Recent advances in the understanding of endometriosis: The role of inflammatory mediators in disease pathogenesis and treatment

F1000Research

Volumn 5, Issue , 2016, Pages

  Nothnick, Warren ^a,b   Alali, Zahraa ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4 HYDROXYPHENYL) 4,5 DIHYDRO 5 ISOXAZOLE ACETIC ACID METHYL ESTER; 4 [2 PHENYL 5,7 BIS(TRIFLUOROMETHYL)PYRAZOLO[1,5 A]PYRIMIDIN 3 YL]PHENOL; CHLOROINDAZOLE; CYCLOOXYGENASE 2; CYTOKINE RECEPTOR ANTAGONIST; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ANTAGONIST; ESTROGEN RECEPTOR BETA; GESTAGEN; INTERLEUKIN 8; MACROPHAGE MIGRATION INHIBITION FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; OXABICYCLOHEPTENE SULFONATE; PRINABEREL; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANTIINFLAMMATORY ACTIVITY; COST BENEFIT ANALYSIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DISEASE COURSE; DRUG TARGETING; ENDOMETRIOSIS; GYNECOLOGIC SURGERY; HUMAN; INFLAMMATION; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW;

EID: 84964526368     PISSN: 20461402     EISSN: 1759796X     Source Type: Journal    
DOI: 10.12688/f1000research.7504.1     Document Type: Review

References (62)

1. Simoens S Hummelshoj L D'Hooghe T: Endometriosis: cost estimates and methodological perspective. Hum Reprod Update. 2007;13(4):395-404. 17584822 10.1093/humupd/dmm010
2. Raible MD: Pathophysiology and treatment of endometriosis. Am J Hosp Pharm. 1981;38(11):1696-1701. 7030070
3. Gazvani R Templeton A: Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis. Reproduction. 2002;123(2):217-226. 11866688 10.1530/rep.0.1230217
4. Haney AF Weinberg JB: Reduction of the intraperitoneal inflammation associated with endometriosis by treatment with medroxyprogesterone acetate. Am J Obstet Gynecol. 1988;159(2):450-454. 3407705 10.1016/S0002-9378(88)80106-6
5. Vercellini P Cortesi I Crosignani PG: Progestins for symptomatic endometriosis: a critical analysis of the evidence. Fertil Steril. 1997;68(3):393-401. 9314903 10.1016/S0015-0282(97)00193-3
6. Regidor PA Regidor M Schmidt M: Prospective randomized study comparing the GnRH-agonist leuprorelin acetate and the gestagen lynestrenol in the treatment of severe endometriosis. Gynecol Endocrinol. 2001;15(3):202-209. 11447732
7. Overton CE Lindsay PC Johal B: A randomized, double-blind, placebo-controlled study of luteal phase dydrogesterone (Duphaston) in women with minimal to mild endometriosis. Fertil Steril. 1994;62(4):701-707. 7926076
8. Bulun SE Cheng YH Yin P: Progesterone resistance in endometriosis: link to failure to metabolize estradiol. Mol Cell Endocrinol. 2006;248(1-2):94-103. 16406281 10.1016/j.mce.2005.11.041
9. Attia GR Zeitoun K Edwards D: Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab. 2000;85(8):2897-2902. 10946900 10.1210/jcem.85.8.6739
10. D'Antonio M Martelli F Peano S: Ability of recombinant human TNF binding protein-1 (r-hTBP-1) to inhibit the development of experimentally-induced endometriosis in rats. J Reprod Immunol. 2000;48(2):81-98. 11011074 10.1016/S0165-0378(00)00073-5
11. D'Hooghe TM Nugent NP Cuneo S: Recombinant human TNFRSF1A (r-hTBP1) inhibits the development of endometriosis in baboons: a prospective, randomized, placebo- and drug-controlled study. Biol Reprod. 2006;74(1):131-136. 16177224 10.1095/biolreprod.105.043349
12. Falconer H Mwenda JM Chai DC: Treatment with anti-TNF monoclonal antibody (c5N) reduces the extent of induced endometriosis in the baboon. Hum Reprod. 2006;21(7):1856-1862. 16517562 10.1093/humrep/del044
13. Kyama CM Overbergh L Mihalyi A: Effect of recombinant human TNF-binding protein-1 and GnRH antagonist on mRNA expression of inflammatory cytokines and adhesion and growth factors in endometrium and endometriosis tissues in baboons. Fertil Steril. 2008;89(5 Suppl):1306-1313. 18061171 10.1016/j.fertnstert.2006.11.205
14. Eisermann J Gast MJ Pineda J: Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery. Fertil Steril. 1988;50(4):573-579. 2971579
15. Kennan JA Chen TT Chadwell NL: IL-1 beta, TNF-alpha, and IL-2 in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am J Reprod Immunol. 1995;34(6):381-385. 8607944 10.1111/j.1600-0897.1995.tb00968.x
16. Li B Jin F Yang L: [Evaluation of tumor necrosis factor-alpha and interleukin-6 levels in serum and peritoneal fluid of patients with endometriosis]. Zhonghua Fu Chan Ke Za Zhi. 2000;35(3):166-168. 11775897
17. Pizzo A Salmeri FM Ardita FV: Behaviour of cytokine levels in serum and peritoneal fluid of women with endometriosis. Gynecol Obstet Invest. 2002;54(2):82-87. 12566749 10.1159/000067717
18. Rana N Braun DP House R: Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis. Fertil Steril. 1996;65(5):925-930. 8612850
19. Bergqvist A Nejaty H Fröysa B: Production of interleukins 1beta, 6 and 8 and tumor necrosis factor alpha in separated and cultured endometrial and endometriotic stromal and epithelial cells. Gynecol Obstet Invest. 2000;50(1):1-6. 10895019 10.1159/000010269
20. Zhang RJ Wild RA Ojago JM: Effect of tumor necrosis factor-alpha on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system. Fertil Steril. 1993;59(6):1196-1201. 8495765 F1000 Recommendation
21. Sillem M Prifti S Koch A: Regulation of matrix metalloproteinases and their inhibitors in uterine endometrial cells of patients with and without endometriosis. Eur J Obstet Gynecol Reprod Biol. 2001;95(2):167-174. 11301163 10.1016/S0301-2115(00)00415-2 F1000 Recommendation
22. Grund EM Kagan D Tran CA: Tumor necrosis factor-alpha regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor kappaB in human endometriotic epithelial cells. Mol Pharmacol. 2008;73(5):1394-1404. 18252806 10.1124/mol.107.042176 F1000 Recommendation
23. Lu D Song H Shi G: Anti-TNF-α treatment for pelvic pain associated with endometriosis. Cochrane Database Syst Rev. 2013;3:CD008088. 23543560 10.1002/14651858.CD008088.pub3 F1000 Recommendation
24. Berkley KJ Dmitrieva N Curtis KS: Innervation of ectopic endometrium in a rat model of endometriosis. Proc Natl Acad Sci U S A. 2004;101(30):11094-11098. 15256593 10.1073/pnas.0403663101 491992 F1000 Recommendation
25. Liu M Liu X Zhang Y: Valproic acid and progestin inhibit lesion growth and reduce hyperalgesia in experimentally induced endometriosis in rats. Reprod Sci. 2012;19(4):360-373. 22344726 10.1177/1933719111424453 F1000 Recommendation
26. Arosh JA Lee J Balasubbramanian D: Molecular and preclinical basis to inhibit PGE 2 receptors EP2 and EP4 as a novel nonsteroidal therapy for endometriosis. Proc Natl Acad Sci U S A. 2015;112(31):9716-9721. 26199416 10.1073/pnas.1507931112 4534219 F1000 Recommendation
27. Kats R Collette T Metz CN: Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis. Fertil Steril. 2002;78(1):69-76. 12095493 10.1016/S0015-0282(02)03189-8
28. Morin M Bellehumeur C Therriault MJ: Elevated levels of macrophage migration inhibitory factor in the peripheral blood of women with endometriosis. Fertil Steril. 2005;83(4):865-872. 15820792 10.1016/j.fertnstert.2004.10.039
29. Akoum A Kong J Metz C: Spontaneous and stimulated secretion of monocyte chemotactic protein-1 and macrophage migration inhibitory factor by peritoneal macrophages in women with and without endometriosis. Fertil Steril. 2002;77(5):989-994. 12009356 10.1016/S0015-0282(02)03082-0
30. Kats R Metz CN Akoum A: Macrophage migration inhibitory factor is markedly expressed in active and early-stage endometriotic lesions. J Clin Endocrinol Metab. 2002;87(2):883-889. 11836337 10.1210/jcem.87.2.8260
31. Akoum A Metz CN Al-Akoum M: Macrophage migration inhibitory factor expression in the intrauterine endometrium of women with endometriosis varies with disease stage, infertility status, and pelvic pain. Fertil Steril. 2006;85(5):1379-1385. 16616746 10.1016/j.fertnstert.2005.10.073
32. Veillat V Sengers V Metz CN: Macrophage migration inhibitory factor is involved in a positive feedback loop increasing aromatase expression in endometriosis. Am J Pathol. 2012;181(3):917-927. 22759564 10.1016/j.ajpath.2012.05.018 F1000 Recommendation
33. Graham A Falcone T Nothnick WB: The expression of microRNA-451 in human endometriotic lesions is inversely related to that of macrophage migration inhibitory factor (MIF) and regulates MIF expression and modulation of epithelial cell survival. Hum Reprod. 2015;30(3):642-652. 25637622 10.1093/humrep/dev005 4325675
34. Chesney J Metz C Bacher M: An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med. 1999;5(3):181-191. 10404515 2230298
35. Yang Y Degranpré P Kharfi A: Identification of macrophage migration inhibitory factor as a potent endothelial cell growth-promoting agent released by ectopic human endometrial cells. J Clin Endocrinol Metab. 2000;85(12):4721-4727. 11134134 10.1210/jcem.85.12.7003 F1000 Recommendation
36. Carli C Metz CN Al-Abed Y: Up-regulation of cyclooxygenase-2 expression and prostaglandin E 2 production in human endometriotic cells by macrophage migration inhibitory factor: involvement of novel kinase signaling pathways. Endocrinology. 2009;150(7):3128-3137. 19299454 10.1210/en.2008-1088 2703510
37. Veillat V Carli C Metz CN: Macrophage migration inhibitory factor elicits an angiogenic phenotype in human ectopic endometrial cells and triggers the production of major angiogenic factors via CD44, CD74, and MAPK signaling pathways. J Clin Endocrinol Metab. 2010;95(12):E403-412. 20829186 10.1210/jc.2010-0417
38. Bernhagen J Calandra T Cerami A: Macrophage migration inhibitory factor is a neuroendocrine mediator of endotoxaemia. Trends Microbiol. 1994;2(6):198-201. 8087451
39. Cao WG Morin M Sengers V: Tumour necrosis factor-alpha up-regulates macrophage migration inhibitory factor expression in endometrial stromal cells via the nuclear transcription factor NF-kappaB. Hum Reprod. 2006;21(2):421-428. 16210389 10.1093/humrep/dei315
40. Nothnick WB Colvin A Cheng KF: Inhibition of macrophage migration inhibitory factor reduces endometriotic implant size in mice with experimentally induced disease. J Endometr. 2011;3(3):135-142. 24790725 4002052
41. Khoufache K Bazin S Girard K: Macrophage migration inhibitory factor antagonist blocks the development of endometriosis in vivo. PLoS One. 2012;7(5):e37264. 22649515 10.1371/journal.pone.0037264 3359359 F1000 Recommendation
42. Rakhila H Girard K Leboeuf M: Macrophage migration inhibitory factor is involved in ectopic endometrial tissue growth and peritoneal-endometrial tissue interaction in vivo: a plausible link to endometriosis development. PLoS One. 2014;9(10):e110434. 25329068 10.1371/journal.pone.0110434 4201552 F1000 Recommendation
43. Leng L Metz CN Fang Y: MIF signal transduction initiated by binding to CD74. J Exp Med. 2003;197(11):1467-1476. 12782713 10.1084/jem.20030286 2193907
44. Wu MH Lu CW Chuang PC: Prostaglandin E 2: the master of endometriosis? Exp Biol Med (Maywood). 2010;235(6):668-677. 20511671 10.1258/ebm.2010.009321 F1000 Recommendation
45. Ota H Igarashi S Sasaki M: Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis. Hum Reprod. 2001;16(3):561-566. 11228229 10.1093/humrep/16.3.561
46. Rakhila H Carli C Daris M: Identification of multiple and distinct defects in prostaglandin biosynthetic pathways in eutopic and ectopic endometrium of women with endometriosis. Fertil Steril. 2013;100(6):1650-9.e1-2. 24035605 10.1016/j.fertnstert.2013.08.016
47. Wu MH Sun HS Lin CC: Distinct mechanisms regulate cyclooxygenase-1 and -2 in peritoneal macrophages of women with and without endometriosis. Mol Hum Reprod. 2002;8(12):1103-1110. 12468643 10.1093/molehr/8.12.1103
48. De Leon FD Vijayakumar R Brown M: Peritoneal fluid volume, estrogen, progesterone, prostaglandin, and epidermal growth factor concentrations in patients with and without endometriosis. Obstet Gynecol. 1986;68(2):189-194. 3488529
49. Banu SK Lee J Speights VO Jr: Selective inhibition of prostaglandin E2 receptors EP2 and EP4 induces apoptosis of human endometriotic cells through suppression of ERK1/2, AKT, NFkappaB, and beta-catenin pathways and activation of intrinsic apoptotic mechanisms. Mol Endocrinol. 2009;23(8):1291-1305. 19407222 10.1210/me.2009-0017 F1000 Recommendation
50. Lee J Banu SK Burghardt RC: 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. 23242524 10.1095/biolreprod.112.100883 4013861 F1000 Recommendation
51. Lee J Banu SK Rodriguez R: Selective blockade of prostaglandin E 2 receptors EP2 and EP4 signaling inhibits proliferation of human endometriotic epithelial cells and stromal cells through distinct cell cycle arrest. Fertil Steril. 2010;93(8):2498-2506. 20207353 10.1016/j.fertnstert.2010.01.038 F1000 Recommendation
52. Lee J Banu SK Subbarao T: Selective inhibition of prostaglandin E2 receptors EP2 and EP4 inhibits invasion of human immortalized endometriotic epithelial and stromal cells through suppression of metalloproteinases. Mol Cell Endocrinol. 2011;332(1-2):306-313. 21111772 10.1016/j.mce.2010.11.022 F1000 Recommendation
53. Laschke MW Elitzsch A Scheuer C: Selective cyclo-oxygenase-2 inhibition induces regression of autologous endometrial grafts by down-regulation of vascular endothelial growth factor-mediated angiogenesis and stimulation of caspase-3-dependent apoptosis. Fertil Steril. 2007;87(1):163-171. 17081538 10.1016/j.fertnstert.2006.05.068 F1000 Recommendation
54. Cobellis L Razzi S De Simone S: The treatment with a COX-2 specific inhibitor is effective in the management of pain related to endometriosis. Eur J Obstet Gynecol Reprod Biol. 2004;116(1):100-102. 15294376 10.1016/j.ejogrb.2004.02.007 F1000 Recommendation
55. Brandenberger AW Lebovic DI Tee MK: Oestrogen receptor (ER)-alpha and ER-beta isoforms in normal endometrial and endometriosis-derived stromal cells. Mol Hum Reprod. 1999;5(7):651-655. 10381820 10.1093/molehr/5.7.651
56. Fujimoto J Hirose R Sakaguchi H: Expression of oestrogen receptor-alpha and -beta in ovarian endometriomata. Mol Hum Reprod. 1999;5(8):742-747. 10421802 10.1093/molehr/5.8.742
57. Xue Q Lin Z Cheng YH: Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol Reprod. 2007;77(4):681-687. 17625110 10.1095/biolreprod.107.061804 F1000 Recommendation
58. Trukhacheva E Lin Z Reierstad S: Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis. J Clin Endocrinol Metab. 2009;94(2):615-622. 19001520 10.1210/jc.2008-1466 2646522 F1000 Recommendation
59. Bulun SE Monsavais D Pavone ME: Role of estrogen receptor-β in endometriosis. Semin Reprod Med. 2012;30(1):39-45. 22271293 10.1055/s-0031-1299596 4034571
60. Harris HA Bruner-Tran KL Zhang X: A selective estrogen receptor-beta agonist causes lesion regression in an experimentally induced model of endometriosis. Hum Reprod. 2005;20(4):936-941. 15618247 10.1093/humrep/deh711 F1000 Recommendation
61. Zhao Y Gong P Chen Y: Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis. Sci Transl Med. 2015;7(271):271ra9. 25609169 10.1126/scitranslmed.3010626 F1000 Recommendation
62. Han SJ Jung SY Wu SP: Estrogen Receptor β Modulates Apoptosis Complexes and the Inflammasome to Drive the Pathogenesis of Endometriosis. Cell. 2015;163(4):960-974. 26544941 10.1016/j.cell.2015.10.034 4640214 F1000 Recommendation