RSS-Feed abonnieren
DOI: 10.1055/s-0034-1376355
Homeostasis Imbalance in the Endometrium of Women with Implantation Defects: The Role of Estrogen and Progesterone
Publikationsverlauf
Publikationsdatum:
24. Juni 2014 (online)
![](https://www.thieme-connect.de/media/srm/201405/lookinside/thumbnails/10.1055-s-0034-1376355-1.jpg)
Abstract
Embryo implantation is regulated by an inflammatory process in response to sequential exposure to estrogen and progesterone, followed by resolution and repair. The actions of estrogen and progesterone on these inflammatory processes are tightly and reciprocally controlled through regulated expression of steroid receptors, cofactors, chaperone proteins, and downstream signaling components. In endometriosis, the inflammatory cascades, normally seen at menstruation, are prematurely activated and endogenous endometrial mechanisms of inflammation resolution appear defective. The temporally abnormally inflammation is also associated with an imbalance between estrogen and progesterone actions; the normal luteal-phase dominance of progesterone action appears to be lost and is replaced by progesterone resistance and estrogen dominance. In this review, we examine these relationships in greater detail and argue that estrogen action is a prime target for future therapeutic solutions to endometriosis and implantation failure that result from this chronic, inflammatory disease.
-
References
- 1 Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420 (6917) 860-867
- 2 Grimble RF. Inflammatory status and insulin resistance. Curr Opin Clin Nutr Metab Care 2002; 5 (5) 551-559
- 3 Figarella-Branger D, Civatte M, Bartoli C, Pellissier JF. Cytokines, chemokines, and cell adhesion molecules in inflammatory myopathies. Muscle Nerve 2003; 28 (6) 659-682
- 4 Benelli R, Lorusso G, Albini A, Noonan DM. Cytokines and chemokines as regulators of angiogenesis in health and disease. Curr Pharm Des 2006; 12 (24) 3101-3115
- 5 Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 2006; 354 (6) 610-621
- 6 Martin GR, Wallace JL. Gastrointestinal inflammation: a central component of mucosal defense and repair. Exp Biol Med (Maywood) 2006; 231 (2) 130-137
- 7 Kulinsky VI. Biochemical aspects of inflammation. Biochemistry (Mosc) 2007; 72 (6) 595-607
- 8 Carlo T, Levy BD. Molecular circuits of resolution in airway inflammation. ScientificWorldJournal 2010; 10: 1386-1399
- 9 Mathis D, Shoelson SE. Immunometabolism: an emerging frontier. Nat Rev Immunol 2011; 11 (2) 81
- 10 Shachar I, Karin N. The dual roles of inflammatory cytokines and chemokines in the regulation of autoimmune diseases and their clinical implications. J Leukoc Biol 2013; 93 (1) 51-61
- 11 Serhan CN. Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu Rev Immunol 2007; 25: 101-137
- 12 Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 2008; 8 (5) 349-361
- 13 Lessey BA, Lebovic DI, Taylor RN. Eutopic endometrium in women with endometriosis: ground zero for the study of implantation defects. Semin Reprod Med 2013; 31 (2) 109-124
- 14 Genbacev OD, Prakobphol A, Foulk RA , et al. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 2003; 299 (5605) 405-408
- 15 Dominguez F, Yáñez-Mó M, Sanchez-Madrid F, Simón C. Embryonic implantation and leukocyte transendothelial migration: different processes with similar players?. FASEB J 2005; 19 (9) 1056-1060
- 16 Lea RG, Sandra O. Immunoendocrine aspects of endometrial function and implantation. Reproduction 2007; 134 (3) 389-404
- 17 Macdonald LJ, Boddy SC, Denison FC, Sales KJ, Jabbour HN. A role for lipoxin A, as an anti-inflammatory mediator in the human endometrium. Reproduction 2011; 142 (2) 345-352
- 18 Winger EE, Reed JL, Ashoush S, El-Toukhy T, Ahuja S, Taranissi M. Degree of TNF-α/IL-10 cytokine elevation correlates with IVF success rates in women undergoing treatment with Adalimumab (Humira) and IVIG. Am J Reprod Immunol 2011; 65 (6) 610-618
- 19 Granot I, Gnainsky Y, Dekel N. Endometrial inflammation and effect on implantation improvement and pregnancy outcome. Reproduction 2012; 144 (6) 661-668
- 20 Barash A, Dekel N, Fieldust S, Segal I, Schechtman E, Granot I. Local injury to the endometrium doubles the incidence of successful pregnancies in patients undergoing in vitro fertilization. Fertil Steril 2003; 79 (6) 1317-1322
- 21 Agic A, Xu H, Finas D, Banz C, Diedrich K, Hornung D. Is endometriosis associated with systemic subclinical inflammation?. Gynecol Obstet Invest 2006; 62 (3) 139-147
- 22 Wu MH, Lu CW, Chuang PC, Tsai SJ. Prostaglandin E2: the master of endometriosis?. Exp Biol Med (Maywood) 2010; 235 (6) 668-677
- 23 Canny GO, Lessey BA. The role of lipoxin A4 in endometrial biology and endometriosis. Mucosal Immunol 2013; 6 (3) 439-450
- 24 Berbic M, Fraser IS. Regulatory T cells and other leukocytes in the pathogenesis of endometriosis. J Reprod Immunol 2011; 88 (2) 149-155
- 25 Bulmer JN, Jones RK, Searle RF. Intraepithelial leukocytes in endometriosis and adenomyosis: comparison of eutopic and ectopic endometrium with normal endometrium. Hum Reprod 1998; 13: 2910-2915
- 26 Jones RK, Bulmer JN, Searle RF. Immunohistochemical characterization of stromal leukocytes in ovarian endometriosis: comparison of eutopic and ectopic endometrium with normal endometrium. Fertil Steril 1996; 66 (1) 81-89
- 27 Lessey BA, Killam AP, Metzger DA, Haney AF, Greene GL, McCarty Jr KS. Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J Clin Endocrinol Metab 1988; 67 (2) 334-340
- 28 Brenner RM, McClellan MC, West NB, Novy MJ, Haluska GJ, Sternfeld MD. Estrogen and progestin receptors in the macaque endometrium. Ann N Y Acad Sci 1991; 622: 149-166
- 29 Critchley HO, Brenner RM, Henderson TA , et al. Estrogen receptor beta, but not estrogen receptor alpha, is present in the vascular endothelium of the human and nonhuman primate endometrium. J Clin Endocrinol Metab 2001; 86 (3) 1370-1378
- 30 Garcia E, Bouchard P, De Brux J , et al. Use of immunocytochemistry of progesterone and estrogen receptors for endometrial dating. J Clin Endocrinol Metab 1988; 67 (1) 80-87
- 31 Padykula HA, Coles LG, Okulicz WC , et al. The basalis of the primate endometrium: a bifunctional germinal compartment. Biol Reprod 1989; 40 (3) 681-690
- 32 Okulicz WC, Ace CI, Scarrell R. Zonal changes in proliferation in the rhesus endometrium during the late secretory phase and menses. Proc Soc Exp Biol Med 1997; 214 (2) 132-138
- 33 Brenner RM, West NB, McClellan MC. Estrogen and progestin receptors in the reproductive tract of male and female primates. Biol Reprod 1990; 42 (1) 11-19
- 34 Tan J, Paria BC, Dey SK, Das SK. Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 1999; 140 (11) 5310-5321
- 35 de Ziegler D. Hormonal control of endometrial receptivity. Hum Reprod 1995; 10 (1) 4-7
- 36 de Ziegler D, Bergeron C, Cornel C , et al. Effects of luteal estradiol on the secretory transformation of human endometrium and plasma gonadotropins. J Clin Endocrinol Metab 1992; 74 (2) 322-331
- 37 de Ziegler D, Frydman R, Bouchard P. Contribution of estrogen to the morphology of “secretory” endometrium?. Fertil Steril 1995; 63 (5) 1135
- 38 Lee DK, Kurihara I, Jeong JW , et al. Suppression of ERalpha activity by COUP-TFII is essential for successful implantation and decidualization. Mol Endocrinol 2010; 24 (5) 930-940
- 39 Lessey BA, Palomino WA, Apparao KB, Young SL, Lininger RA. Estrogen receptor-alpha (ER-alpha) and defects in uterine receptivity in women. Reprod Biol Endocrinol 2006; 4 (Suppl. 01) S9
- 40 Park JS, Lee JH, Kim M, Chang HJ, Hwang KJ, Chang KH. Endometrium from women with endometriosis shows increased proliferation activity. Fertil Steril 2009; 92 (4) 1246-1249
- 41 Young SL, Lessey BA. Progesterone function in human endometrium: clinical perspectives. Semin Reprod Med 2010; 28 (1) 5-16
- 42 Noble LS, Simpson ER, Johns A, Bulun SE. Aromatase expression in endometriosis. J Clin Endocrinol Metab 1996; 81 (1) 174-179
- 43 Li X, Large MJ, Creighton CJ , et al. COUP-TFII regulates human endometrial stromal genes involved in inflammation. Mol Endocrinol 2013; 27 (12) 2041-2054
- 44 Talbi S, Hamilton AE, Vo KC , et al. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006; 147 (3) 1097-1121
- 45 Cooke PS, Buchanan DL, Young P , et al. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci U S A 1997; 94 (12) 6535-6540
- 46 Dickson RB, Lippman ME. Estrogenic regulation of growth and polypeptide growth factor secretion in human breast carcinoma. Endocr Rev 1987; 8 (1) 29-43
- 47 Ritvos O, Ranta T, Jalkanen J , et al. Insulin-like growth factor (IGF) binding protein from human decidua inhibits the binding and biological action of IGF-I in cultured choriocarcinoma cells. Endocrinology 1988; 122 (5) 2150-2157
- 48 Prossnitz ER, Arterburn JB, Sklar LA. GPR30: A G protein-coupled receptor for estrogen. Mol Cell Endocrinol 2007; 265-266: 138-142
- 49 Smith HO, Arias-Pulido H, Kuo DY , et al. GPR30 predicts poor survival for ovarian cancer. Gynecol Oncol 2009; 114 (3) 465-471
- 50 Prossnitz ER, Maggiolini M. Mechanisms of estrogen signaling and gene expression via GPR30. Mol Cell Endocrinol 2009; 308 (1–2) 32-38
- 51 Li Q, Kannan A, DeMayo FJ , et al. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 2011; 331 (6019) 912-916
- 52 Kurihara I, Lee DK, Petit FG , et al. COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS Genet 2007; 3 (6) e102
- 53 Lee DK, Kurihara I, DeMayo F, Tsai MJ, Tsai SY. ICI 182,780, a pure ERa antagonist partially rescued the implantation and decidualization defects in uterine specific COUP-TFII deficient mice. SCCPRIR Research Meeting; 2009; Chicago, IL
- 54 Xiong J, Zeng P, Cheng X , et al. Lipoxin A4 blocks embryo implantation by controlling estrogen receptor a activity. Reproduction 2013; Advance Publication (REP-12–0469)
- 55 Miller PB, Parnell BA, Bushnell G , et al. Endometrial receptivity defects during IVF cycles with and without letrozole. Hum Reprod 2012; 27 (3) 881-888
- 56 Straub RH. The complex role of estrogens in inflammation. Endocr Rev 2007; 28 (5) 521-574
- 57 Cutolo M, Capellino S, Sulli A , et al. Estrogens and autoimmune diseases. Ann N Y Acad Sci 2006; 1089: 538-547
- 58 Sakiani S, Olsen NJ, Kovacs WJ. Gonadal steroids and humoral immunity. Nat Rev Endocrinol 2013; 9 (1) 56-62
- 59 Olsen NJ, Kovacs WJ. Gonadal steroids and immunity. Endocr Rev 1996; 17 (4) 369-384
- 60 Zhang X, Xu H, Lin J, Qian Y, Deng L. Peritoneal fluid concentrations of interleukin-17 correlate with the severity of endometriosis and infertility of this disorder. BJOG 2005; 112 (8) 1153-1155
- 61 Andreoli CG, Genro VK, Souza CA , et al. T helper (Th)1, Th2, and Th17 interleukin pathways in infertile patients with minimal/mild endometriosis. Fertil Steril 2011; 95 (8) 2477-2480
- 62 Hirata T, Osuga Y, Takamura M , et al. Interleukin-17F increases the secretion of interleukin-8 and the expression of cyclooxygenase 2 in endometriosis. Fertil Steril 2011; 96 (1) 113-117
- 63 Boomsma CM, Kavelaars A, Eijkemans MJ , et al. Cytokine profiling in endometrial secretions: a non-invasive window on endometrial receptivity. Reprod Biomed Online 2009; 18 (1) 85-94
- 64 Fujimoto J, Hori M, Ichigo S, Tamaya T. Ovarian steroids regulate the expression of basic fibroblast growth factor and its mRNA in fibroblasts derived from uterine endometrium. Ann Clin Biochem 1997; 34 (Pt 1) 91-96
- 65 Presta M. Sex hormones modulate the synthesis of basic fibroblast growth factor in human endometrial adenocarcinoma cells: implications for the neovascularization of normal and neoplastic endometrium. J Cell Physiol 1988; 137 (3) 593-597
- 66 Gagliardi AR, Hennig B, Collins DC. Antiestrogens inhibit endothelial cell growth stimulated by angiogenic growth factors. Anticancer Res 1996; 16: 1101-1106
- 67 Irwin JC, Utian WH, Eckert RL. Sex steroids and growth factors differentially regulate the growth and differentiation of cultured human endometrial stromal cells. Endocrinology 1991; 129 (5) 2385-2392
- 68 Kanda N, Watanabe S. 17beta-estradiol inhibits the production of RANTES in human keratinocytes. J Invest Dermatol 2003; 120 (3) 420-427
- 69 Kanda N, Watanabe S. 17Beta-estradiol inhibits MCP-1 production in human keratinocytes. J Invest Dermatol 2003; 120 (6) 1058-1066
- 70 Akoum A, Jolicoeur C, Boucher A. Estradiol amplifies interleukin-1-induced monocyte chemotactic protein-1 expression by ectopic endometrial cells of women with endometriosis. J Clin Endocrinol Metab 2000; 85 (2) 896-904
- 71 Akoum A, Lawson C, McColl S, Villeneuve M. Ectopic endometrial cells express high concentrations of interleukin (IL)-8 in vivo regardless of the menstrual cycle phase and respond to oestradiol by up-regulating IL-1-induced IL-8 expression in vitro. Mol Hum Reprod 2001; 7 (9) 859-866
- 72 Bulun SE, Monsavais D, Pavone ME , et al. Role of estrogen receptor-β in endometriosis. Semin Reprod Med 2012; 30 (1) 39-45
- 73 Gashaw I, Stiller S, Böing C, Kimmig R, Winterhager E. Premenstrual regulation of the pro-angiogenic factor CYR61 in human endometrium. Endocrinology 2008; 149 (5) 2261-2269
- 74 Zhao L, Wu H, Zhou X, Wang Q, Zhu W, Chen J. Effects of progressive muscular relaxation training on anxiety, depression and quality of life of endometriosis patients under gonadotrophin-releasing hormone agonist therapy. Eur J Obstet Gynecol Reprod Biol 2012; 162 (2) 211-215
- 75 Absenger Y, Hess-Stumpp H, Kreft B , et al. Cyr61, a deregulated gene in endometriosis. Mol Hum Reprod 2004; 10 (6) 399-407
- 76 Gashaw I, Hastings JM, Jackson KS, Winterhager E, Fazleabas AT. Induced endometriosis in the baboon (Papio anubis) increases the expression of the proangiogenic factor CYR61 (CCN1) in eutopic and ectopic endometria. Biol Reprod 2006; 74 (6) 1060-1066
- 77 Ishizuka M, Hatori M, Suzuki T , et al. Sex steroid receptors in rheumatoid arthritis. Clin Sci (Lond) 2004; 106 (3) 293-300
- 78 Tabibzadeh SS, Santhanam U, Sehgal PB, May LT. Cytokine-induced production of IFN-beta 2/IL-6 by freshly explanted human endometrial stromal cells. Modulation by estradiol-17 beta. J Immunol 1989; 142 (9) 3134-3139
- 79 Ray P, Ghosh SK, Zhang DH, Ray A. Repression of interleukin-6 gene expression by 17 beta-estradiol: inhibition of the DNA-binding activity of the transcription factors NF-IL6 and NF-kappa B by the estrogen receptor. FEBS Lett 1997; 409 (1) 79-85
- 80 Su EJ, Lin ZH, Zeine R , et al. Estrogen receptor-beta mediates cyclooxygenase-2 expression and vascular prostanoid levels in human placental villous endothelial cells. Am J Obstet Gynecol 2009; 200 (4) e1-e8
- 81 Bulun SE, Cheng YH, Pavone ME , et al. Estrogen receptor-beta, estrogen receptor-alpha, and progesterone resistance in endometriosis. Semin Reprod Med 2010; 28 (1) 36-43
- 82 Evans J, Salamonsen LA. Inflammation, leukocytes and menstruation. Rev Endocr Metab Disord 2012; 13 (4) 277-288
- 83 Hudelist G, Keckstein J, Czerwenka K , et al. Estrogen receptor beta and matrix metalloproteinase 1 are coexpressed in uterine endometrium and endometriotic lesions of patients with endometriosis. Fertil Steril 2005; 84 (Suppl. 02) 1249-1256
- 84 Sato T, Ito A, Mori Y, Yamashita K, Hayakawa T, Nagase H. Hormonal regulation of collagenolysis in uterine cervical fibroblasts. Modulation of synthesis of procollagenase, prostromelysin and tissue inhibitor of metalloproteinases (TIMP) by progesterone and oestradiol-17 beta. Biochem J 1991; 275 (Pt 3) 645-650
- 85 Ryu K, Park C, Lee Y. Hypoxia-inducible factor 1 alpha represses the transcription of the estrogen receptor alpha gene in human breast cancer cells. Biochem Biophys Res Commun 2011; 407 (4) 831-836
- 86 Wu MH, Lu CW, Chang FM, Tsai SJ. Estrogen receptor expression affected by hypoxia inducible factor-1α in stromal cells from patients with endometriosis. Taiwan J Obstet Gynecol 2012; 51 (1) 50-54
- 87 Polotsky VY, Rubin AE, Balbir A , et al. Intermittent hypoxia causes REM sleep deficits and decreases EEG delta power in NREM sleep in the C57BL/6J mouse. Sleep Med 2006; 7 (1) 7-16
- 88 Chwalisz K, Garfield RE. Role of nitric oxide in implantation and menstruation. Hum Reprod 2000; 15 (Suppl. 03) 96-111
- 89 Thomas DD, Ridnour LA, Isenberg JS , et al. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 2008; 45 (1) 18-31
- 90 Han G, Magee T, Khorram O. Regulation of nitric oxide synthase isoforms by estrogen in the human endometrium. Fertil Steril 2005; 84 (Suppl. 02) 1220-1227
- 91 Kakui K, Itoh H, Sagawa N , et al. Augmented endothelial nitric oxide synthase (eNOS) protein expression in human pregnant myometrium: possible involvement of eNOS promoter activation by estrogen via both estrogen receptor (ER)alpha and ERbeta. Mol Hum Reprod 2004; 10 (2) 115-122
- 92 Jang EJ, Seok YM, Arterburn JB, Olatunji LA, Kim IK. GPER-1 agonist G1 induces vasorelaxation through activation of epidermal growth factor receptor-dependent signalling pathway. J Pharm Pharmacol 2013; 65 (10) 1488-1499
- 93 Plante BJ, Lessey BA, Taylor RN , et al. G protein-coupled estrogen receptor (GPER) expression in normal and abnormal endometrium. Reprod Sci 2012; 19 (7) 684-693
- 94 Nanni S, Benvenuti V, Grasselli A , et al. Endothelial NOS, estrogen receptor beta, and HIFs cooperate in the activation of a prognostic transcriptional pattern in aggressive human prostate cancer. J Clin Invest 2009; 119 (5) 1093-1108
- 95 Prossnitz ER, Barton M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol 2011; 7 (12) 715-726
- 96 Yates MA, Li Y, Chlebeck PJ, Offner H. GPR30, but not estrogen receptor-alpha, is crucial in the treatment of experimental autoimmune encephalomyelitis by oral ethinyl estradiol. BMC Immunol 2010; 11: 20
- 97 Brunsing RL, Prossnitz ER. Induction of interleukin-10 in the T helper type 17 effector population by the G protein coupled estrogen receptor (GPER) agonist G-1. Immunology 2011; 134 (1) 93-106
- 98 Serhan CN, Samuelsson B. Lipoxins: a new series of eicosanoids (biosynthesis, stereochemistry, and biological activities). Adv Exp Med Biol 1988; 229: 1-14
- 99 Hedqvist P, Raud J, Palmertz U, Haeggström J, Nicolaou KC, Dahlén SE. Lipoxin A4 inhibits leukotriene B4-induced inflammation in the hamster cheek pouch. Acta Physiol Scand 1989; 137 (4) 571-572
- 100 Lee TH, Lympany P, Crea AE, Spur BW. Inhibition of leukotriene B4-induced neutrophil migration by lipoxin A4: structure-function relationships. Biochem Biophys Res Commun 1991; 180 (3) 1416-1421
- 101 Badr KF, DeBoer DK, Schwartzberg M, Serhan CN. Lipoxin A4 antagonizes cellular and in vivo actions of leukotriene D4 in rat glomerular mesangial cells: evidence for competition at a common receptor. Proc Natl Acad Sci U S A 1989; 86 (9) 3438-3442
- 102 McMahon B, Mitchell D, Shattock R, Martin F, Brady HR, Godson C. Lipoxin, leukotriene, and PDGF receptors cross-talk to regulate mesangial cell proliferation. FASEB J 2002; 16 (13) 1817-1819
- 103 Russell R, Gori I, Pellegrini C, Kumar R, Achtari C, Canny GO. Lipoxin A4 is a novel estrogen receptor modulator. FASEB J 2011; 25 (12) 4326-4337
- 104 Fiore S, Romano M, Reardon EM, Serhan CN. Induction of functional lipoxin A4 receptors in HL-60 cells. Blood 1993; 81 (12) 3395-3403
- 105 Fiore S, Maddox JF, Perez HD, Serhan CN. Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor. J Exp Med 1994; 180 (1) 253-260
- 106 Serhan CN. Controlling the resolution of acute inflammation: a new genus of dual anti-inflammatory and proresolving mediators. J Periodontol 2008; 79 (8, Suppl): 1520-1526
- 107 Chiang N, Serhan CN, Dahlén SE , et al. The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo. Pharmacol Rev 2006; 58 (3) 463-487
- 108 Salamonsen LA, Woolley DE. Menstruation: induction by matrix metalloproteinases and inflammatory cells. J Reprod Immunol 1999; 44 (1–2) 1-27
- 109 Bulun SE, Cheng YH, Pavone ME , et al. Estrogen receptor-beta, estrogen receptor-alpha, and progesterone resistance in endometriosis. Semin Reprod Med 2010; 28 (1) 36-43
- 110 McDonnell DP, Norris JD. Connections and regulation of the human estrogen receptor. Science 2002; 296 (5573) 1642-1644
- 111 Coleman KM, Smith CL. Intracellular signaling pathways: nongenomic actions of estrogens and ligand-independent activation of estrogen receptors. Front Biosci 2001; 6: D1379-D1391
- 112 Weigel NL, Zhang Y. Ligand-independent activation of steroid hormone receptors. J Mol Med (Berl) 1998; 76 (7) 469-479
- 113 Hafner F, Holler E, von Angerer E. Effect of growth factors on estrogen receptor mediated gene expression. J Steroid Biochem Mol Biol 1996; 58 (4) 385-393
- 114 Gori I, Pellegrini C, Staedler D, Russell R, Jan C, Canny GO. Tumor necrosis factor-. α activates estrogen signaling pathways in endometrial epithelial cells via estrogen receptor α. Mol Cell Endocrinol 2011; 345 (1–2) 27-37
- 115 Tabibzadeh S. Cytokines and the hypothalamic-pituitary-ovarian-endometrial axis. Hum Reprod 1994; 9 (5) 947-967
- 116 Baulieu EE. RU486: a compound that gets itself talked about. Hum Reprod 1994; 9 (Suppl. 01) 1-6
- 117 Kachkache M, Acker GM, Chaouat G, Noun A, Garabédian M. Hormonal and local factors control the immunohistochemical distribution of immunocytes in the rat uterus before conceptus implantation: effects of ovariectomy, fallopian tube section, and injection. Biol Reprod 1991; 45 (6) 860-868
- 118 Tibbetts TA, Conneely OM, O'Malley BW. Progesterone via its receptor antagonizes the pro-inflammatory activity of estrogen in the mouse uterus. Biol Reprod 1999; 60 (5) 1158-1165
- 119 Hughes GC. Progesterone and autoimmune disease. Autoimmun Rev 2012; 11 (6–7) A502-A514
- 120 Munoz-Suano A, Hamilton AB, Betz AG. Gimme shelter: the immune system during pregnancy. Immunol Rev 2011; 241 (1) 20-38
- 121 Hazell GG, Yao ST, Roper JA, Prossnitz ER, O'Carroll AM, Lolait SJ. Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues. J Endocrinol 2009; 202 (2) 223-236
- 122 Tseng L, Gurpide E. Induction of human endometrial estradiol dehydrogenase by progestins. Endocrinology 1975; 97 (4) 825-833
- 123 Tseng L, Gurpide E. Effects of progestins on estradiol receptor levels in human endometrium. J Clin Endocrinol Metab 1975; 41 (2) 402-404
- 124 Burney RO, Talbi S, Hamilton AE , et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 2007; 148 (8) 3814-3826
- 125 Burney RO, Hamilton AE, Aghajanova L , et al. MicroRNA expression profiling of eutopic secretory endometrium in women with versus without endometriosis. Mol Hum Reprod 2009; 15 (10) 625-631
- 126 Kurita T, Lee KJ, Cooke PS, Lydon JP, Cunha GR. Paracrine regulation of epithelial progesterone receptor and lactoferrin by progesterone in the mouse uterus. Biol Reprod 2000; 62 (4) 831-838
- 127 Large MJ, DeMayo FJ. The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling. Mol Cell Endocrinol 2012; 358 (2) 155-165
- 128 Tan H, Yi L, Rote NS, Hurd WW, Mesiano S. Progesterone receptor-A and -B have opposite effects on proinflammatory gene expression in human myometrial cells: implications for progesterone actions in human pregnancy and parturition. J Clin Endocrinol Metab 2012; 97 (5) E719-E730
- 129 Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE. Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab 2000; 85 (8) 2897-2902
- 130 Bukulmez O, Hardy DB, Carr BR, Word RA, Mendelson CR. Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology 2008; 149 (3) 1190-1204
- 131 Igarashi TM, Bruner-Tran KL, Yeaman GR , et al. Reduced expression of progesterone receptor-B in the endometrium of women with endometriosis and in cocultures of endometrial cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fertil Steril 2005; 84 (1) 67-74
- 132 Khoufache K, Michaud N, Harir N, Kibangou Bondza P, Akoum A. Anomalies in the inflammatory response in endometriosis and possible consequences: a review. Minerva Endocrinol 2012; 37 (1) 75-92
- 133 Attar E, Tokunaga H, Imir G , et al. Prostaglandin E2 via steroidogenic factor-1 coordinately regulates transcription of steroidogenic genes necessary for estrogen synthesis in endometriosis. J Clin Endocrinol Metab 2009; 94 (2) 623-631
- 134 Jabbour HN, Kelly RW, Fraser HM, Critchley HO. Endocrine regulation of menstruation. Endocr Rev 2006; 27 (1) 17-46
- 135 Lessey BA, Young SL. The structure, function, and evaluation of the female reproductive tract. In: Strauss III JF, Barbieri RL, , eds. Reproductive Endocrinology: Physiology, Pathophysiology, and Clinical Management. Philadelphia, PA: Saunders Elsevier; 2012: 192-235
- 136 Tabibzadeh S. The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod 1996; 2 (2) 77-92
- 137 Markee JE. Menstruation in intraocular endometrial transplants in the Rhesus monkey. Am J Obstet Gynecol 1978; 131 (5) 558-559
- 138 Curry Jr TE, Osteen KG. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 2003; 24 (4) 428-465
- 139 Maybin JA, Critchley HO. Progesterone: a pivotal hormone at menstruation. Ann N Y Acad Sci 2011; 1221: 88-97
- 140 Henriet P, Gaide Chevronnay HP, Marbaix E. The endocrine and paracrine control of menstruation. Mol Cell Endocrinol 2012; 358 (2) 197-207
- 141 Guo Y, He B, Xu X, Wang J. Comprehensive analysis of leukocytes, vascularization and matrix metalloproteinases in human menstrual xenograft model. PLoS ONE 2011; 6 (2) e16840
- 142 Slayden OD, Brenner RM. A critical period of progesterone withdrawal precedes menstruation in macaques. Reprod Biol Endocrinol 2006; 4 (Suppl. 01) S6
- 143 Brenner RM, Nayak NR, Slayden OD, Critchley HO, Kelly RW. Premenstrual and menstrual changes in the macaque and human endometrium: relevance to endometriosis. Ann N Y Acad Sci 2002; 955: 60-74 , discussion 86–88, 396–406
- 144 Nayak NR, Critchley HO, Slayden OD , et al. Progesterone withdrawal up-regulates vascular endothelial growth factor receptor type 2 in the superficial zone stroma of the human and macaque endometrium: potential relevance to menstruation. J Clin Endocrinol Metab 2000; 85 (9) 3442-3452
- 145 Pickles VR. A plain-muscle stimulant in the menstruum. Nature 1957; 180 (4596) 1198-1199
- 146 Downie J, Poyser NL, Wunderlich M. Levels of prostaglandins in human endometrium during the normal menstrual cycle. J Physiol 1974; 236 (2) 465-472
- 147 Baird DT, Cameron ST, Critchley HO , et al. Prostaglandins and menstruation. Eur J Obstet Gynecol Reprod Biol 1996; 70 (1) 15-17
- 148 Wu MH, Shoji Y, Chuang PC, Tsai SJ. Endometriosis: disease pathophysiology and the role of prostaglandins. Expert Rev Mol Med 2007; 9 (2) 1-20
- 149 Lee J, Banu SK, Burghardt RC, Starzinski-Powitz A, Arosh JA. Selective inhibition of prostaglandin E2 receptors EP2 and EP4 inhibits adhesion of human endometriotic epithelial and stromal cells through suppression of integrin-mediated mechanisms. Biol Reprod 2013; 88 (3) 77
- 150 Lousse JC, Van Langendonckt A, Defrere S, Ramos RG, Colette S, Donnez J. Peritoneal endometriosis is an inflammatory disease. Front Biosci (Elite Ed) 2012; 4: 23-40
- 151 Kyama CM, Overbergh L, Debrock S , et al. Increased peritoneal and endometrial gene expression of biologically relevant cytokines and growth factors during the menstrual phase in women with endometriosis. Fertil Steril 2006; 85 (6) 1667-1675
- 152 Maybin JA, Hirani N, Jabbour HN, Critchley HO. Novel roles for hypoxia and prostaglandin E2 in the regulation of IL-8 during endometrial repair. Am J Pathol 2011; 178 (3) 1245-1256
- 153 D'Hooghe TM, Bambra CS, Xiao L, Peixe K, Hill JA. Effect of menstruation and intrapelvic injection of endometrium on inflammatory parameters of peritoneal fluid in the baboon (Papio anubis and Papio cynocephalus). Am J Obstet Gynecol 2001; 184 (5) 917-925
- 154 Dmowski WP, Gebel HM, Braun DP. The role of cell-mediated immunity in pathogenesis of endometriosis. Acta Obstet Gynecol Scand Suppl 1994; 159: 7-14
- 155 Seli E, Arici A. Endometriosis: interaction of immune and endocrine systems. Semin Reprod Med 2003; 21 (2) 135-144
- 156 Lydon JP, DeMayo FJ, Funk CR , et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 1995; 9 (18) 2266-2278
- 157 Otsuki Y. Apoptosis in human endometrium: apoptotic detection methods and signaling. Med Electron Microsc 2001; 34 (3) 166-173
- 158 Kokawa K, Shikone T, Nakano R. Apoptosis in the human uterine endometrium during the menstrual cycle. J Clin Endocrinol Metab 1996; 81 (11) 4144-4147
- 159 Konno R, Yamakawa H, Utsunomiya H, Ito K, Sato S, Yajima A. Expression of survivin and Bcl-2 in the normal human endometrium. Mol Hum Reprod 2000; 6 (6) 529-534
- 160 Lovely LP, Fazleabas AT, Fritz MA, McAdams DG, Lessey BA. Prevention of endometrial apoptosis: randomized prospective comparison of human chorionic gonadotropin versus progesterone treatment in the luteal phase. J Clin Endocrinol Metab 2005; 90 (4) 2351-2356
- 161 King A. Uterine leukocytes and decidualization. Hum Reprod Update 2000; 6 (1) 28-36
- 162 Marbaix E, Kokorine I, Moulin P, Donnez J, Eeckhout Y, Courtoy PJ. Menstrual breakdown of human endometrium can be mimicked in vitro and is selectively and reversibly blocked by inhibitors of matrix metalloproteinases. Proc Natl Acad Sci U S A 1996; 93 (17) 9120-9125
- 163 Rodgers WH, Matrisian LM, Giudice LC , et al. Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones. J Clin Invest 1994; 94 (3) 946-953
- 164 Irwin JC, Kirk D, Gwatkin RBL, Navre M, Cannon P, Giudice LC. Human endometrial matrix metalloproteinase-2, a putative menstrual proteinase. Hormonal regulation in cultured stromal cells and messenger RNA expression during the menstrual cycle. J Clin Invest 1996; 97 (2) 438-447
- 165 Henriet P, Cornet PB, Lemoine P , et al. Circulating ovarian steroids and endometrial matrix metalloproteinases (MMPs). Ann N Y Acad Sci 2002; 955: 119-138 , discussion 157–158, 396–406
- 166 Wentz AC. Premenstrual spotting: its association with endometriosis but not luteal phase inadequacy. Fertil Steril 1980; 33 (6) 605-607
- 167 Tabibzadeh S, Mason JM, Shea W, Cai Y, Murray MJ, Lessey B. Dysregulated expression of ebaf, a novel molecular defect in the endometria of patients with infertility. J Clin Endocrinol Metab 2000; 85 (7) 2526-2536
- 168 Bartosik D, Damjanov I, Viscarello RR, Riley JA. Immunoproteins in the endometrium: clinical correlates of the presence of complement fractions C3 and C4. Am J Obstet Gynecol 1987; 156 (1) 11-15
- 169 Isaacson KB, Coutifaris C, Garcia CR, Lyttle CR. Production and secretion of complement component 3 by endometriotic tissue. J Clin Endocrinol Metab 1989; 69 (5) 1003-1009
- 170 Sundstrom SA, Komm BS, Ponce-de-Leon H, Yi Z, Teuscher C, Lyttle CR. Estrogen regulation of tissue-specific expression of complement C3. J Biol Chem 1989; 264 (28) 16941-16947
- 171 Hasty LA, Lambris JD, Lessey BA, Pruksananonda K, Lyttle CR. Hormonal regulation of complement components and receptors throughout the menstrual cycle. Am J Obstet Gynecol 1994; 170 (1, Pt 1) 168-175
- 172 Young SL, Lessey BA, Fritz MA , et al. In vivo and in vitro evidence suggest that HB-EGF regulates endometrial expression of human decay-accelerating factor. J Clin Endocrinol Metab 2002; 87 (3) 1368-1375
- 173 Palomino WA, Argandoña F, Azúa R, Kohen P, Devoto L. Complement C3 and decay-accelerating factor expression levels are modulated by human chorionic gonadotropin in endometrial compartments during the implantation window. Reprod Sci 2013; 20 (9) 1103-1110
- 174 Lessey BA. Two pathways of progesterone action in the human endometrium: implications for implantation and contraception. Steroids 2003; 68 (10–13) 809-815
- 175 Lessey BA, Gui Y, Apparao KB, Young SL, Mulholland J. Regulated expression of heparin-binding EGF-like growth factor (HB-EGF) in the human endometrium: a potential paracrine role during implantation. Mol Reprod Dev 2002; 62 (4) 446-455
- 176 Illera MJ, Rumen J, Yuan LW, Lessey BA. Peritoneal fluid from infertile women with endometriosis and aberrant endometrial integrin expression blocks embryo implantation in a mouse model. The Endocrine Society 77th Annual Meeting; 1995;P2–98:315
- 177 Kim JJ, Taylor HS, Lu Z , et al. Altered expression of HOXA10 in endometriosis: potential role in decidualization. Mol Hum Reprod 2007; 13 (5) 323-332
- 178 Taylor HS, Bagot C, Kardana A, Olive D, Arici A. HOX gene expression is altered in the endometrium of women with endometriosis. Hum Reprod 1999; 14 (5) 1328-1331
- 179 Lessey BA, Castelbaum AJ, Sawin SW , et al. Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 1994; 79 (2) 643-649
- 180 Kaul A, Nagamani M, Nowicki B. Decreased expression of endometrial decay accelerating factor (DAF), a complement regulatory protein, in patients with luteal phase defect. Am J Reprod Immunol 1995; 34 (4) 236-240
- 181 Banadakoppa M, Goluszko P, Liebenthal D, Yallampalli C. Nitric oxide induces segregation of decay accelerating factor (DAF or CD55) from the membrane lipid-rafts and its internalization in human endometrial cells. Cell Biol Int 2012; 36 (10) 901-907
- 182 Khorram O, Lessey BA. Alterations in expression of endometrial endothelial nitric oxide synthase and alpha(v)beta(3) integrin in women with endometriosis. Fertil Steril 2002; 78 (4) 860-864
- 183 Aisemberg J, Vercelli CA, Bariani MV, Billi SC, Wolfson ML, Franchi AM. Progesterone is essential for protecting against LPS-induced pregnancy loss. LIF as a potential mediator of the anti-inflammatory effect of progesterone. PLoS ONE 2013; 8 (2) e56161
- 184 Ota H, Igarashi S, Hatazawa J, Tanaka T. Endothelial nitric oxide synthase in the endometrium during the menstrual cycle in patients with endometriosis and adenomyosis. Fertil Steril 1998; 69 (2) 303-308
- 185 Cullinan EB, Abbondanzo SJ, Anderson PS, Pollard JW, Lessey BA, Stewart CL. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation. Proc Natl Acad Sci U S A 1996; 93 (7) 3115-3120
- 186 Espey LL. Ovulation as an inflammatory reaction—a hypothesis. Biol Reprod 1980; 22 (1) 73-106
- 187 Finn CA. Implantation, menstruation and inflammation. Biol Rev Camb Philos Soc 1986; 61 (4) 313-328
- 188 Borrelli GM, Abrao MS, Mechsner S. Can chemokines be used as biomarkers for endometriosis? A systematic review. Hum Reprod 2014; 29 (2) 253-266
- 189 May KE, Conduit-Hulbert SA, Villar J, Kirtley S, Kennedy SH, Becker CM. Peripheral biomarkers of endometriosis: a systematic review. Hum Reprod Update 2010; 16 (6) 651-674
- 190 Kyama CM, Mihalyi A, Simsa P , et al. Role of cytokines in the endometrial-peritoneal cross-talk and development of endometriosis. Front Biosci (Elite Ed) 2009; 1: 444-454 (Elite Ed)
- 191 Bulun SE. Endometriosis. N Engl J Med 2009; 360 (3) 268-279