Early endometriosis in females is directed by immune-Mediated estrogen receptor a and IL-6 cross-Talk

Endocrinology

Volumn 159, Issue 1, 2018, Pages 103-118

  Burns, Katherine A ^a   Thomas, Seddon Y ^a   Hamilton, Katherine J ^a   Young, Steven L ^b   Cook, Donald N ^a   Korach, Kenneth S ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; INTERLEUKIN 6; BIOLOGICAL MARKER; ESTROGEN RECEPTOR ALPHA, HUMAN; IL6 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; ENDOMETRIOSIS; FEMALE; GENE EXPRESSION; HOST; MACROPHAGE; MOLECULAR INTERACTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PERITONEAL CAVITY; PERITONEAL FLUID; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UTERUS TISSUE; AGONISTS; ANIMAL; ASCITES FLUID; C57BL MOUSE; DISEASE EXACERBATION; ENDOMETRIUM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; MACROPHAGE ACTIVATION; METABOLISM; NATURAL KILLER CELL; OVARIECTOMY; PATHOLOGY; PATHOPHYSIOLOGY; RANDOMIZATION;

ANIMALS; ASCITIC FLUID; BIOMARKERS; DISEASE PROGRESSION; ENDOMETRIOSIS; ENDOMETRIUM; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INTERLEUKIN-6; KILLER CELLS, NATURAL; MACROPHAGE ACTIVATION; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; OVARIECTOMY; RANDOM ALLOCATION; SIGNAL TRANSDUCTION;

EID: 85040732690     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2017-00562     Document Type: Article

References (86)

1. Simoens S, Dunselman G, Dirksen C, Hummelshoj L, Bokor A, Brandes I, Brodszky V, Canis M, Colombo GL, DeLeire T, Falcone T, Graham B, Halis G, Horne A, Kanj O, Kjer JJ, Kristensen J, Lebovic D, Mueller M, Vigano P, Wullschleger M, D’Hooghe T. The burden of endometriosis: costs and quality of life of women with endometriosis and treated in referral centres. Hum Reprod. 2012;27(5):1292–1299.
2. Giudice LC, Kao LC. Endometriosis. Lancet. 2004;364(9447): 1789–1799.
3. 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.
4. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3(2):93–110.
5. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30(4):293–342.
6. Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev. 1999;20(3): 358–417.
7. Capellino S, Montagna P, Villaggio B, Sulli A, Soldano S, Ferrero S, Remorgida V, Cutolo M. Role of estrogens in inflammatory response: expression of estrogen receptors in peritoneal fluid macrophages from endometriosis. Ann N Y Acad Sci. 2006;1069: 263–267.
8. 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.
9. Burns KA, Rodriguez KF, Hewitt SC, Janardhan KS, Young SL, Korach KS. Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model. Endocrinology. 2012;153(8):3960–3971.
10. Zhao Y, Gong P, Chen Y, Nwachukwu JC, Srinivasan S, Ko C, Bagchi MK, Taylor RN, Korach KS, Nettles KW, Katzenellenbogen JA, Katzenellenbogen BS. Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis. Sci Transl Med. 2015;7(271):271ra9.
11. Halme J, Becker S, Haskill S. Altered maturation and function of peritoneal macrophages: possible role in pathogenesis of endometriosis. Am J Obstet Gynecol. 1987;156(4):783–789.
12. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T. Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum. Fertil Steril. 2004;81(3): 652–661.
13. Bulun SE, Yang S, Fang Z, Gurates B, Tamura M, Sebastian S. Estrogen production and metabolism in endometriosis. Ann N Y Acad Sci. 2002;955:75–85; discussion 86–78, 396–406.
14. Sharpe-Timms KL. Endometrial anomalies in women with endometriosis. Ann N Y Acad Sci. 2001;943:131–147.
15. Guo SW. Recurrence of endometriosis and its control. Hum Reprod Update. 2009;15(4):441–461.
16. Wright KP, Johnson JV. Evaluation of extended and continuous use oral contraceptives. Ther Clin Risk Manag. 2008;4(5):905–911.
17. Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J, Osteen KG. Steroid and cytokine regulation of matrix metal-loproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab. 2002;87(10):4782–4791.
18. Ricci AG, Olivares CN, Bilotas MA, Meresman GF, Barañao RI. Effect of vascular endothelial growth factor inhibition on endometrial implant development in a murine model of endometriosis. Reprod Sci. 2011;18(7):614–622.
19. Kyama CM, Mihalyi A, Simsa P, Falconer H, Fulop V, Mwenda JM, Peeraer K, Tomassetti C, Meuleman C, D’Hooghe TM. Role of cytokines in the endometrial-peritoneal cross-talk and development of endometriosis. Front Biosci (Elite Ed). 2009;1:444–454.
20. Straub RH. The complex role of estrogens in inflammation. Endocr Rev. 2007;28(5):521–574.
21. Kelly RW, King AE, Critchley HO. Cytokine control in human endometrium. Reproduction. 2001;121(1):3–19.
22. Salamonsen LA, Lathbury LJ. Endometrial leukocytes and menstruation. Hum Reprod Update. 2000;6(1):16–27.
23. Kaitu’u-Lino TJ, Morison NB, Salamonsen LA. Neutrophil depletion retards endometrial repair in a mouse model. Cell Tissue Res. 2007;328(1):197–206.
24. Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, Prykhozhij S, Peri F, Wilson SW, Ruhrberg C. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood. 2010;116(5): 829–840.
25. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159–175.
26. Christoffersson G, Vågesjö E, Vandooren J, Lidén M, Massena S, Reinert RB, Brissova M, Powers AC, Opdenakker G, Phillipson M. VEGF-A recruits a proangiogenic MMP-9-delivering neutrophil subset that induces angiogenesis in transplanted hypoxic tissue. Blood. 2012;120(23):4653–4662.
27. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11(8):519–531.
28. Phillipson M, Kubes P. The neutrophil in vascular inflammation. Nat Med. 2011;17(11):1381–1390.
29. Sadik CD, Kim ND, Luster AD. Neutrophils cascading their way to inflammation. Trends Immunol. 2011;32(10):452–460.
30. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11(11):723–737.
31. Punnonen J, Teisala K, Ranta H, Bennett B, Punnonen R. Increased levels of interleukin-6 and interleukin-10 in the peritoneal fluid of patients with endometriosis. Am J Obstet Gynecol. 1996;174(5): 1522–1526.
32. Styer AK, Sullivan BT, Puder M, Arsenault D, Petrozza JC, Ser-ikawa T, Chang S, Hasan T, Gonzalez RR, Rueda BR. Ablation of leptin signaling disrupts the establishment, development, and maintenance of endometriosis-like lesions in a murine model. Endocrinology. 2008;149(2):506–514.
33. Khan KN, Kitajima M, Hiraki K, Fujishita A, Sekine I, Ishimaru T, Masuzaki H. Immunopathogenesis of pelvic endometriosis: role of hepatocyte growth factor, macrophages and ovarian steroids. Am J Reprod Immunol. 2008;60(5):383–404.
34. Battersby S, Critchley HO, de Brum-Fernandes AJ, Jabbour HN. Temporal expression and signalling of prostacyclin receptor in the human endometrium across the menstrual cycle. Reproduction. 2004;127(1):79–86.
35. Salamonsen LA, Woolley DE. Menstruation: induction by matrix metalloproteinases and inflammatory cells. J Reprod Immunol. 1999;44(1-2):1–27.
36. Hewitt SC, Kissling GE, Fieselman KE, Jayes FL, Gerrish KE, Korach KS. Biological and biochemical consequences of global deletion of exon 3 from the ER alpha gene. FASEB J. 2010;24(12): 4660–4667.
37. Winuthayanon W, Piyachaturawat P, Suksamrarn A, Ponglikitmongkol M, Arao Y, Hewitt SC, Korach KS. Diarylheptanoid phytoestrogens isolated from the medicinal plant Curcuma comosa: biologic actions in vitro and in vivo indicate estrogen receptor-dependent mechanisms. Environ Health Perspect. 2009;117(7):1155–1161.
38. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):e45.
39. Hewitt SC, Li L, Grimm SA, Winuthayanon W, Hamilton KJ, Pockette B, Rubel CA, Pedersen LC, Fargo D, Lanz RB, DeMayo FJ, Schütz G, Korach KS. Novel DNA motif binding activity observed in vivo with an estrogen receptor a mutant mouse. Mol Endocrinol. 2014;28(6):899–911.
40. Greene AD, Lang SA, Kendziorski JA, Sroga-Rios JM, Herzog TJ, Burns KA. Endometriosis: where are we and where are we going? Reproduction. 2016;152(3):R63–R78.
41. Xia W, Hilgenbrink AR, Matteson EL, Lockwood MB, Cheng JX, Low PS. A functional folate receptor is induced during macrophage activation and can be used to target drugs to activated macrophages. Blood. 2009;113(2):438–446.
42. Manaster I, Mizrahi S, Goldman-Wohl D, Sela HY, Stern-Ginossar N, Lankry D, Gruda R, Hurwitz A, Bdolah Y, Haimov-Kochman R, Yagel S, Mandelboim O. Endometrial NK cells are special immature cells that await pregnancy. J Immunol. 2008;181(3): 1869–1876.
43. Hannan NJ, Paiva P, Meehan KL, Rombauts LJ, Gardner DK, Salamonsen LA. Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology. 2011;152(12):4948–4956.
44. Stanic AK, Kim M, Styer AK, Rueda BR. Dendritic cells attenuate the early establishment of endometriosis-like lesions in a murine model. Reprod Sci. 2014;21(10):1228–1236.
45. Nwachukwu JC, Srinivasan S, Bruno NE, Parent AA, Hughes TS, Pollock JA, Gjyshi O, Cavett V, Nowak J, Garcia-Ordonez RD, Houtman R, Griffin PR, Kojetin DJ, Katzenellenbogen JA, Conkright MD, Nettles KW. Resveratrol modulates the inflammatory response via an estrogen receptor-signal integration network. eLife. 2014;3:e02057.
46. Stein B, Yang MX. Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Mol Cell Biol. 1995;15(9):4971–4979.
47. Pottratz ST, Bellido T, Mocharla H, Crabb D, Manolagas SC. 17 beta-Estradiol inhibits expression of human interleukin-6 promoter-reporter constructs by a receptor-dependent mechanism. J Clin Invest. 1994;93(3):944–950.
48. Liu H, Liu K, Bodenner DL. Estrogen receptor inhibits interleukin-6 gene expression by disruption of nuclear factor kappaB trans-activation. Cytokine. 2005;31(4):251–257.
49. D’Hooghe TM, Bambra CS, De Jonge I, Lauweryns JM, Koninckx PR. The prevalence of spontaneous endometriosis in the baboon (Papio anubis, Papio cynocephalus) increases with the duration of captivity. Acta Obstet Gynecol Scand. 1996; 75(2):98–101.
50. Evans J, Salamonsen LA. Inflammation, leukocytes and menstruation. Rev Endocr Metab Disord. 2012;13(4):277–288.
51. 2a during human endometrial repair. J Clin Endocrinol Metab. 2011;96(8):2475–2483.
52. Milewski Ł, Dziunycz P, Barcz E, Radomski D, Roszkowski PI, Korczak-Kowalska G, Kaminski ´ P, Malejczyk J. Increased levels of human neutrophil peptides 1, 2, and 3 in peritoneal fluid of patients with endometriosis: association with neutrophils, T cells and IL-8. J Reprod Immunol. 2011;91(1-2):64–70.
53. Soehnlein O, Lindbom L. Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol. 2010;10(6): 427–439.
54. Soehnlein O, Zernecke A, Eriksson EE, Rothfuchs AG, Pham CT, Herwald H, Bidzhekov K, Rottenberg ME, Weber C, Lindbom L. Neutrophil secretion products pave the way for inflammatory monocytes. Blood. 2008;112(4):1461–1471.
55. Piva M, Horowitz GM, Sharpe-Timms KL. Interleukin-6 differentially stimulates haptoglobin production by peritoneal and endometriotic cells in vitro: a model for endometrial-peritoneal interaction in endometriosis. J Clin Endocrinol Metab. 2001;86(6): 2553–2561.
56. 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.
57. Akoum A, Lemay A, Paradis I, Rheault N, Maheux R. Secretion of interleukin-6 by human endometriotic cells and regulation by proinflammatory cytokines and sex steroids. Hum Reprod. 1996; 11(10):2269–2275.
58. Martínez S, Garrido N, Coperias JL, Pardo F, Desco J, García-Velasco JA, Simón C, Pellicer A. Serum interleukin-6 levels are elevated in women with minimal-mild endometriosis. Hum Reprod. 2007;22(3):836–842.
59. Pruenster M, Mudde L, Bombosi P, Dimitrova S, Zsak M, Middleton J, Richmond A, Graham GJ, Segerer S, Nibbs RJ, Rot A. The Duffy antigen receptor for chemokines transports chemokines and supports their promigratory activity. Nat Immunol. 2009;10(1): 101–108.
60. Williams MR, Azcutia V, Newton G, Alcaide P, Luscinskas FW. Emerging mechanisms of neutrophil recruitment across endothe-lium. Trends Immunol. 2011;32(10):461–469.
61. Soehnlein O, Lindbom L, Weber C. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood. 2009;114(21): 4613–4623.
62. Olive DL, Weinberg JB, Haney AF. Peritoneal macrophages and infertility: the association between cell number and pelvic pathology. Fertil Steril. 1985;44(6):772–777.
63. Haney AF. Endometriosis, macrophages, and adhesions. Prog Clin Biol Res. 1993;381:19–44.
64. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8(12):958–969.
65. Kajihara H, Yamada Y, Kanayama S, Furukawa N, Noguchi T, Haruta S, Yoshida S, Sado T, Oi H, Kobayashi H. New insights into the pathophysiology of endometriosis: from chronic inflammation to danger signal. Gynecol Endocrinol. 2011;27(2):73–79.
66. Capobianco A, Rovere-Querini P. Endometriosis, a disease of the macrophage. Front Immunol. 2013;4:9.
67. Beste MT, Pfäffle-Doyle N, Prentice EA, Morris SN, Lauffenburger DA, Isaacson KB, Griffith LG. Molecular network analysis of endometriosis reveals a role for c-Jun-regulated macrophage activation. Sci Transl Med. 2014;6(222):222ra16.
68. Bacci M, Capobianco A, Monno A, Cottone L, Di Puppo F, Camisa B, Mariani M, Brignole C, Ponzoni M, Ferrari S, Panina-Bordignon P, Manfredi AA, Rovere-Querini P. Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease. Am J Pathol. 2009;175(2):547–556.
69. Capobianco A, Monno A, Cottone L, Venneri MA, Biziato D, Di Puppo F, Ferrari S, De Palma M, Manfredi AA, Rovere-Querini P. Proangiogenic Tie2(+) macrophages infiltrate human and murine endometriotic lesions and dictate their growth in a mouse model of the disease. Am J Pathol. 2011;179(5):2651–2659.
70. Cao X, Yang D, Song M, Murphy A, Parthasarathy S. The presence of endometrial cells in the peritoneal cavity enhances monocyte recruitment and induces inflammatory cytokines in mice: implications for endometriosis. Fertil Steril. 2004;82(Suppl 3): 999–1007.
71. Lin YJ, Lai MD, Lei HY, Wing LY. Neutrophils and macrophages promote angiogenesis in the early stage of endometriosis in a mouse model. Endocrinology. 2006;147(3):1278–1286.
72. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Bio-chim Biophys Acta. 2011;1813(5):878–888.
73. Clahsen T, Schaper F. Interleukin-6 acts in the fashion of a classical chemokine on monocytic cells by inducing integrin activation, cell adhesion, actin polymerization, chemotaxis, and transmigration. J Leukoc Biol. 2008;84(6):1521–1529.
74. Ray A, Prefontaine KE, Ray P. Down-modulation of interleukin-6 gene expression by 17 beta-estradiol in the absence of high affinity DNA binding by the estrogen receptor. J Biol Chem. 1994;269(17): 12940–12946.
75. Cutolo M, Villaggio B, Bisso A, Sulli A, Coviello D, Dayer JM. Presence of estrogen receptors in human myeloid monocytic cells (THP-1 cell line). Eur Cytokine Netw. 2001;12(2):368–372.
76. Okada M, Suzuki A, Mizuno K, Asada Y, Ino Y, Kuwayama T, Tamakoshi K, Mizutani S, Tomoda Y. Effects of 17 beta-estradiol and progesterone on migration of human monocytic THP-1 cells stimulated by minimally oxidized low-density lipoprotein in vitro. Cardiovasc Res. 1997;34(3):529–535.
77. Suzuki A, Mizuno K, Ino Y, Okada M, Kikkawa F, Mizutani S, Tomoda Y. Effects of 17 beta-estradiol and progesterone on growth-factor-induced proliferation and migration in human female aortic smooth muscle cells in vitro. Cardiovasc Res. 1996; 32(3):516–523.
78. Sasser AK, Sullivan NJ, Studebaker AW, Hendey LF, Axel AE, Hall BM. Interleukin-6 is a potent growth factor for ER-alpha-positive human breast cancer. FASEB J. 2007;21(13):3763–3770.
79. Baumgarten SC, Frasor J. Minireview: Inflammation: an instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol Endocrinol. 2012;26(3):360–371.
80. Kim BG, Yoo JY, Kim TH, Shin JH, Langenheim JF, Ferguson SD, Fazleabas AT, Young SL, Lessey BA, Jeong JW. Aberrant activation of signal transducer and activator of transcription-3 (STAT3) signaling in endometriosis. Hum Reprod. 2015;30(5): 1069–1078.
81. Yoo JY, Jeong JW, Fazleabas AT, Tayade C, Young SL, Lessey BA. Protein inhibitor of activated STAT3 (PIAS3) is down-regulated in eutopic endometrium of women with endometriosis. Biol Reprod. 2016;95(1):11.
82. González-Ramos R, Donnez J, Defrère S, Leclercq I, Squifflet J, Lousse JC, Van Langendonckt A. Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis. Mol Hum Reprod. 2007;13(7):503–509.
83. Han SJ, Hawkins SM, Begum K, Jung SY, Kovanci E, Qin J, Lydon JP, DeMayo FJ, O’Malley BW. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med. 2012;18(7):1102–1111.
84. Han SJ, Jung SY, Wu SP, Hawkins SM, Park MJ, Kyo S, Qin J, Lydon JP, Tsai SY, Tsai MJ, DeMayo FJ, O’Malley BW. Estrogen receptor b modulates apoptosis complexes and the inflammasome to drive the pathogenesis of endometriosis. Cell. 2015;163(4): 960–974.
85. Gately S, Li WW. Multiple roles of COX-2 in tumor angiogenesis: a target for antiangiogenic therapy. Semin Oncol. 2004;31(2, Suppl 7):2–11.
86. Zhou H, Ivanov VN, Gillespie J, Geard CR, Amundson SA, Brenner DJ, Yu Z, Lieberman HB, Hei TK. Mechanism of radiation-induced bystander effect: role of the cyclooxygenase-2 signaling pathway. Proc Natl Acad Sci USA. 2005;102(41):14641–14646.