Peritoneal endometriosis is an inflammatory disease

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 1, 2012, Pages 23-40

  Lousse, Jean Christophe ^a   Van Langendonckt, Anne ^a   Defrere, Sylvie ^a   Gonzalez Ramos, Reinaldo ^a   Colette, Sebastien ^a   Donnez, Jacques ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Inflammation; Iron; Macrophages; Medical treatment; NF kappa B; Oxidative stress; Peritoneal endometriosis; Prostaglandins; Review

Indexed keywords

ALPHA TOCOPHEROL; ANGIOGENIC FACTOR; ASCORBIC ACID; BILIRUBIN; CELECOXIB; CYCLIC AMP; DEFEROXAMINE; FERRITIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HEPCIDIN; ICOSANOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; IRON; MONOCYTE CHEMOTACTIC PROTEIN; PROSTAGLANDIN; PROSTAGLANDIN RECEPTOR; REACTIVE OXYGEN METABOLITE; SECRETORY PHOSPHOLIPASE A2; SUPEROXIDE DISMUTASE; TAURINE; TRANSFERRIN; TRANSFERRIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL DAMAGE; CELL PROLIFERATION; CHRONIC INFLAMMATION; ENDOMETRIOSIS; ENDOMETRIUM CELL; ERYTHROCYTE; FENTON REACTION; HUMAN; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY DISEASE; IRON METABOLISM; IRON OVERLOAD; MAST CELL; MENSTRUAL CYCLE; MENSTRUATION; MESOTHELIUM; MESOTHELIUM CELL; MOLECULAR INTERACTION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PERITONEAL CAVITY; PERITONEAL DISEASE; PERITONEAL FLUID; PERITONEUM MACROPHAGE; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UTERUS MALFORMATION; FEMALE; INFLAMMATION; METABOLISM; PATHOLOGY; REVIEW;

ENDOMETRIOSIS; FEMALE; HUMANS; INFLAMMATION; IRON; NF-KAPPA B; PERITONEAL DISEASES; PROSTAGLANDINS;

EID: 84860851712     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: 10.2741/358     Document Type: Article

References (151)

1. J. Donnez, F. Chantraine and M. Nisolle: The efficacy of medical and surgical treatment of endometriosis-associated infertility: arguments in favour of a medico-surgical aproach. Hum Reprod Update 8, 89-94 (2002)
2. M. Nisolle and J. Donnez: Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three ifferent entities. Fertil Steril 68, 585-596 (1997)
3. L.C. Giudice and L.C. Kao: Endometriosis. Lancet 364, 1789-1799 (2004)
4. J. Halme, M.G. Hammond, J.F. Hulka, S.G. Raj and L.M. Talbert: Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 64, 151- 154 (1984)
5. J.A. Sampson: Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 14, 422-469 (1927)
6. J.C. Lousse, S. Defrère, R. González Ramos, A. Van Langendonckt, S. Colette and J. Donnez: Involvement of iron, nuclear factor-kappa B (NF-kappa B) and prostaglandins in the pathogenesis of peritoneal endometriosis-associated inflammation: a review. J Endometr 1, 19-29 (2009)
7. R. Gazvani and A. Templeton: Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis. Reproduction 123, 217-226 (2002)
8. A. Van Langendonckt, F. Casanas-Roux and J. Donnez: Oxidative stress and peritoneal endometriosis. Fertil Steril 77, 861-870 (2002)
9. C.H. Syrop and J. Halme: Cyclic changes of peritoneal fluid parameters in normal and infertile patients. Obstet Gynecol 69, 416-418 (1984)
10. E. Oral, D.L. Olive, A. Arici: The peritoneal environment in endometriosis. Hum Reprod Update 2, 385- 398 (1996)
11. A. Akoum, A. Lemay, C. Brunet and J. Hébert: Secretion of monocyte chemotactic protein-1 by cytokinestimulated endometrial cells of women with endometriosis. Le groupe d'investigation en gynécologie. Fertil Steril 63, 322-328 (1995)
12. A. Arici, E. Oral, O. Bukulmez, S. Buradagunta, O. Bahtiyar and E.E. Jones: Monocyte chemotactic protein-1 expression in human preovulatory follicles and ovarian cells. J Reprod Immunol 32, 201-219 (1997)
13. D. Hornung, I.P. Ryan, V.A. Chao, J.L. Vigne, E.D. Schriock and R.N. Taylor: Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells. J Clin Endocrinol Metab 82, 1621-1628 (1997)
14. C.M. Kyama, L. Overbergh, S. Debrock, D. Valckx, S. Vander Perre, C. Meuleman, A. Mihalyi, J.M. Mwenda, C. Mathieu and T.M. D'Hooghe: Increased peritoneal and endometrial gene expression of biologically relevant cytokines and growth factors during the menstrual phase in women with endometriosis. Fertil Steril 85, 1667-1675 (2006)
15. T. Harada, T. Iwabe and N. Terakawa: Role of cytokines in endometriosis. Fertil Steril 76, 1-10 (2001)
16. A. Agarwal, S. Gupta and S. Sikka: The role of oxidative stress in endometriosis. Curr Opin Obstet Gynecol 18, 325-332 (2006)
17. S. Hippeli and E.F. Elstner: Transitional metal ioncatalyzed oxygen activation during pathogenic processes. FEBS Lett 443, 1-7 (1999)
18. B. Halliwell and J.M. Gutteridge: Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186, 1-85 (1990)
19. B.P. Yu: Cellular defenses against damage from reactive oxygen species. Physiol Rev 74, 139-159 (1994)
20. J.M. Zeller, I. Henig, E. Radwanska and W.P. Dmowski: Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am J Reprod Immunol Microbiol 13,78-82 (1987)
21. H. Ota, S. Igarashi and T. Tanaka: Xanthine oxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis. Fertil Steril 75, 785-790 (2001)
22. D.M. Portz, T.E. Elkins, R. White, J. Warren, S. Adadevoh and J. Randolph: Oxygen free radicals and pelvic adhesion formation: blocking oxygen free radical toxicity to prevent adhesion formation in an endometriosis model. Int J Fertil 36, 39-42 (1991)
23. Y. Wang, R.K. Sharma, T. Falcone, J. Goldberg and A. Agarwal: Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil Steril 68, 826-830 (1997)
24. H.N. Ho, M.Y. Wu, S.U. Chen, K.H. Chao, C.D. Chen and Y.S. Yang: Total antioxidant status and nitric oxide do not increase in peritoneal fluids from women with endometriosis. Hum Reprod 12, 2810-2815 (1997)
25. G. Polak, M. Koziol-Montewka, M. Gogacz, I. Blaszkowska and J. Kotarski: Total antioxidant status of the peritoneal fluid in infertile women. Eur J Obstet Gynecol Reprod Biol 94, 261-263 (2001)
26. K. Arumugam and Y.C. Yip: De novo formation of adhesions in endometriosis: the role of iron and free radical reactions. Fertil Steril 64, 62-64 (1995)
27. A.A. Murphy, N. Santanam and S. Parthasarathy: Endometriosis: a disease of oxidative stress? Semin Reprod Endocrinol 16, 263-73 (1998)
28. T.M. Buttke and P.A. Sandstrom: Oxidative stress as a mediator of apoptosis. Immunol Today 15, 7-10 (1994)
29. T.P. Dalton, H.G. Shertzer and A. Puga: Regulation of gene expression by reactive oxygen. Annu Rev Pharmacol Toxicol 39, 67-101 (1999)
30. P. Viatour, M.P. Merville, V. Bours and A. Chariot: Phosphorylation of NF-kappa B and I-kappa B proteins: implications in cancer and inflammation. Trends Biochem Sci 30, 43-52 (2005)
31. M.H. Wu, Y. Shoji, P. Chuang and S. Tsai: Endometriosis: disease pathophysiology and the role of prostaglandins. Expert Rev Mol Med 9, 1-20 (2007)
32. R. Crichton, S. Wilmet, R. Legssyer and R.J. Ward: Molecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells. J Inorg Biochem 91, 9-18 (2002)
33. A. Van Langendonckt, F. Casanas-Roux and J. Donnez: Iron overload in the peritoneal cavity of women with pelvic endometriosis. Fertil Steril 78, 712-718 (2002)
34. K. Arumugam: Endometriosis and infertility: raised iron concentration in the peritoneal fluid and its effect on the acrosome reaction. Hum Reprod 9, 1153-1157 (1994)
35. J.C. Louse, S. Defrère, A. Van Langendonckt, J. Gras, R. González Ramos, S. Colette and J. Donnez: Iron storage is significantly increased in peritoneal macrophages of endometriosis patients and correlates with iron overload in peritoneal fluid. Fertil Steril 91, 1668-1675 (2009)
36. S.P. Mathur, J.H. Lee, H. Jiang, P. Arnaud and P.F. Rust: Levels of transferrin and alpha 2-HS glycoprotein in women with and without endometriosis. Autoimmunity 29, 121-127 (1999)
37. A. Van Langendonckt, F. Casanas-Roux, M.M. Dolmans and J. Donnez: Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 77, 561-70 (2002)
38. T. Ganz: Hepcidin-a regulator of intestinal iron absorption and iron recycling by macrophages. Best Pract Res Clin Haematol 18, 171-182 (2005)
39. C. Peyssonnaux, A.S. Zinkernagel, V. Datta, X. Lauth, R.S. Johnson and V. Nizet: TLR4-dependent hepcidin expression by myeloid cells in response to bacterial pathogens. Blood 107, 3727-3732 (2006)
40. N.B. Nguyen, K.D. Callaghan, A.J. Ghio, D.J. Haile and F. Yang: Hepcidin expression and iron transport in alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 291, 417- 425 (2006)
41. V. Petrozza, F.M. Magliocca, S. Pulvirenti, G. Massimi, C. de Salazar and F. Carpino: Asymptomatic peritoneal endometriosis following cesarean section. Minerva Ginecol 45, 349-353 (1993)
42. A. Van Langendonckt, F. Casanas-Roux, J. Eggermont and J. Donnez: Characterization of iron deposition in endometriotic lesions induced in the nude mouse model. Hum Reprod 19, 1265-1271 (2004)
43. A. Gaulier, A. Jouret-Mourin, C. Marsan: Peritoneal endometriosis: report of a case with cytologic, cytochemical and histopathologic study. Acta Cytol 27, 446-449 (1983)
44. K.L. Sharpe-Timms, E.A. Ricke, M. Piva and G.M. Horowitz: Differential expression and localization of denovo synthesized endometriotic haptoglobin in endometrium and endometriotic lesions. Hum Reprod 15, 2180-2185 (2000)
45. M. Piva, G.M. Horowitz and K.L. Sharpe-Timms: 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 86, 2553-2561 (2001)
46. S. Martínez-Román, J. Balasch, M. Creus, F. Fábregues, F. Carmona, R. Vilella and J.A. Vanrell: Transferrin receptor (CD71) expression in peritoneal macrophages from fertile and infertile women with and without endometriosis. Am J Reprod Immunol 38, 413-417 (1997)
47. K.L. Sharpe-Timms, R.L. Zimmer, E.A. Ricke, M. Piva, G.M. Horowitz: Endometriotic haptoglobin binds to peritoneal macrophages and alters their function in women with endometriosis. Fertil Steril 78, 810-819 (2002)
48. S. Defrère, A. Van Langendonckt, S. Vaesen, M. Jouret, R. González Ramos, D. Gonzalez and J. Donnez: Iron overload enhances epithelial cell proliferation in endometriotic lesions induced in a murine model. Hum Reprod 21, 2810-2816 (2006)
49. M. Knutson and M. Wessling-Resnick: Iron metabolism in the reticuloendothelial system. Crit Rev Biochem Mol Biol 38, 61-88 (2003)
50. H. Mizuuchi, R. Kudo, H. Tamura, K. Tsukahara, N. Tsumura, K. Kumai and K. Sato: Identification of transferrin receptor in cervical and endometrial tissues. Gynecol Oncol 31, 292-300 (1988)
51. S. Defrère, J.C. Lousse, R. González Ramos, S. Colette, J. Donnez and A. Van Langendonckt: Potential involvement of iron in the pathogenesis of peritoneal endometriosis. Mol Hum Reprod 14, 377-385 (2008)
52. R. Crichton: Inorganic biochemistry of iron metabolism: from molecular mechanisms to clinical consequences. John Wiley and Sons, Chichester (2001)
53. G. Balla, H.S. Jacob, J. Balla, M. Rosenberg, K. Nath, F. Apple, J.W. Eaton and G.M. Vercellotti: Ferritin: a cytoprotective antioxidant stratagem of endothelium. J Biol Chem 267, 18148-18153 (1992)
54. R.J. Ward, S. Wilmet, R. Legssyer and R.R. Crichton: The influence of iron homoeostasis on macrophage function. Biochem Soc Trans 30, 762-765 (2002)
55. A.Y. Demir, P.G. Groothuis, A.W. Nap, C. Punyadeera, A.F. de Goeij, J.L. Evers and G.A. Dunselman: Menstrual effluent induces epithelial-mesenchymal transitions in mesothelial cells. Hum Reprod 19, 21-29 (2004)
56. T.F. Tam, R. Leung-Toung, W. Li, Y. Wang, K. Karimian and M. Spino: Iron chelator research: past, present and future. Curr Med Chem 10, 983-995 (2003)
57. J.S. Sanfilippo, N.G. Wakim, K.N. Schikler, M.A. Yussman: Endometriosis in association with uterine anomaly. Am J Obstet Gynecol 154, 39-43 (1986)
58. S.L. Darrow, J.E. Vena, R.E. Batt, M.A. Zielezny, A.M. Michalek, S. Selman: Menstrual cycle characteristics and the risk of endometriosis. Epidemiology 4, 135-142 (1993)
59. P. Vercellini, O. De Giorgi, G. Aimi, S. Panazza, A. Uglietti and P.G. Crosignani: Menstrual characteristics in women with and without endometriosis. Obstet Gynecol 90, 264-268 (1997)
60. D. Vinatier, G. Orzi, M. Cosson and P. Dufour: Theories of endometriosis. Eur J Obstet Gynecol Reprod Biol 96, 21-34 (2001)
61. K. Arumugam and J.M. Lim: Menstrual characteristics associated with endometriosis. Br J Obstet Gynaecol 104, 948-950 (1997)
62. R. González Ramos, J. Donnez, S. Defrère, I. Leclerq, J. Squifflet, J.C. Lousse and A. Van Langendonckt: Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis. Mol Hum Reprod 13, 503-509 (2007)
63. J.C. Lousse, A. Van Langendonckt, R. González Ramos, S. Defrère, E. Renkin and J. Donnez: Increased activation of nuclear factor-kappa B (NF-kappa B) in isolated peritoneal macrophages of patients with endometriosis. Fertil Steril 90, 217-220 (2008)
64. M. Karin: Nuclear factor-kappa B in cancer development and progression. Nature 441, 431-436 (2006)
65. M. Karin, Y. Yamamoto and Q.M. Wang: The IKK NFkappa B system: a treasure trove for drug development. Nat Rev Drug Discov 3, 17-26 (2004)
66. A. Hoffmann and D. Baltimore: Circuitry of nuclear factor κB signaling. Immunol Rev 210, 171-186 (2006)
67. R. González Ramos, A. Van Langendonckt, S. Defrère, J.C. Lousse, S. Colette, L. Devoto and J. Donnez: Involvement of the nuclear factor-kappaB (NF-kappa B) pathway in the pathogenesis of endometriosis. Fertil Steril online Feb 24 (2010)
68. S.M. Laird, E.M. Tuckerman, B.A. Cork and T.C. Li: Expression of nuclear factor kappa B in human endometrium; role in the control of interleukin 6 and leukaemia inhibitory factor production. Mol Hum Reprod 6, 34-40 (2000)
69. M. Page, E.M. Tuckerman, T.C. Li and S.M. Laird: Expression of nuclear factor kappa-B components in human endometrium. J Reprod Immunol 54, 1-13 (2002)
70. A.E. King, H. Critchley and R.W. Kelly: The NF-kappa B pathway in human endometrium and first trimester decidua. Mol Hum Reprod 7, 175-183 (2001)
71. C. Ponce, M. Torres, C. Galleguillos, H. Sovino, M.A. Boric, A. Fuentes and M.C. Johnson: Nuclear factor-kappa B pathway and interleukin-6 are affected in eutopic endometrium of women with endometriosis. Reproduction 137, 727-737 (2009)
72. C.A. Witz: Cell adhesion molecules and endometriosis. Semin Reprod Med 21, 173-182 (2003)
73. R. Zhang, R.A. Wild and J.M. Ojago: Effect of tumor necrosis factor-alpha on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system. Fertil Steril 59, 1196-1201 (1993)
74. J.S. Griffith, A.K. Rodgers, R.S. Schenken: Reviews: In vitro models to study the pathogenesis of endometriosis. Reprod Sci 17, 5-12 (2010)
75. B.B. Aggarwal: Nuclear factor-kappa B: the enemy within. Cancer Cell 6, 203-208 (2004)
76. A.R. Farina, A. Tacconelli, A. Vacca, M. Maroder, A. Gulino and A.R. Mackay: Transcriptional up-regulation of matrix metalloproteinase-9 expression during spontaneous epithelial to neuroblast phenotype conversion by SK-N-SH neuroblastoma cells, involved in enhanced invasivity, depends upon GT-box and nuclear factor kappa B elements. Cell Growth Differ 10, 353-367 (1999)
77. A.S. Baldwin: Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappa B. J Clin Invest 107, 241-246 (2001)
78. E. Andreakos, C. Smith, S. Kiriakidis, C. Monaco, R.de Martin, F.M. Brennan, E. Paleolog, M. Feldmann and B.M. Foxwell: Heterogeneous requirement of IkappaB kinase 2 for inflammatory cytokine and matrix metalloproteinase production in rheumatoid arthritis: implications for therapy. Arthritis Rheum 48, 1901-1912 (2003)
79. E.M. Grund, D. Kagan, C.A. Tran, A. Zeitvogel, A. Starzinski-Powitz, S. Nataraja and S.S. Palmer: Tumor necrosis factor-alpha regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor kappa B in human endometriotic epithelial cells. Mol Pharmacol 73, 1394- 1404 (2008)
80. R. González Ramos, A. Van Langendonckt, S. Defrère, J.C. Lousse, M. Mettlen, A. Guillet and J. Donnez: Agents blocking the nuclear factor-kappa B (NF-kappa B) pathway are effective inhibitors of endometriosis in an in vivo experimental model. Gynecol Obstet Invest 65, 174-186 (2008)
81. J. McLaren, A. Prentice, D.S. Charnock-Jones, S.K. Smith: Vascular endothelial growth factor (VEGF) concentrations are elevated in peritoneal fluid of women with endometriosis. Hum Reprod 11, 220-223 (1996)
82. Y. Sakamoto, T. Harada, S. Horie, Y. Iba, F. Taniguchi, S. Yoshida, T. Iwabe and N. Terakawa: Tumor necrosis factoralpha- induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kappa B activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab 88, 730-735 (2003)
83. Y. Ohama, T. Harada, T. Iwabe, F. Taniguchi, Y. Takenaka and N. Terakawa: Peroxisome proliferator-activated receptor-gamma ligand reduced tumor necrosis factor-alphainduced interleukin-8 production and growth in endometriotic stromal cells. Fertil Steril 89, 311-317 (2008)
84. O. Celik, S. Hascalik, K. Elter, M.E. Tagluk, B. Gurates and N.E. Aydin: Combating endometriosis by blocking proteasome and nuclear factor-kappa B pathways. Hum Reprod 23, 2458-2465 (2008)
85. F.D. De Leon, R. Vijayakumar, M. Brown, C.V. Rao, M.A. Yussman and G. Schultz: Peritoneal fluid volume, estrogen, progesterone, prostaglandin, and epidermal growth factor concentrations in patients with and without endometriosis. Obstet Gynecol 68, 189-194 (1986)
86. M.H. Wu, H.S. Sun, C.C. Lin, K.Y. Hsiao, P.C. Chuang, H.A. Pan and S.J. Tsai: Distinct mechanisms regulate cyclooxygenase-1 and -2 in peritoneal macrophages of women with and without endometriosis. Mol Hum Reprod 8, 1103- 1110 (2002)
87. M. Yamaguchi and N. Mori: Prostaglandin and leukotriene concentration of the peritoneal fluid of endometriosis and other gynecologic disorders in the secretory phase. Prostaglandins Leukot Essent Fatty Acids 39, 43-45 (1990)
88. M. Peters-Golden and W. Henderson: Leukotrienes. New Engl J Med 357, 1841-1854 (2007)
89. E.M. Smyth, T. Grosser, M. Wang, Y. Yu and G.A. FitzGerald: Prostanoids in health and disease. J Lipid Res 50, S423-S428 (2009)
90. M. Tsujii and R.N. DuBois: Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell 83, 493-501 (1995)
91. M. Tsujii, S. Kawano, S. Tsuji, H. Sawaoka, M. Hori and R.N. DuBois: Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93, 705-716 (1998)
92. M. Tsujii, S. Kawano, R.N. DuBois: Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc Natl Acad Sci USA 94, 3336-3340 (1997)
93. D.L. DeWitt: Prostaglandin endoperoxide synthase: regulation of enzyme expression. Biochim Biophys Acta 1083, 121-134 (1991)
94. M. Murakami and I. Kudo: Recent advances in molecular biology and physiology of the prostaglandin E2- biosynthetic pathway. Prog Lipid Res 43, 3-35 (2004)
95. T. Lindstrom and P. Bennett: Transcriptional regulation of genes for enzymes of the prostaglandin biosynthetic pathway. Prostaglandins Leukot Essent Fatty Acids 70, 115-135 (2004)
96. K. Sales and H. Jabbour: Cyclooxygenase enzymes and prostaglandins in pathology of the endometrium. Reproduction 126, 559-567 (2003)
97. S. Narumiya, Y. Sugimoto and F. Ushikubi: Prostanoid receptors structures, properties, and functions. Physiol Rev 79, 1193-226 (1999)
98. B. Ashby: Co-expression of prostaglandin receptors with opposite effects: a model for homeostatic control of autocrine and paracrine signalling. Biochem Pharmacol 55, 239-246 (1998)
99. C.R. Kennedy, Y. Zhang, S. Brandon, Y. Guan, K. Coffee, C.D. Funk, M.A. Magnuson, J.A. Oates, M.D. Breyer and R.M. Breyer: Salt-sensitive hypertension and reduced fertility in mice lacking the prostaglandin EP2 receptor. Nat Med 5,217-220 (1999)
100. S. Narumiya and G.A. FitzGerald: Genetic and pharmacological analysis of prostanoid receptor function. J Clin Invest 108, 25-30 (2001)
101. S. Ferreira and J. Vane: Half-lives of peptides and amines in the circulation. Nature 215, 1237-1240 (1967)
102. J.C. Lousse, S. Defrère, S. Colette, A. Van Langendonckt, J. Donnez: Expression of eicosanoid biosynthetic and catabolic enzymes in peritoneal endometriosis. Hum Reprod 25, 734-741 (2010)
103. S. Smith: Prostaglandins and growth factors in the endometrium. Baillieres Clin Obstet Gynaecol 3, 249-270 (1989)
104. H. Ota, S. Igarashi, M. Sasaki and T. Tanaka: Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis. Hum Reprod 16, 561-566 (2001)
105. F. Chishima, S. Hayakawa, K. Sugita, N. Kinukawa, S. Aleemuzzaman, N. Nemoto, T. Yamamoto and M. Honda: Increased expression of cyclooxygenase-2 in local lesions of endometriosis patients. Am J Reprod Immunol 48, 50-56 (2002)
106. F. Chishima, S. Hayakawa, T. Yamamoto, M. Sugitani, M. Karasaki-Suzuki, K. Sugita and N. Nemoto: Expression of inducible microsomal prostaglandin E synthase in local lesions of endometriosis patients. Am J Reprod Immunol 57, 218-226 (2007)
107. M.H. Wu, C. Wang, C. Lin, L. Chen, W. Chang and S. Tsai: Distinct regulation of cyclooxygenase-2 by interleukin-1 beta in normal and endometriotic stromal cells. J Clin Endocrinol Metab 90, 286-295 (2005)
108. O. Bukulmez, D. Hardy, B. Carr, A. Word and C. Mendelson: Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology 149, 1190-1204 (2008)
109. Y.J. Kang, U.R. Mbonye, C.J. DeLong, M. Wada and W.L. Smith: Regulation of intracellular cyclooxygenase levels by gene transcription and protein degradation. Prog Lipid Res 46, 108-125 (2007)
110. T.O. Ishikawa, N. Jain, H.R. Herschman: Feedback regulation of cyclooxygenase-2 transcription ex vivo and in vivo. Biochem Biophys Res Commun 378, 534-538 (2009).
111. C. Olivares, M. Bilotas, R. Buquet, M. Borghi, C. Sueldo, M. Tesone and G. Meresman: Effects of a selective cyclooxygenase-2 inhibitor on endometrial epithelial cells from patients with endometriosis. Hum Reprod 23, 2701- 2708 (2008)
112. E.A. Willman, W.P. Collins and S.G. Clayton: Studies in the involvement of prostaglandins in uterine symptomatology and pathology. Br J Obstet Gynaecol 83, 337-341 (1976)
113. A.T. Koki, N.K. Khan, B.M. Woerner, K. Seibert, J.L. Harmon, A.J. Dannenberg, R.A. Soslow and J.L. Masferrer: Characterization of cyclooxygenase-2 (COX-2) during tumorigenesis in human epithelial cancers: evidence for potential clinical utility of COX-2 inhibitors in epithelial cancers. Prostaglandins Leukot Essent Fatty Acids 66, 13-18 (2002)
114. D.L. DeWitt: Prostaglandin endoperoxide synthase: regulation of enzyme expression. Biochim Biophys Acta 1991;1083:121-34.
115. P.C. Chuang, Y.J. Lin, M.H. Wu, L.Y. Wing, Y. Shoji and S.J. Tsai: Inhibition of CD36-dependent phagocytosis by prostaglandin E2 contributes to the development of endometriosis. Am J Pathol 176, 850-60 (2010)
116. S.K. Banu, J. Lee, V.O. Speights, A. Starzinski-Powitz and J.A. Arosh: Cyclooxygenase-2 regulates survival, migration, and invasion of human endometriotic cells through multiple mechanisms. Endocrinology 149, 1180- 1189 (2008)
117. B.A. Erickson, W.E. Longo, N. Panesar, J.E. Mazuski and D.L. Kaminiski: The effect of selective cyclooxygenase inhibitors on intestinal epithelial cell mitogenesis. Journal of Surgery Research 81, 101-107 (1999)
118. S.A. Milne and H.N. Jabbour: Prostaglandin (PG) F(2alpha) receptor expression and signaling in human endometrium: role of PGF(2alpha) in epithelial cell proliferation. J Clin Endocrinol Metab 88, 1825-1832 (2003)
119. J. Lee, S.K. Banu, R. Rodriguez, A. Starzinski-Powitz and J.A. Arosh: Selective blockade of prostaglandin E2 receptors EP2 and EP4 signaling inhibits proliferation of human endometriotic epithelial cells and stromal cells through distinct cell cycle arrest. Fertil Steril 93, 2498- 2506 (2010)
120. S.K. Banu, J. Lee, V.O. Speights, A. Starzinski-Powitz and J.A. Arosh: Selective inhibition of prostaglandin E2 receptors EP2 and EP4 induces apoptosis of human endometriotic cells through suppression of ERK1/2, AKT, NF-kappa B, and beta-catenin pathways and activation of intrinsic apoptotic mechanisms. Mol Endocrinol 23, 1291- 1305 (2009)
121. G.B. Perchick and H.N. Jabbour: Cyclooxygenase-2 overexpression inhibits cathepsin D-mediated cleavage of plasminogen to the potent antiangiogenic factor angiostatin. Endocrinology 144, 5322-5328 (2003)
122. K.J. Sales, S. Maudsley and H.N. Jabbour. Elevated prostaglandin EP2 receptor in endometrial adenocarcinoma cells promotes vascular endothelial growth factor expression via cyclic 3',5'-adenosine monophosphate-mediated transactivation of the epidermal growth factor receptor and extracellular signal-regulated kinase 1/2 signaling pathways. Mol Endocrinol 18, 1533-1545 (2004)
123. M. Laschke, A. Elitzsch, C. Scheuer, B. Vollmar and M. Menger: Selective cyclo-oxygenase-2 inhibition induces regression of autologous endometrial grafts by downregulation of vascular endothelial growth factor-mediated angiogenesis and stimulation of caspase-3-dependent apoptosis. Fertil Steril 87, 163-171 (2007)
124. D.E. Machado, P.T. Berardo, R.G. Landgraf, P.D. Fernandes, C. Palmero, L.M. Alves, M.S. Abrao and L.E. Nasciutti: A selective cyclooxygenase-2 inhibitor suppresses the growth of endometriosis with an antiangiogenic effect in a rat model. Fertil Steril 93, 2674-2679 (2010)
125. S. Matsuzaki, M. Canis, C. Darcha, R. Dallel, K. Okamura, G. Mage: Cyclooxygenase-2 selective inhibitor prevents implantation of eutopic endometrium to ectopic sites in rats. Fertil Steril 82, 1609-1615 (2004)
126. E. Dogan, U. Sayigili, C. Posaci, B. Tuna, S. Caliskan, S. Altunyurt and B. Saatli: Regression of endometrial explants in rats treated with the cyclooxygenase-2 inhibitor rofecoxib. Fertil Steril 82, 1115-1120 (2004)
127. Y. Ozawa, T. Murakami, M. Tamura, Y. Terada, N. Yaegashi and K. Okamura: A selective cyclooxygenase-2 inhibitor suppresses the growth of endometriosis xenografts via antiangiogenic activity in severe combined immunodeficiency mice. Fertil Steril 86, 1146-1151 (2006)
128. L. Cobellis, S. Razzi, S. De Simone, A. Sartini, A. Fava, S. Danero, W. Gioffrè, M. Mazzini and F. Petraglia: The treatment with a COX-2 specific inhibitor is effective in the management of pain related to endometriosis. Eur J Obstet Gynecol Reprod Biol 116, 100-102 (2004)
129. H. Lim, B.C. Paria, S.K. Das, J.E. Dinchuk, R. Langenbach, J.M. Trzaskos and S.K. Dey: Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91, 197-208 (1997)
130. Y.I. Cha and R.N. DuBois: NSAIDs and cancer prevention: targets down-stream of COX-2. Annu Rev Med 58, 239-252 (2007)
131. M. Triggiani, F. Granata, A. Frattini and G. Marone: Activation of human inflammatory cells by secreted phospholipases A2. Biochim Biophys Acta 1761, 1289- 1300 (2006)
132. M.T. Rizzo, E. Nguyen, M. Aldo-Benson, G. Lambeau: Secreted phospholipase A(2) induces vascular endothelial cell migration. Blood 96, 3809-3815 (2000)
133. S. Beck, G. Lambeau, K. Scholz-Pedretti, M.H. Gelb, M.J. Janssen, S.H. Edwards, D.C. Wilton, J. Pfeilschifter and M. Kaszkin: Potential of tumor necrosis factor alphainduced secreted phospholipase A2 (sPLA2)-IIA expression in mesangial cells by an autocrine loop involving sPLA2 and peroxisome proliferator-activated receptor alpha activation. J Biol Chem 278, 29799-29812 (2003)
134. M.C. Meyer, P. Rastogi, C.S. Beckett and J. McHowat: Phospholipase A2 inhibitors as potential antiinflammatory agents. Curr Pharm Des 11, 1301-1312 (2005)
135. H. Kobayashi, Y. Yamada, S. Kanayama, N. Furukawa, T. Noguchi, S. Haruta, S. Yoshida, M. Sakata, T. Sado and H. Oi: The role of iron in the pathogenesis of endometriosis. Gynecol Endocrinol 25, 39-52 (2009)
136. N. Yamauchi, T. Harada, F. Taniguchi, S. Yoshida, T. Iwabe and N. Terakawa: Tumor necrosis factor-α induced the release of interleukin-6 from endometriotic stromal cells by the nuclear factor-kappa B and mitogen-activated protein kinase pathways. Fertil Steril 82, 1023-1028 (2004)
137. E.L. Sheldrick, K. Derecka, E. Marshall, E.C. Chin, L. Hodges, D.C. Wathes, D.R. Abayasekara and A.P. Flint: Peroxisome-proliferator-activated receptors and the control of levels of prostaglandin-endoperoxide synthase 2 by arachidonic acid in the bovine uterus. Biochem J 406,175- 183 (2007)
138. K. Derecka, E.L. Sheldrick, D.C. Wathes, D.R. Abayasekara and A.P. Flint: A PPAR-independent pathway to PUFA-induced COX-2 expression. Mol Cell Endocrinol 287, 65-71 (2008)
139. W.G. Cao, M. Morin, C. Metz, R. Maheux and A. Akoum: Stimulation of macrophage migration inhibitory factor expression in endometrial stromal cells by interleukin 1, beta involving the nuclear transcription factor NF-kappa B. Biol Reprod 73, 565-570 (2005)
140. V. Veillat, C.H. Lavoie, C.N. Metz, T. Roger, Y. Labelle and A. Akoum: Involvement of nuclear factorkappa B in macrophage migration inhibitory factor gene transcription up-regulation induced by interleukin- 1 beta in ectopic endometrial cells. Fertil Steril 91, 2148-2156 (2009)
141. F. Wieser, J.L. Vigne, I. Ryan, D. Hornung, S. Djlali and R.N. Taylor: Sulindac suppresses nuclear factor-kappa B activation and RANTES gene and protein expression in endometrial stromal cells from women with endometriosis. J Clin Endocrinol Metab 90, 6441-6447 (2005)
142. T. Yagyu, H. Kobayashi, H. Matsuzaki, K. Wakahara, T. Kondo, N. Kurita, H. Sekino, K. Inagaki, M. Suzuki, N. Kanayama and T. Terao: Thalidomide inhibits tumor necrosis factor-alpha-induced interleukin-8 (IL-8) expression in endometriotic stromal cells possibly through suppression of nuclear factor-kappa B activation. J Clin Endocrinol Metab 90, 3017-3021 (2005)
143. S. Horie, T. Harada, M. Mitsunari, F. Taniguchi, T. Iwabe and N. Terakawa: Progesterone and progestational compounds attenuate tumor necrosis factor alpha-induced interleukin-8 production via nuclear factor kappa B inactivation in endometriotic stromal cells. Fertil Steril 83, 1530-1535 (2005)
144. Y. Tagashira, F. Taniguchi, T. Harada, A. Ikeda, A. Watanabe and N. Terakawa: Interleukin-10 attenuates TNF-alpha-induced interleukin-6 production in endometriotic stromal cells. Fertil Steril 91, 2185-2192 (2009)
145. W. Xiu-li, C. Wen-jun, D. Hui-hua, H. Su-ping and F. Shi-long: ERB-041, a selective ER beta agonist, inhibits iNOS production in LPS-activated peritoneal macrophages of endometriosis via suppression of NF-kappa B activation. Mol Immunol 46, 2413-2418 (2009)
146. K. Nasu, M. Nishida, T. Ueda, A. Yuge, N. Takai and H. Narahara: Application of the nuclear factor-kappa B inhibitor BAY 11-7085 for the treatment of endometriosis: an in vitro study. Am J Physiol Endocrinol Metab 293, 16- 23 (2007)
147. M. Güney, S. Nasir, B. Oral, N. Karahan and T. Mungan: Effect of caffeic acid phenethyl ester on the regression of endometrial explants in an experimental rat model. Reprod Sci 14, 270-279 (2007)
148. S. Netsu, R. Konno, K. Odagiri, M. Soma, H. Fujiwara and M. Suzuki: Oral eicosapentaenoic acid supplementation as possible therapy for endometriosis. Fertil Steril 90, 1496-1502 (2008)
149. M.W. Laschke, C. Schwender, C. Scheuer, B. Vollmar and M.D. Menger: Dietary glycine does not affect physiological angiogenesis and reproductive function, but inhibits apoptosis in endometrial and ovarian tissue by down-regulation of nuclear factor-kappa B. Fertil Steril 90, 1460-1469 (2008)
150. A.V. Huber, J.C. Huber, A. Kolbus, M. Imhof, F. Nagele, D. Loizou, U. Kaufmann and C.F. Singer: Systemic HCG treatment in patients with endometriosis: a new perspective for a painful disease. Wien Klin Wochenschr 116, 839-843 (2004)
151. A.V. Huber, L. Saleh, J. Prast, P. Haslinger and M. Knöfler: Human chorionic gonadotrophin attenuates NFkappa B activation and cytokine expression of endometriotic stromal cells. Mol Hum Reprod 13, 595-604 (2007)