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

Volumn 150, Issue 7, 2009, Pages 3128-3137

  Carli, Cédric ^a   Metz, Christine N ^b   Al Abed, Yousef ^b   Naccache, Paul H ^a   Akoum, Ali ^a  

^a LAVAL UNIVERSITY   (Canada)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; MACROPHAGE MIGRATION INHIBITION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROSTAGLANDIN E2;

ADULT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOMETRIOSIS; ENDOMETRIUM CELL; ENZYME INDUCTION; ENZYME SYNTHESIS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ADULT; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; CELLS, CULTURED; CYCLOOXYGENASE 2; DINOPROSTONE; ENDOMETRIOSIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MACROPHAGE MIGRATION-INHIBITORY FACTORS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 67649662617     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1088     Document Type: Article

References (72)

1. Giudice LC, Kao LC 2004 Endometriosis. Lancet 364:1789-1799
2. Siristatidis C, Nissotakis C, Chrelias C, Iacovidou H, Salamalekis E 2006 Immunological factors and their role in the genesis and development of endometriosis. J Obstet Gynaecol Res 32:162-170
3. Agic A, Xu H, Finas D, Banz C, Diedrich K, HornungD2006 Is endometriosis associated with systemic subclinical inflammation? Gynecol Obstet Invest 62: 139-147
4. Minici F, Tiberi F, Tropea A, Fiorella M, Orlando M, Gangale MF, Romani F, Catino S, Campo S, Lanzone A, Apa R 2007 Paracrine regulation of endometriotic tissue. Gynecol Endocrinol 23:574-580 (Pubitemid 47613726)
5. Braun DP, Gebel H, Rana N, Dmowski WP 1998 Cytolysis of eutopic and ectopic endometrial cells by peripheral blood monocytes and peritoneal macrophages in women with endometriosis. Fertil Steril 69:1103-1108 (Pubitemid 28274901)
6. Dmowski WP, Gebel H, Braun DP 1998 Decreased apoptosis and sensitivity to macrophage mediated cytolysis of endometrial cells in endometriosis. Hum Reprod Update 4:696-701 (Pubitemid 29041482)
7. Ulukus M, Arici A 2005 Immunology of endometriosis. Minerva Ginecol 57: 237-248 (Pubitemid 41503757)
8. Wang H, Dey SK 2005 Lipid signaling in embryo implantation. Prostaglandins Other Lipid Mediat 77:84-102 (Pubitemid 41133418)
9. Achache H, Revel A 2006 Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update 12:731-746 (Pubitemid 44605511)
10. PoyserNL1995 The control of prostaglandin production by the endometrium in relation to luteolysis and menstruation. Prostaglandins Leukot Essent Fatty Acids 53:147-195
11. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK 1997 Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91:197-208 (Pubitemid 27456387)
12. Sales KJ, Jabbour HN 2003 Cyclooxygenase enzymes and prostaglandins in pathology of the endometrium. Reproduction 126:559-567 (Pubitemid 37540615)
13. Cabral GA 2005 Lipids as bioeffectors in the immune system. Life Sci 77: 1699-1710 (Pubitemid 41073663)
14. Matsuoka T, Narumiya S 2007 Prostaglandin receptor signaling in disease. ScientificWorldJournal 7:1329-1347 (Pubitemid 47435437)
15. Miller SB 2006 Prostaglandins in health and disease: an overview. Semin Arthritis Rheum 36:37-49 (Pubitemid 44128595)
16. Li W, Xu RJ, Zhang HH, Jiang LH 2006 Overexpression of cyclooxygenase-2 correlates with tumor angiogenesis in endometrial carcinoma. Int J Gynecol Cancer 16:1673-1678 (Pubitemid 44060397)
17. Harris HA 2007 Estrogen receptor-β: recent lessons from in vivo studies. Mol Endocrinol 21:1-13
18. Ota H, Igarashi S, Sasaki M, Tanaka T 2001 Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis. Hum Reprod 16:561-566 (Pubitemid 32218810)
19. Chakraborty I, Das SK,WangJ, Dey SK1996 Developmental expression of the cyclo-oxygenase-1 and cyclo-oxygenase-2 genes in the peri-implantation mouse uterus and their differential regulation by the blastocyst and ovarian steroids. J Mol Endocrinol 16:107-122 (Pubitemid 26157010)
20. Frank GR, Brar AK, Cedars MI, Handwerger S 1994 Prostaglandin E2 enhances human endometrial stromal cell differentiation. Endocrinology 134: 258-263 (Pubitemid 2035675)
21. Attar E, Bulun SE 2006 Aromatase and other steroidogenic genes in endometriosis: translational aspects. Hum Reprod Update 12:49-56 (Pubitemid 43013746)
22. Kats R, Collette T, Metz CN, Akoum A 2002 Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis. Fertil Steril 78:69-76 (Pubitemid 34722673)
23. Kats R, Metz CN, Akoum A 2002 Macrophage migration inhibitory factor is markedly expressed in active and early-stage endometriotic lesions. J Clin Endocrinol Metab 87:883-889 (Pubitemid 34158268)
24. Calandra T, Roger T 2003 Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3:791-800 (Pubitemid 37328657)
25. Javeed A, Zhao Y, ZhaoY 2008 Macrophage-migration inhibitory factor: role in inflammatory diseases and graft rejection. Inflamm Res 57:45-50 (Pubitemid 351302062)
26. Ayoub S, Hickey MJ, Morand EF 2008 Mechanisms of disease: macrophage migration inhibitory factor in SLE, RA and atherosclerosis. Nat Clin Pract Rheumatol 4:98-105
27. Ohkawara T, Nishihira J, Takeda H, Asaka M, Sugiyama T 2005 Pathophysiological roles of macrophage migration inhibitory factor in gastrointestinal, hepatic, and pancreatic disorders. J Gastroenterol 40:117-122 (Pubitemid 40425197)
28. Metz CN, Bucala R 1997 Role of macrophage migration inhibitory factor in the regulation of the immune response. Adv Immunol 66:197-223 (Pubitemid 127702123)
29. Akoum A, Lemay A, Brunet C, Hébert J 1995 Cytokine-induced secretion of monocyte chemotactic protein-1 by human endometriotic cells in culture. The Groupe d'Investigation en Gynecologie. Am J Obstet Gynecol 172(2 Pt 1): 594-600
30. Al-Abed Y, Dabideen D, Aljabari B, Valster A, Messmer D, Ochani M, Tanovic M, Ochani K, Bacher M, Nicoletti F, Metz C, Pavlov VA, Miller EJ, Tracey KJ 2005 ISO-1 binding to the tautomerase active site of MIF inhibits its pro-inflammatory activity and increases survival in severe sepsis. J Biol Chem 280:36541-36544 (Pubitemid 41587728)
31. Wu MH, Wang CA, Lin CC, Chen LC, Chang WC, Tsai SJ 2005 Distinct regulation of cyclooxygenase-2 by interleukin-1β in normal and endometriotic stromal cells. J Clin Endocrinol Metab 90:286-295 (Pubitemid 40116670)
32. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R 2003 MIF signal transduction initiated by binding to CD74. J Exp Med 197:1467-1476 (Pubitemid 36686708)
33. Santos LL, Lacey D, Yang Y, LeechM,Morand EF 2004 Activation of synovial cell p38MAPkinase by macrophage migration inhibitory factor. J Rheumatol 31:1038-1043 (Pubitemid 38715876)
34. Wu GS 2007 Role of mitogen-activated protein kinase phosphatases (MKPs) in cancer. Cancer Metastasis Rev 26:579-585 (Pubitemid 350115109)
35. Firestein GS, ManningAM1999 Signal transduction and transcription factors in rheumatic disease. Arthritis Rheum 42:609-621 (Pubitemid 29171980)
36. Murakami M, Kudo I 2006 Prostaglandin E synthase: a novel drug target for inflammation and cancer. Curr Pharm Des 12:943-954
37. Jüngel A, Distler O, Schulze-Horsel U, Huber LC, Ha HR, Simmen B, Kalden JR, Pisetsky DS, Gay S, Distler JH 2007 Microparticles stimulate the synthesis of prostaglandin E(2) via induction of cyclooxygenase 2 and microsomal prostaglandin E synthase 1. Arthritis Rheum 56:3564-3574 (Pubitemid 350100689)
38. Han R, Tsui S, Smith TJ 2002 Up-regulation of prostaglandin E2 synthesis by interleukin-1β in human orbital fibroblasts involves coordinate induction of prostaglandin-endoperoxide H synthase-2 and glutathione-dependent prostaglandin E2 synthase expression. J Biol Chem 277:16355-16364 (Pubitemid 34967644)
39. Degousee N, Angoulvant D, Fazel S, Stefanski E, Saha S, Iliescu K, Lindsay TF, Fish JE, Marsden PA, Li RK, Audoly LP, Jakobsson PJ, Rubin BB 2006 c-Jun N-terminal kinase-mediated stabilization of microsomal prostaglandin E2 synthase-1mRNAregulates delayed microsomal prostaglandin E2 synthase-1 expression and prostaglandin E2 biosynthesis by cardiomyocytes. J Biol Chem 281:16443-16452 (Pubitemid 43909595)
40. Kojima F, Naraba H, Miyamoto S, Beppu M, Aoki H, Kawai S 2004 Membrane- associated prostaglandin E synthase-1 is upregulated by proinflammatory cytokines in chondrocytes from patients with osteoarthritis. Arthritis Res Ther 6:R355-R365
41. Stichtenoth DO, Thorén S, Bian H, Peters-Golden M, Jakobsson PJ, Crofford LJ 2001 Microsomal prostaglandin E synthase is regulated by proinflammatory cytokines and glucocorticoids in primary rheumatoid synovial cells. J Immunol 167:469-474 (Pubitemid 32567813)
42. Pascual RM, Carr EM, Seeds MC, Guo M, Panettieri Jr RA, Peters SP, Penn RB 2006 Regulatory features of interleukin-1β-mediated prostaglandin E2 synthesis in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 290: L501-L508 (Pubitemid 43725095)
43. Bradbury DA, Corbett L, Knox AJ 2004 PI 3-kinase and MAP kinase regulate bradykinin induced prostaglandin E(2) release in human pulmonary artery by modulating COX-2 activity. FEBS Lett 560:30-34 (Pubitemid 38264288)
44. Sampey AV, Hall PH, Mitchell RA, Metz CN, Morand EF 2001 Regulation of synoviocyte phospholipase A2 and cyclooxygenase 2 by macrophage migration inhibitory factor. Arthritis Rheum 44:1273-1280 (Pubitemid 32537525)
45. Pakozdi A, Amin MA, Haas CS, Martinez RJ, Haines 3rd GK, Santos LL, Morand EF, David JR, Koch AE 2006 Macrophage migration inhibitory factor: a mediator of matrix metalloproteinase-2 production in rheumatoid arthritis. Arthritis Res Ther 8:R132
46. Amin MA, Haas CS, Zhu K, Mansfield PJ, Kim MJ, Lackowski NP, Koch AE 2006 Migration inhibitory factor up-regulates vascular cell adhesion molecule- 1 and intercellular adhesion molecule-1 via Src, PI3 kinase, and NFκB. Blood 107:2252-2261 (Pubitemid 43345542)
47. Toh ML, Aeberli D, Lacey D, Yang Y, Santos LL, Clarkson M, Sharma L, Clyne C, Morand EF 2006 Regulation of IL-1 and TNF receptor expression and function by endogenous macrophage migration inhibitory factor. J Immunol 177:4818-4825 (Pubitemid 44469817)
48. Murk W, Atabekoglu CS, Cakmak H, Heper A, Ensari A, Kayisli UA, Arici A 2008 Extracellularly signal-regulated kinase activity in the human endometrium: possible roles in the pathogenesis of endometriosis. J Clin Endocrinol Metab 93:3532-3540
49. Yoshino O, Osuga Y, Hirota Y, Koga K, Hirata T, Harada M, Morimoto C, Yano T, Nishii O, Tsutsumi O, Taketani Y 2004 Possible pathophysiological roles of mitogen-activated protein kinases (MAPKs) in endometriosis. Am J Reprod Immunol 52:306-311 (Pubitemid 39585717)
50. Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, Bucala R 2002 Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci USA 99:345-350 (Pubitemid 34060365)
51. Nishihira J, Ishibashi T, Fukushima T, Sun B, Sato Y, Todo S 2003 Macrophage migration inhibitory factor (MIF): its potential role in tumor growth and tumor-associated angiogenesis. Ann NY Acad Sci 995:171-182 (Pubitemid 36706624)
52. Arcuri F, Cintorino M, Vatti R, Carducci A, Liberatori S, Paulesu L 1999 Expression of macrophage migration inhibitory factor transcript and protein by first-trimester human trophoblasts. Biol Reprod 60:1299-1303 (Pubitemid 29240911)
53. Bondza PK, Metz CN, Akoum A 2008 Postgestational effects of macrophage migration inhibitory factor on embryonic implantation in mice. Fertil Steril 90(Suppl):1433-1443
54. Yang Y, Degranpré P, Kharfi A, Akoum A 2000 Identification of macrophage migration inhibitory factor as a potent endothelial cell growth-promoting agent released by ectopic human endometrial cells. J Clin Endocrinol Metab 85:4721-4727 (Pubitemid 32157658)
55. May K, Becker CM 2008 Endometriosis and angiogenesis. Minerva Ginecol 60:245-254
56. Van Langendonckt A, Donnez J, Defrére S, Dunselman GA, Groothuis PG 2008 Antiangiogenic and vascular-disrupting agents in endometriosis: pitfalls and promises. Mol Hum Reprod 14:259-268 (Pubitemid 351804027)
57. Wiegerinck MA, Van Dop PA, Brosens IA 1993 The staging of peritoneal endometriosis by the type of active lesion in addition to the revised American Fertility Society classification. Fertil Steril 60:461-464 (Pubitemid 23278802)
58. Eisinger AL, Prescott SM, Jones DA, Stafforini DM 2007 The role of cyclooxygenase- 2 and prostaglandins in colon cancer. Prostaglandins Other Lipid Mediat 82:147-154 (Pubitemid 44880176)
59. Wang MT, Honn KV, Nie D 2007 Cyclooxygenases, prostanoids, and tumor progression. Cancer Metastasis Rev 26:525-534 (Pubitemid 350115125)
60. Mehrotra S, Morimiya A, Agarwal B, Konger R, Badve S 2006 Microsomal prostaglandin E2 synthase-1 in breast cancer: a potential target for therapy. J Pathol 208:356-363 (Pubitemid 43210522)
61. Rao R, Redha R, Macias-Perez I, Su Y, Hao C, Zent R, Breyer MD, Pozzi A 2007 Prostaglandin E2-EP4 receptor promotes endothelial cell migration via ERK activation and angiogenesis in vivo. J Biol Chem 282:16959-16968 (Pubitemid 47093223)
62. Namkoong S, Lee SJ, Kim CK, Kim YM, Chung HT, Lee H, Han JA, Ha KS, Kwon YG, Kim YM 2005 Prostaglandin E2 stimulates angiogenesis by activating the nitric oxide/cGMP pathway in human umbilical vein endothelial cells. Exp Mol Med 37:588-600 (Pubitemid 43143521)
63. Jabbour HN, Sales KJ, Smith OP, Battersby S, Boddy SC 2006 Prostaglandin receptors are mediators of vascular function in endometrial pathologies. Mol Cell Endocrinol 252:191-200 (Pubitemid 43914098)
64. Finetti F, Solito R, Morbidelli L, Giachetti A, Ziche M, Donnini S 2008 Prostaglandin E2 regulates angiogenesis via activation of fibroblast growth factor receptor-1. J Biol Chem 283:2139-2146
65. Ogawa H, Nishihira J, Sato Y, Kondo M, Takahashi N, Oshima T, Todo S 2000 An antibody for macrophage migration inhibitory factor suppresses tumour growth and inhibits tumour-associated angiogenesis. Cytokine 12: 309-314 (Pubitemid 30449820)
66. Chesney J, Metz C, Bacher M, Peng T, Meinhardt A, Bucala R 1999 An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med 5:181-191 (Pubitemid 29252666)
67. Vercellini P, Frontino G, De Giorgi O, Pietropaolo G, Pasin R, Crosignani PG 2003 Endometriosis: preoperative and postoperative medical treatment. Obstet Gynecol Clin North Am 30:163-180 (Pubitemid 36356719)
68. Noble LS, Takayama K, Zeitoun KM, Putman JM, Johns DA, Hinshelwood MM, Agarwal VR, Zhao Y, Carr BR, Bulun SE 1997 Prostaglandin E2 stimulates aromatase expression in endometriosis-derived stromal cells. J Clin Endocrinol Metab 82:600-606 (Pubitemid 27068636)
69. Pierro E, Minici F, Alesiani O, Monica LD, Anna MM, Muncuso S, Lanzone A 2003 In vitro regulation of β1 and β3 integrin subunits in endometrial epithelial cells from normal endometrium. Am J Reprod Immunol 49:373-376
70. Wu MH, Sun HS, Lin CC, Hsiao KY, Chuang PC, Pan HA, Tsai SJ 2002 Distinct mechanisms regulate cyclooxygenase-1 and -2 in peritoneal macrophages of women with and without endometriosis. MolHumReprod 8:1103-1110 (Pubitemid 36032848)
71. Oral E, Olive DL, Arici A 1996 The peritoneal environment in endometriosis. Hum Reprod Update 2:385-398 (Pubitemid 27087175)
72. Carli C, Leclerc P, Metz CN, Akoum A 2007 Direct effect of macrophage migration inhibitory factor on sperm function: possible involvement in endometriosis- associated infertility. Fertil Steril 88:1240-1247 (Pubitemid 47520616)