanti P., Poppenberg K., Aronica S.M. Estrogen decreases expression of chemokine receptors, and suppresses chemokine bioactivity in murine monocytes. Am. J. Reprod. Immunol. 2004, 51(1):22-31.
31. Friedrich E.B., Clever Y.P., Wassmann S., Hess C., Nickenig G. 17β-estradiol inhibits monocyte adhesion via down-regulation of Rac1 GTPase. J. Mol. Cell. Cardiol. 2006, 40(1):87-95.
32. Schneider C.P., Schwacha M.G., Samy T.S., Bland K.I., Chaudry I.H. Androgen-mediated modulation of macrophage function after trauma-hemorrhage: central role of 5α-dihydrotestosterone. J. Appl. Physiol. 2003, 95(1):104-112.
33. Chao T.C., Van Alten P.J., Walter R.J. Steroid sex hormones and macrophage function: modulation of reactive oxygen intermediates and nitrite release. Am. J. Reprod. Immunol. 1994, 32(1):43-52.
34. Robert R., Spitzer J.A. Effects of female hormones (17β-estradiol and progesterone) on nitric oxide production by alveolar macrophages in rats. Nitric Oxide 1997, 1(6):453-462.
35. Miller L., Alley E.W., Murphy W.J., Russell S.W., Hunt J.S. Progesterone inhibits inducible nitric oxide synthase gene expression and nitric oxide production in murine macrophages. J. Leukoc. Biol. 1996, 59(3):442-450.
36. Huang H., He J., Yuan Y., Aoyagi E., Takenaka H., Itagaki T., Sannomiya K., Tamaki K., Harada N., Shono M., Shimizu I., Takayama T. Opposing effects of estradiol and progesterone on the oxidative stress-induced production of chemokine and proinflammatory cytokines in murine peritoneal macrophages. J. Med. Invest. 2008, 55(1-2):133-141.
37. Vegeto E., Ghisletti S., Meda C., Etteri S., Belcredito S., Maggi A. Regulation of the lipopolysaccharide signal transduction pathway by 17β-estradiol in macrophage cells. J. Steroid Biochem. Mol. Biol. 2004, 91(1-2):59-66.
38. Deshpande R., Khalili H., Pergolizzi R.G., Michael S.D., Chang M.D. Estradiol down-regulates LPS-induced cytokine production and NFkB activation in murine macrophages. Am. J. Reprod. Immunol. 1997, 38(1):46-54.
39. You H.J., Kim J.Y., Jeong H.G. 17β-Estradiol increases inducible nitric oxide synthase expression in macrophages. Biochem. Biophys. Res. Commun. 2003, 303(4):1129-1134.
40. Calippe B., Douin-Echinard V., Laffargue M., Laurell H., Rana-Poussine V., Pipy B., Guéry J.C., Bayard F., Arnal J.F., Gourdy P. Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J. Immunol. 2008, 180(12):7980-7988.
41. Rettew J.A., Huet Y.M., Marriott I. Estrogens augment cell surface TLR4 expression on murine macrophages and regulate sepsis susceptibility in vivo. Endocrinology 2009, 50(8):3877-3884.
42. Katayama M.L., Federico M.H., Brentani R.R., Brentani M.M. Eosinophil accumulation in rat uterus following estradiol administration is modulated by laminin and its integrin receptors. Cell Adhes. Commun. 1998, 5(5):409-424.
43. Tchernitchin A.N., Barrera J., Arroyo P., Mena M.A., Vilches K., Grunert G. Degranulatory action of estradiol on blood eosinophil leukocytes in vivo and in vitro. Agents Actions 1985, 17(1):60-66.
44. Hamano N., Terada N., Maesako K., Numata T., Konno A. Effect of sex hormones on eosinophilic inflammation in nasal mucosa. Allergy Asthma Proc. 1998, 19(5):263-269.
45. Mayo J.C., Sáinz R.M., Antolín I., Uría H., Menéndez-Peláez A., Rodríguez C. Androgen-dependent mast cell degranulation in the Harderian gland of female Syrian hamsters: in vivo and organ culture evidence. Anat. Embryol. (Berl.) 1997, 196(2):133-140.
46. Belot M.P., Abdennebi-Najar L., Gaudin F., Lieberherr M., Godot V., Taïeb J., Emilie D., Machelon V. Progesterone reduces the migration of mast cells toward the chemokine stromal cell-derived factor-1/CXCL12 with an accompanying decrease in CXCR4 receptors. Am. J. Physiol. Endocrinol. Metab. 2007, 292(5):E1410-E1417.
47. Belot M.P., Abdennebi-Najar L., Gaudin F., Emilie D., Machelon V. Progesterone increases csk homologous kinase in HMC-1560 human mast cells and reduces cell proliferation. J. Cell. Biochem. 2007, 102(5):1271-1280.
48. Vasiadi M., Kempuraj D., Boucher W., Kalogeromitros D., Theoharides T.C. Progesterone inhibits mast cell secretion. Int. J. Immunopathol. Pharmacol. 2006, 19(4):787-794.
49. Vliagoftis H., Dimitriadou V., Theoharides T.C. Progesterone triggers selective mast cell secretion of 5-hydroxytryptamine. Int. Arch. Allergy Appl. Immunol. 1990, 93(2-3):113-119.
50. Theoharides T.C., Dimitriadou V., Letourneau R., Rozniecki J.J., Vliagoftis H., Boucher W. Synergistic action of estradiol and myelin basic protein on mast cell secretion and brain myelin changes resembling early stages of demyelination. Neuroscience 1993, 57(3):861-871.
51. Vliagoftis H., Dimitriadou V., Boucher W., Rozniecki J.J., Correia I., Raam S., Theoharides T.C. Estradiol augments while tamoxifen inhibits rat mast cell secretion. Int. Arch. Allergy Immunol. 1992, 98(4):398-409.
52. Zaitsu M., Narita S., Lambert K.C., Grady J.J., Estes D.M., Curran E.M., Brooks E.G., Watson C.S., Goldblum R.M., Midoro-Horiuti T. Estradiol activates mast cells via a non-genomic estrogen receptor-alpha and calcium influx. Mol. Immunol. 2007, 44(8):1977-1985.
53. Kim M.S., Chae H.J., Shin T.Y., Kim H.M., Kim H.R. Estrogen regulates cytokine release in human mast cells. Immunopharmacol. Immunotoxicol. 2001, 23(4):495-504.
54. Cocchiara R., Albeggiani G., Di Trapani G., Azzolina A., Lampiasi N., Rizzo F., Geraci D. Modulation of rat peritoneal mast cell and human basophil histamine release by estrogens. Int. Arch. Allergy Appl. Immunol. 1990, 93(2-3):192-197.
55. Khetawat G., Faraday N., Nealen M.L., Vijayan K.V., Bolton E., Noga S.J., Bray P.F. Human megakaryocytes and platelets contain the estrogen receptor β and androgen receptor (AR): testosterone regulates AR expression. Blood 2000, 95(7):2289-2296.
56. Moro L., Reineri S., Piranda D., Pietrapiana D., Lova P., Bertoni A., Graziani A., Defilippi P., Canobbio I., Torti M., Sinigaglia F. Nongenomic effects of 17β-estradiol in human platelets: potentiation of thrombin-induced aggregation through estrogen receptor beta and Src kinase. Blood 2005, 105(1):115-121.
57. Rosenblum W.I., el-Sabban F., Nelson G.H., Allison T.B. Effects in mice of testosterone and dihydrotestosterone on platelet aggregation in injured arterioles and ex vivo. Thromb. Res. 1987, 45(6):719-728.
58. Li S., Li X., Li J., Deng X., Li Y. Inhibition of oxidative-stress-induced platelet aggregation by androgen at physiological levels via its receptor is associated with the reduction of thromboxane A2 release from platelets. Steroids 2007, 72(13):875-880.
59. Ajayi A.A., Mathur R., Halushka P.V. Testosterone increases human platelet thromboxane A2 receptor density and aggregation responses. Circulation 1995, 91(11):2742-2747.
60. Selles J., Polini N., Alvarez C., Massheimer V. Progesterone and 17β-estradiol acutely stimulate nitric oxide synthase activity in rat aorta and inhibit platelet aggregation. Life Sci. 2001, 69(7):815-827.
61. Maccarrone M., Bari M., Battista N., Finazzi-Agrò A. Estrogen stimulates arachidonoylethanolamide release from human endothelial cells and platelet activation. Blood 2002, 100(12):4040-4048.
62. 2+-independent activation of endothelial nitric-oxide synthase/Hsp90 involving ERK1/2 and Akt phosphorylation in human endothelial cells. J. Biol. Chem. 2006, 281(37):27335-27345.
63. Toth B., Saadat G., Geller A., Scholz C., Schulze S., Friese K., Jeschke U. Human umbilical vascular endothelial cells express estrogen receptor beta (ERβ) and progesterone receptor A (PR-A), but not ERα and PR-B. Histochem. Cell Biol. 2008, 130(2):399-405.
64. Otsuki M., Saito H., Xu X., Sumitani S., Kouhara H., Kishimoto T., Kasayama S. Progesterone, but not medroxyprogesterone, inhibits vascular cell adhesion molecule-1 expression in human vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2001, 21(2):243-248.
65. Amant C., Holm P., Xu S.H., Tritman N., Kearney M., Losordo D.W. Estrogen receptor-mediated, nitric oxide-dependent modulation of the immunologic barrier function of the endothelium: regulation of fas ligand expression by estradiol. Circulation 2001, 104(21):2576-2581.
66. Alvarez A., Hermenegildo C., Issekutz A.C., Esplugues J.V., Sanz M.J. Estrogens inhibit angiotensin II-induced leukocyte-endothelial cell interactions in vivo via rapid endothelial nitric oxide synthase and cyclooxygenase activation. Circ. Res. 2002, 91(12):1142-1150.
67. Gao H., Liang M., Bergdahl A., Hamrén A., Lindholm M.W., Dahlman-Wright K., Nilsson B.O. Estrogen attenuates vascular expression of inflammation associated genes and adhesion of monocytes to endothelial cells. Inflamm. Res. 2006, 55(8):349-353.
68. Caulin-Glaser T., Watson C.A., Pardi R., Bender J.R. Effects of 17β-estradiol on cytokine-induced endothelial cell adhesion molecule expression. J. Clin. Invest. 1996, 98(1):36-42.
69. Nakai K., Itoh C., Hotta K., Itoh T., Yoshizumi M., Hiramori K. Estradiol-17β regulates the induction of VCAM-1 mRNA expression by interleukin-1β in human umbilical vein endothelial cells. Life Sci. 1994, 54(13):PL221-PL227.
70. Rodríguez E., López R., Paez A., Massó F., Montaño L.F. 17β-Estradiol inhibits the adhesion of leukocytes in TNF-α stimulated human endothelial cells by blocking IL-8 and MCP-1 secretion, but not its transcription. Life Sci. 2002, 71(18):2181-2193.
71. Seli E., Pehlivan T., Selam B., Garcia-Velasco J.A., Arici A. Estradiol down-regulates MCP-1 expression in human coronary artery endothelial cells. Fertil. Steril. 2002, 77(3):542-547.
72. Mikkola T.S., St Clair R.W. Estradiol reduces basal and cytokine induced monocyte adhesion to endothelial cells. Maturitas 2002, 41(4):313-319.
73. Geraldes P., Gagnon S., Hadjadj S., Merhi Y., Sirois M.G., Cloutier I., Tanguay J.F. Estradiol blocks the induction of CD40 and CD40L expression on endothelial cells and prevents neutrophil adhesion: an ERα-mediated pathway. Cardiovasc. Res. 2006, 71(3):566-573.
74. Cid M.C., Kleinman H.K., Grant D.S., Schnaper H.W., Fauci A.S., Hoffman G.S. Estradiol enhances leukocyte binding to tumor necrosis factor (TNF)-stimulated endothelial cells via an increase in TNF-induced adhesion molecules E-selectin, intercellular adhesion molecule type 1, and vascular cell adhesion molecule type 1. J. Clin. Invest. 1994, 93(1):17-25.
75. Death A.K., McGrath K.C., Sader M.A., Nakhla S., Jessup W., Handelsman D.J., Celermajer D.S. Dihydrotestosterone promotes vascular cell adhesion molecule-1 expression in male human endothelial cells via a nuclear factor-κB-dependent pathway. Endocrinology 2004, 145(4):1889-1897.
76. McCrohon J.A., Jessup W., Handelsman D.J., Celermajer D.S. Androgen exposure increases human monocyte adhesion to vascular endothelium and endothelial cell expression of vascular cell adhesion molecule-1. Circulation 1999, 99(17):2317-2322.
77. Norata G.D., Tibolla G., Seccomandi P.M., Poletti A., Catapano A.L. Dihydrotestosterone decreases tumor necrosis factor-α and lipopolysaccharide-induced inflammatory response in human endothelial cells. J. Clin. Endocrinol. Metab. 2006, 91(2):546-554.
78. Barton M., Cremer J., Mügge A. 17β-estradiol acutely improves endothelium-dependent relaxation to bradykinin in isolated human coronary arteries. Eur. J. Pharmacol. 1998, 362(1):73-76.
79. Rubio-Gayosso I., Garcia-Ramirez O., Gutierrez-Serdan R., Guevara-Balcazar G., Muñoz-García O., Morato-Cartajena T., Zamora-Garza M., Ceballos-Reyes G. Testosterone inhibits bradykinin-induced intracellular calcium kinetics in rat aortic endothelial cells in culture. Steroids 2002, 67(5):393-397.
80. Koh K.K., Mincemoyer R., Bui M.N., Csako G., Pucino F., Guetta V., Waclawiw M., Cannon R.O. Effects of hormone-replacement therapy on fibrinolysis in postmenopausal women. N. Engl. J. Med. 1997, 336(10):683-690.
81. Marques-Vidal P., Sie P., Cambou J.P., Chap H., Perret B. Relationships of plasminogen activator inhibitor activity and lipoprotein(a) with insulin, testosterone, 17β-estradiol, and testosterone binding globulin in myocardial infarction patients and healthy controls. J. Clin. Endocrinol. Metab. 1995, 80(6):1794-1798.
82. Gebara O.C., Mittleman M.A., Sutherland P., Lipinska I., Matheney T., Xu P., Welty F.K., Wilson P.W., Levy D., Muller J.E. Association between increased estrogen status and increased fibrinolytic potential in the Framingham Offspring Study. Circulation 1995, 91(7):1952-1958.
83. Gordon E.M., Johnson T.R., Ramos L.P., Schmeidler-Sapiro K.T. Enhanced expression of factor XII (Hageman factor) in isolated livers of estrogen- and prolactin-treated rats. J. Lab. Clin. Med. 1991, 117(5):353-358.
84. Gordon E.M., Douglas J.G., Ratnoff O.D., Arafah B.M. The influence of estrogen and prolactin on Hageman factor (factor XII) titer in ovariectomized and hypophysectomized rats. Blood 1985, 66(3):602-605.
85. Johnson J.F. Changes in plasma prothrombin, Ac-globulin, and antithrombin concentration following intravenous administration of estrogens, Proc. Soc. Exp. Biol. Med. 1957, 94(1):92-94.
86. Bell S.C. Effects of oestradiol and progesterone on the concentration of α2-macroglobulin in the sera of injured male and female rats. J. Endocrinol. 1980, 86(1):189-191.
87. Palma J.A., Gavotto A.C., Villagra S. Effects of diethylstilbestrol, 17β estradiol, and progesterone on plasma fibrinogen levels in rats submitted to tissue injury (laparotomy). J. Trauma 1983, 23(2):132-135.
88. Conard J., Gompel A., Pelissier C., Mirabel C., Basdevant A. Fibrinogen and plasminogen modifications during oral estradiol replacement therapy. Fertil. Steril. 1997, 68(3):449-453.
89. Cushman M., Meilahn E.N., Psaty B.M., Kuller L.H., Dobs A.S., Tracy R.P. Hormone replacement therapy, inflammation, and hemostasis in elderly women. Arterioscler. Thromb. Vasc. Biol. 1999, 19(4):893-899.
90. Caine Y.G., Bauer K.A., Barzegar S., ten Cate H., Sacks F.M., Walsh B.W., Schiff I., Rosenberg R.D. Coagulation activation following estrogen administration to postmenopausal women. Thromb. Haemost. 1992, 68(4):392-395.
91. Wenger N.K., Speroff L., Packard B. Cardiovascular health and disease in women. N. Engl. J. Med. 1993, 329(4):247-256.
92. Rossouw J.E., Anderson G.L., Prentice R.L., LaCroix A.Z., Kooperberg C., Stefanick M.L., Jackson R.D., Beresford S.A., Howard B.V., Johnson K.C., Kotchen J.M., Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 2002, 288(3):321-333.
93. Anderson G.L., Limacher M., Assaf A.R., Bassford T., Beresford S.A., Black H., Bonds D., Brunner R., Brzyski R., Caan B., Chlebowski R., Curb D., Gass M., Hays J., Heiss G., Hendrix S., Howard B.V., Hsia J., Hubbell A., Jackson R., Johnson K.C., Judd H., Kotchen J.M., Kuller L., LaCroix A.Z., Lane D., Langer R.D., Lasser N., Lewis C.E., Manson J., Margolis K., Ockene J., O'Sullivan M.J., Phillips L., Prentice R.L., Ritenbaugh C., Robbins J., Rossouw J.E., Sarto G., Stefanick M.L., Van Horn L., Wactawski-Wende J., Wallace R., Wassertheil-Smoller S. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004, 291(14):1701-1712.
94. Beral V. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 2003, 362(9382):419-427.
95. Beral V., Bull D., Reeves G. Endometrial cancer and hormone-replacement therapy in the Million Women Study. Lancet 2005, 365(9470):1543-1551.
96. Beral V., Bull D., Green J., Reeves G. Ovarian cancer and hormone replacement therapy in the Million Women Study. Lancet 2007, 369(9574):1703-1710.
97. Kane S.V., Reddy D. Hormonal replacement therapy after menopause is protective of disease activity in women with inflammatory bowel disease. Am. J. Gastroenterol. 2008, 103(5):1193-1196.
98. Troisi R.J., Speizer F.E., Willett W.C., Trichopoulos D., Rosner B. Menopause, postmenopausal estrogen preparations, and the risk of adult-onset asthma. A prospective cohort study. Am. J. Respir. Crit. Care Med. 1995, 152(4 Pt 1):1183-1188.
99. Abu-Taha M., Rius C., Hermenegildo C., Noguera I., Cerda-Nicolas J.M., Issekutz A.C., Jose P.J., Cortijo J., Morcillo E.J., Sanz M.J. Menopause and ovariectomy cause a low grade of systemic inflammation that may be prevented by chronic treatment with low doses of estrogen or losartan. J. Immunol. 2009, 183(2):1393-1402.
100. Lee C.G., Carr M.C., Murdoch S.J., Mitchell E., Woods N.F., Wener M.H., Chandler W.L., Boyko E.J., Brunzell J.D. Adipokines, inflammation, and visceral adiposity across the menopausal transition: a prospective study. J. Clin. Endocrinol. Metab. 2009, 94(4):1104-1110.
101. Vural P., Akgul C., Canbaz M. Effects of hormone replacement therapy on plasma pro-inflammatory and anti-inflammatory cytokines and some bone turnover markers in postmenopausal women. Pharmacol. Res. 2006, 54(4):298-302.
102. Yasui T., Saijo A., Uemura H., Matsuzaki T., Tsuchiya N., Yuzurihara M., Kase Y., Irahara M. Effects of oral and transdermal estrogen therapy on circulating cytokines and chemokines in postmenopausal women with hysterectomy. Eur. J. Endocrinol. 2009, 161(2):267-273.
103. Goudev A., Georgiev D.B., Koycheva N., Manasiev N., Kyurkchiev S. Effects of low dose hormone replacement therapy on markers of inflammation in postmenopausal women. Maturitas 2002, 43(1):49-53.
104. Sites C.K., Toth M.J., Cushman M., L'Hommedieu G.D., Tchernof A., Tracy R.P., Poehlman E.T. Menopause-related differences in inflammation markers and their relationship to body fat distribution and insulin-stimulated glucose disposal. Fertil. Steril. 2002, 77(1):128-135.
105. Kania D.M., Binkley N., Checovich M., Havighurst T., Schilling M., Ershler W.B. Elevated plasma levels of interleukin-6 in postmenopausal women do not correlate with bone density. J. Am. Geriatr. Soc. 1995, 43(3):236-239.
106. Störk S., Bots M.L., Grobbee D.E., van der Schouw Y.T. Endogenous sex hormones and C-reactive protein in healthy postmenopausal women. J. Intern. Med. 2008, 264(3):245-253.
107. Shifren J.L., Rifai N., Desindes S., McIlwain M., Doros G., Mazer N.A. A comparison of the short-term effects of oral conjugated equine estrogens versus transdermal estradiol on C-reactive protein, other serum markers of inflammation, and other hepatic proteins in naturally menopausal women. J. Clin. Endocrinol. Metab. 2008, 93(5):1702-1710.
108. Lowe G.D., Upton M.N., Rumley A., McConnachie A., O'Reilly D.S., Watt G.C. Different effects of oral and transdermal hormone replacement therapies on factor IX, APC resistance, t-PA, PAI and C-reactive protein-a cross-sectional population survey. Thromb. Haemost. 2001, 86(2):550-556.
109. Jakimiuk A.J., Bogusiewicz M., Skorupski P., Adamiak A., Miotła P., Haczyński J., Rechberger T. Relationship between estrogen receptor-α polymorphism and serum levels of vascular cell adhesion molecule-1, intercellular adhesion molecule-1, C-reactive protein and homocysteine in postmenopausal women. Gynecol. Endocrinol. 2007, 23(10):584-589.
110. Nordström P., Glader C.A., Dahlén G., Birgander L.S., Lorentzon R., Waldenström A., Lorentzon M. Oestrogen receptor α gene polymorphism is related to aortic valve sclerosis in postmenopausal women. J. Intern. Med. 2003, 254(2):140-146.
111. Schiavone F.E., Rietschel R.L., Sgoutas D., Harris R. Elevated free testosterone levels in women with acne. Arch. Dermatol. 1983, 119(10):799-802.
112. Cappel M., Mauger D., Thiboutot D. Correlation between serum levels of insulin-like growth factor 1, dehydroepiandrosterone sulfate, and dihydrotestosterone and acne lesion counts in adult women. Arch. Dermatol. 2005, 141(3):333-338.
113. Yotsumoto S., Shimomai K., Hashiguchi T., Uchimiya H., Usuki K., Nishi M., Kanekura T., Kanzaki T. Estrogen dermatitis: a dendritic-cell-mediated allergic condition. Dermatology 2003, 207(3):265-268.
114. Hart R. Autoimmune progesterone dermatitis. Arch. Dermatol. 1977, 113(4):426-430.
115. Spector T.D., Ollier W., Perry L.A., Silman A.J., Thompson P.W., Edwards A. Free and serum testosterone levels in 276 males: a comparative study of rheumatoid arthritis, ankylosing spondylitis and healthy controls. Clin. Rheumatol. 1989, 8(1):37-41.
116. Cutolo M., Capellino S., Montagna P., Villaggio B., Sulli A., Seriolo B., Straub R.H. New roles for estrogens in rheumatoid arthritis. Clin. Exp. Rheumatol. 2003, 21(6):687-690.
117. Costenbader K.H., Feskanich D., Stampfer M.J., Karlson E.W. Reproductive and menopausal factors and risk of systemic lupus erythematosus in women. Arthritis Rheum. 2007, 56(4):1251-1262.
118. Glueck C.J., Lang J., Hamer T., Tracy T. Severe hypertriglyceridemia and pancreatitis when estrogen replacement therapy is given to hypertriglyceridemic women. J. Lab. Clin. Med. 1994, 123(1):59-64.
119. Richette P., Corvol M., Bardin T. Estrogens, cartilage, and osteoarthritis. Joint Bone Spine 2003, 70(4):257-262.
120. Gold S.M., Voskuhl R.R. Estrogen treatment in multiple sclerosis. J. Neurol. Sci. 2009, 286(1-2):99-103.
121. Lusis A.J. Atherosclerosis. Nature 2000, 407(6801):233-241.
122. Ross R. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 1999, 340(2):115-126.
123. Saha P., Modarai B., Humphries J., Mattock K., Waltham M., Burnand K.G., Smith A. The monocyte/macrophage as a therapeutic target in atherosclerosis. Curr. Opin. Pharmacol. 2009, 9(2):109-118.
124. Sorescu D., Weiss D., Lassègue B., Clempus R.E., Szöcs K., Sorescu G.P., Valppu L., Quinn M.T., Lambeth J.D., Vega J.D., Taylor W.R., Griendling K.K. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 2002, 105(12):1429-1435.
125. Choudhury R.P., Lee J.M., Greaves D.R. Mechanisms of disease: macrophage-derived foam cells emerging as therapeutic targets in atherosclerosis. Nat. Clin. Pract. Cardiovasc. Med. 2005, 2(6):309-315.
126. Joakimsen O., Bonaa K.H., Stensland-Bugge E., Jacobsen B.K. Population-based study of age at menopause and ultrasound assessed carotid atherosclerosis: the Tromsø Study. J. Clin. Epidemiol. 2000, 53(5):525-530.
127. Adams M.R., Kaplan J.R., Manuck S.B., Koritnik D.R., Parks J.S., Wolfe M.S., Clarkson T.B. Inhibition of coronary artery atherosclerosis by 17-beta estradiol in ovariectomized monkeys. Lack of an effect of added progesterone. Arteriosclerosis 1990, 10(6):1051-1057.
128. Adams M.R., Register T.C., Golden D.L., Wagner J.D., Williams J.K. Medroxyprogesterone acetate antagonizes inhibitory effects of conjugated equine estrogens on coronary artery atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 1997, 17(1):217-221.
129. Hanke H., Hanke S., Finking G., Muhic-Lohrer A., Mück A.O., Schmahl F.W., Haasis R., Hombach V. Different effects of estrogen and progesterone on experimental atherosclerosis in female versus male rabbits. Quantification of cellular proliferation by bromodeoxyuridine. Circulation 1996, 94(2):175-181.
130. Hodis H.N., Mack W.J., Lobo R.A., Shoupe D., Sevanian A., Mahrer P.R., Selzer R.H., Liu Cr C.R., Liu Ch C.H., Azen S.P. Estrogen in the prevention of atherosclerosis. A randomized, double-blind, placebo-controlled trial. Ann. Intern. Med 2001, 135(11):939-953.
131. Herrington D.M., Reboussin D.M., Brosnihan K.B., Sharp P.C., Shumaker S.A., Snyder T.E., Furberg C.D., Kowalchuk G.J., Stuckey T.D., Rogers W.J., Givens D.H., Waters D. Effects of estrogen replacement on the progression of coronary-artery atherosclerosis. N. Engl. J. Med. 2000, 343(8):522-529.
132. -/- mice. J. Clin. Invest. 2001, 107(3):333-340.
133. Losordo D.W., Kearney M., Kim E.A., Jekanowski J., Isner J.M. Variable expression of the estrogen receptor in normal and atherosclerotic coronary arteries of premenopausal women. Circulation 1994, 89(4):1501-1510.
134. Christian R.C., Liu P.Y., Harrington S., Ruan M., Miller V.M., Fitzpatrick L.A. Intimal estrogen receptor (ER)β, but not ERα expression, is correlated with coronary calcification and atherosclerosis in pre- and postmenopausal women. J. Clin. Endocrinol. Metab. 2006, 91(7):2713-2720.
135. Post W.S., Goldschmidt-Clermont P.J., Wilhide C.C., Heldman A.W., Sussman M.S., Ouyang P., Milliken E.E., Issa J.P. Methylation of the estrogen receptor gene is associated with aging and atherosclerosis in the cardiovascular system. Cardiovasc. Res. 1999, 43(4):985-991.
136. Kim J., Kim J.Y., Song K.S., Lee Y.H., Seo J.S., Jelinek J., Goldschmidt-Clermont P.J., Issa J.P. Epigenetic changes in estrogen receptor beta gene in atherosclerotic cardiovascular tissues and in-vitro vascular senescence. Biochim. Biophys. Acta 2007, 1772(1):72-80.
137. Lehtimäki T., Kunnas T.A., Mattila K.M., Perola M., Penttilä A., Koivula T., Karhunen P.J. Coronary artery wall atherosclerosis in relation to the estrogen receptor 1 gene polymorphism: an autopsy study. J. Mol. Med. 2002, 80(3):176-180.
138. Chen Wing L.Y., Chen Y.C., Shih Y.Y., Cheng J.C., Lin Y.J., Jiang M.J. Effects of oral estrogen on aortic ROS-generating and -scavenging enzymes and atherosclerosis in apoE-deficient mice. Exp. Biol. Med. (Maywood) 2009, 234(9):1037-1046.
139. Elhage R., Bayard F., Richard V., Holvoet P., Duverger N., Fievet C., Arnal J.F. Prevention of fatty streak formation of 17β-estradiol is not mediated by the production of nitric oxide in apolipoprotein E-deficient mice. Circulation 1997, 96(9):3048-3052.
140. Pervin S., Singh R., Rosenfeld M.E., Navab M., Chaudhuri G., Nathan L. Estradiol suppresses MCP-1 expression in vivo: implications for atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 1998, 18(10):1575-1582.
141. Lei Z.B., Fu X.J., Lu Z.T., Wang B.C., Liu X.L., You N.Z. Effect of estradiol on chemokine receptor CXCR2 expression in rats: implications for atherosclerosis. Acta Pharmacol. Sin. 2003, 24(7):670-674.
142. Nathan L., Pervin S., Singh R., Rosenfeld M., Chaudhuri G. Estradiol inhibits leukocyte adhesion and transendothelial migration in rabbits in vivo: possible mechanisms for gender differences in atherosclerosis. Circ. Res. 1999, 85(4):377-385.
143. Sulistiyani R.W., St Clair Effect of 17β-estradiol on metabolism of acetylated low-density lipoprotein by THP-1 macrophages in culture. Arterioscler. Thromb. Vasc. Biol. 1997, 17(9):1691-1700.
144. McCrohon J.A., Nakhla S., Jessup W., Stanley K.K., Celermajer D.S. Estrogen and progesterone reduce lipid accumulation in human monocyte-derived macrophages: a sex-specific effect. Circulation 1999, 100(23):2319-2325.
145. Sukovich D.A., Kauser K., Shirley F.D., DelVecchio V., Halks-Miller M., Rubanyi G.M. Expression of interleukin-6 in atherosclerotic lesions of male ApoE-knockout mice: inhibition by 17β-estradiol. Arterioscler. Thromb. Vasc. Biol. 1998, 18(9):1498-1505.
146. Elhage R., Clamens S., Besnard S., Mallat Z., Tedgui A., Arnal J., Maret A., Bayard F. Involvement of interleukin-6 in atherosclerosis but not in the prevention of fatty streak formation by 17β-estradiol in apolipoprotein E-deficient mice. Atherosclerosis 2001, 156(2):315-320.
147. Beresford S.A., Weiss N.S., Voigt L.F., McKnight B. Risk of endometrial cancer in relation to use of oestrogen combined with cyclic progestagen therapy in postmenopausal women. Lancet 1997, 349(9050):458-461.
148. Adams M.R., Anthony M.S., Manning J.M., Golden D.L., Parks J.S. Low-dose contraceptive estrogen-progestin and coronary artery atherosclerosis of monkeys. Obstet. Gynecol. 2000, 96(2):250-255.
149. Alexandersen P., Haarbo J., Sandholdt I., Shalmi M., Lawaetz H., Christiansen C. Norethindrone acetate enhances the antiatherogenic effect of 17β-estradiol: a secondary prevention study of aortic atherosclerosis in ovariectomized cholesterol-fed rabbits. Arterioscler. Thromb. Vasc. Biol. 1998, 18(6):902-907.
150. Clarkson T.B., Anthony M.S., Wagner J.D. A comparison of tibolone and conjugated equine estrogens effects on coronary artery atherosclerosis and bone density of postmenopausal monkeys. J. Clin. Endocrinol. Metab. 2001, 86(11):5396-5404.
151. Jonas H.A., Kronmal R.A., Psaty B.M., Manolio T.A., Meilahn E.N., Tell G.S., Tracy R.P., Robbins J.A., Anton-Culver H. Current estrogen-progestin and estrogen replacement therapy in elderly women: association with carotid atherosclerosis. Ann. Epidemiol. 1996, 6(4):314-323.
152. Martin P. Wound healing-aiming for perfect skin regeneration. Science 1997, 276(5309):75-81.
153. Ashcroft G.S., Mills S.J. Androgen receptor-mediated inhibition of cutaneous wound healing. J. Clin. Invest. 2002, 110(5):615-624.
154. Gilliver S.C., Ruckshanthi J.P., Hardman M.J., Nakayama T., Ashcroft G.S. Sex dimorphism in wound healing: the roles of sex steroids and macrophage migration inhibitory factor. Endocrinology 2008, 149(11):5747-5757.
155. Nyman S., Lindhe J., Zederfeldt B., Sölvell L. Vascular permeability in wounded areas of estradiol and progesterone treated female rabbits. Acta Chir. Scand. 1971, 137(8):709-714.
156. Lundgren D. Influence of estrogen and progesterone on exudation, inflammatory cell migration and granulation tissue formation in preformed cavities. Scand. J. Plast. Reconstr. Surg. 1973, 7(1):10-14.
157. Routley C.E., Ashcroft G.S. Effect of estrogen and progesterone on macrophage activation during wound healing. Wound Repair Regen. 2009, 17(1):42-50.
158. Ashcroft G.S., Dodsworth J., van Boxtel E., Tarnuzzer R.W., Horan M.A., Schultz G.S., Ferguson M.W. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-β1 levels. Nat. Med. 1997, 3(11):1209-1215.
159. Ashcroft G.S., Greenwell-Wild T., Horan M.A., Wahl S.M., Ferguson M.W. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am. J. Pathol. 1999, 155(4):1137-1146.
160. Hardman M.J., Emmerson E., Campbell L., Ashcroft G.S. Selective estrogen receptor modulators accelerate cutaneous wound healing in ovariectomized female mice. Endocrinology 2008, 149(2):551-557.
161. Brufani M., Ceccacci F., Filocamo L., Garofalo B., Joudioux R., La Bella A., Leonelli F., Migneco L.M., Marini Bettolo R., Farina P.M., Ashcroft G.S., Routley C., Hardman M., Meda C., Rando G., Maggi A. Novel locally active estrogens accelerate cutaneous wound healing. A Preliminary Study. Mol. Pharm. 2009, 6(2):543-556.
162. Leng L., Metz C.N., Fang Y., Xu J., Donnelly S., Baugh J., Delohery T., Chen Y., Mitchell R.A., Bucala R. MIF signal transduction initiated by binding to CD74. J. Exp. Med. 2003, 197(11):1467-1476.
163. Ashcroft G.S., Mills S.J., Flanders K.C., Lyakh L.A., Anzano M.A., Gilliver S.C., Roberts A.B. Role of Smad3 in the hormonal modulation of in vivo wound healing responses. Wound Repair Regen. 2003, 11(6):468-473.
164. Ashcroft G.S., Mills S.J., Lei K., Gibbons L., Jeong M.J., Taniguchi M., Burow M., Horan M.A., Wahl S.M., Nakayama T. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J. Clin. Invest. 2003, 111(9):1309-1318.
165. Hardman M.J., Waite A., Zeef L., Burow M., Nakayama T., Ashcroft G.S. Macrophage migration inhibitory factor: a central regulator of wound healing. Am. J. Pathol. 2005, 167(6):1561-1574.
166. Ashworth J.J., Smyth J.V., Pendleton N., Horan M., Payton A., Worthington J., Ollier W.E., Ashcroft G.S. The dinucleotide (CA) repeat polymorphism of estrogen receptor beta but not the dinucleotide (TA) repeat polymorphism of estrogen receptor alpha is associated with venous ulceration. J. Steroid Biochem. Mol. Biol. 2005, 97(3):266-270.
167. Ashworth J.J., Smyth J.V., Pendleton N., Horan M., Payton A., Worthington J., Ollier W.E., Ashcroft G.S. Polymorphisms spanning the 0N exon and promoter of the estrogen receptor-beta (ERβ) gene ESR2 are associated with venous ulceration. Clin. Genet. 2008, 73(1):55-61.
168. Gilliver S.C., Ashworth J.J., Mills S.J., Hardman M.J., Ashcroft G.S. Androgens modulate the inflammatory response during acute wound healing. J. Cell Sci. 2006, 119(4):722-732.
169. Ashcroft G.S., Yang X., Glick A.B., Weinstein M., Letterio J.L., Mizel D.E., Anzano M., Greenwell-Wild T., Wahl S.M., Deng C., Roberts A.B. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1999, 1(5):260-266.
170. Saika S., Ikeda K., Yamanaka O., Flanders K.C., Okada Y., Miyamoto T., Kitano A., Ooshima A., Nakajima Y., Ohnishi Y., Kao W.W. Loss of tumor necrosis factor α potentiates transforming growth factor β-mediated pathogenic tissue response during wound healing. Am. J. Pathol. 2006, 168(6):1848-1860.
171. Nitsch S.M., Wittmann F., Angele P., Wichmann M.W., Hatz R., Hernandez-Richter T., Chaudry I.H., Jauch K.W., Angele M.K. Physiological levels of 5α-dihydrotestosterone depress wound immune function and impair wound healing following trauma-hemorrhage. Arch. Surg. 2004, 139(2):157-163.
172. Kalinchenko S., Zemlyanoy A., Gooren L.J. Improvement of the diabetic foot upon testosterone administration to hypogonadal men with peripheral arterial disease. Report of three cases. Cardiovasc. Diabetol. 2009, 8(19).
173. Klein S.L. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol. 2004, 26(6-7):247-264.
174. Foth D., Cline J.M. Effects of mammalian and plant estrogens on mammary glands and uteri of macaques. Am. J. Clin. Nutr. 1998, 68(6 Suppl.):1413S-1417S.
175. Chuang K.H., Altuwaijri S., Li G., Lai J.J., Chu C.Y., Lai K.P., Lin H.Y., Hsu J.W., Keng P., Wu M.C., Chang C. Neutropenia with impaired host defense against microbial infection in mice lacking androgen receptor. J. Exp. Med. 2009, 206(5):1181-1199.
176. Molero L., García-Durán M., Diaz-Recasens J., Rico L., Casado S., López-Farré A. Expression of estrogen receptor subtypes and neuronal nitric oxide synthase in neutrophils from women and men: regulation by estrogen. Cardiovasc. Res. 2002, 56(1):43-51.
177. Murphy A.J., Guyre P.M., Wira C.R., Pioli P.A. Estradiol regulates expression of estrogen receptor ERα46 in human macrophages. PLoS One 2009, 4(5):e5539.
178. McCrohon J.A., Death A.K., Nakhla S., Jessup W., Handelsman D.J., Stanley K.K., Celermajer D.S. Androgen receptor expression is greater in macrophages from male than from female donors. A sex difference with implications for atherogenesis. Circulation 2000, 101(3):224-226.
179. Cutolo M., Accardo S., Villaggio B., Barone A., Sulli A., Coviello D.A., Carabbio C., Felli L., Miceli D., Farruggio R., Carruba G., Castagnetta L. Androgen and estrogen receptors are present in primary cultures of human synovial macrophages. J. Clin. Endocrinol. Metab. 1996, 81(2):820-827.
180. Khan K.N., Masuzaki H., Fujishita A., Kitajima M., Sekine I., Matsuyama T., Ishimaru T. Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis. Hum. Reprod. 2005, 20(7):2004-2013.
181. Zhao X.J., McKerr G., Dong Z., Higgins C.A., Carson J., Yang Z.Q., Hannigan B.M. Expression of oestrogen and progesterone receptors by mast cells alone, but not lymphocytes, macrophages or other immune cells in human upper airways. Thorax 2001, 56(3):205-211.
182. Butts C.L., Shukair S.A., Duncan K.M., Bowers E., Horn C., Belyavskaya E., Tonelli L., Sternberg E.M. Progesterone inhibits mature rat dendritic cells in a receptor-mediated fashion. Int. Immunol. 2007, 19(3):287-296.
183. intermediate dendritic cells from bone marrow precursors. J. Immunol. 2004, 172(3):1426-1436.
184. Arruvito L., Giulianelli S., Flores A.C., Paladino N., Barboza M., Lanari C., Fainboim L. NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J. Immunol. 2008, 180(8):5746-5753.
185. Curran E.M., Berghaus L.J., Vernetti N.J., Saporita A.J., Lubahn D.B., Estes D.M. 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. 2001, 214(1):12-20.
186. Benten W.P., Stephan C., Wunderlich F. B cells express intracellular but not surface receptors for testosterone and estradiol. Steroids 2002, 67(7):647-654.
187. Dosiou C., Hamilton A.E., Pang Y., Overgaard M.T., Tulac S., Dong J., Thomas P., Giudice L.C. Expression of membrane progesterone receptors on human T lymphocytes and Jurkat cells and activation of G-proteins by progesterone. J. Endocrinol. 2008, 196(1):67-77.
188. Suenaga R., Evans M.J., Mitamura K., Rider V., Abdou N.I. Peripheral blood T cells and monocytes and B cell lines derived from patients with lupus express estrogen receptor transcripts similar to those of normal cells. J. Rheumatol. 1998, 25(7):1305-1312.