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

Journal of Clinical Endocrinology and Metabolism

Volumn 95, Issue 12, 2010, Pages

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

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD74 ANTIGEN; HERMES ANTIGEN; INTERLEUKIN 8; MACROPHAGE MIGRATION INHIBITION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; VASCULOTROPIN;

ADULT; ANGIOGENESIS; ARTICLE; CLINICAL ARTICLE; DOWN REGULATION; ENDOMETRIOSIS; ENDOMETRIUM BIOPSY; ENDOMETRIUM CELL; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN TISSUE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

EID: 78650046206     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2010-0417     Document Type: Article

References (40)

1. Taylor RN, Yu J, Torres PB, Schickedanz AC, Park JK, Mueller MD, Sidell N 2009 Mechanistic and therapeutic implications of angiogenesis in endometriosis. Reprod Sci 16:140-146
2. Rogers PA, Donoghue JF, Walter LM, Girling JE 2009 Endometrial angiogenesis, vascular maturation, and lymphangiogenesis. Reprod Sci 16:147-151
3. Sluimer JC, Daemen MJ 2009 Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis. J Pathol 218:7-29
4. Nisolle M, Casanas-Roux F, Anaf V, Mine JM, Donnez J 1993 Morphometric study of the stromal vascularization in peritoneal endometriosis. Fertil Steril 59:681-684 (Pubitemid 23086336)
5. Oosterlynck DJ, Meuleman C, Sobis H, Vandeputte M, Koninckx PR 1993 Angiogenic activity of peritoneal fluid from women with endometriosis. Fertil Steril 59:778-782 (Pubitemid 23104178)
6. McLaren J, Prentice A, Charnock-Jones DS, Millican SA, Müller KH, Sharkey AM, Smith SK 1996 Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids. J Clin Invest 98:482-489 (Pubitemid 26255749)
7. Akoum A, Lemay A, McColl S, Turcot-Lemay L, Maheux R 1996 Elevated concentration and biologic activity of monocyte chemotactic protein-1 in the peritoneal fluid of patients with endometriosis. Fertil Steril 66:17-23
8. Akoum A, Lawson C, McColl S, Villeneuve M 2001 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 7:859-866
9. 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
10. 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
11. Ren Y, Chan HM, Li Z, Lin C, Nicholls J, Chen CF, Lee PY, Lui V, Bacher M, Tam PK 2004 Upregulation of macrophage migration inhibitory factor contributes to induced N-Myc expression by the activation of ERK signaling pathway and increased expression of interleukin-8 and VEGF in neuroblastoma. Oncogene 23:4146-4154
12. Calandra T, Roger T 2003 Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3:791-800 (Pubitemid 37328657)
13. Santos LL, Morand EF 2009 Macrophage migration inhibitory factor: a key cytokine in RA, SLE and atherosclerosis. Clin Chim Acta 399:1-7
14. Bach JP, Deuster O, Balzer-Geldsetzer M, Meyer B, Dodel R, Bacher M 2009 The role of macrophage inhibitory factor in tumorigenesis and central nervous system tumors. Cancer 115:2031-2040
15. 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)
16. 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)
17. Akoum A, Metz CN, Al-Akoum M, Kats R 2006 Macrophage migration inhibitory factor expression in the intrauterine endometrium of women with endometriosis varies with disease stage, infertility status, and pelvic pain. Fertil Steril 85:1379-1385
18. 3 integrin and vascular endothelial growth factor expression in endometrial adenocarcinoma cell line Ishikawa. J Reprod Immunol 77:142-151
19. 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 172:594-600
20. Sumathi VP, McCluggage WG 2002 CD10 is useful in demonstrating endometrial stroma at ectopic sites and in confirming a diagnosis of endometriosis. J Clin Pathol 55:391-392
21. 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
22. Carli C, Metz CN, Al-Abed Y, Naccache PH, Akoum A 2009 Upregulation of cyclooxygenase-2 expression and prostaglandin E2 production in human endometriotic cells by macrophage migration inhibitory factor: involvement of novel kinase signaling pathways. Endocrinology 150:3128-3137
23. 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
24. Meyer-Siegler KL, Leifheit EC, Vera PL 2004 Inhibition of macrophage migration inhibitory factor decreases proliferation and cytokine expression in bladder cancer cells. BMC Cancer 4:34
25. Shi X, Leng L, Wang T, Wang W, Du X, Li J, McDonald C, Chen Z, Murphy JW, Lolis E, Noble P, Knudson W, Bucala R 2006 CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 25:595-606
26. Mahutte NG, Matalliotakis IM, Goumenou AG, Koumantakis GE, Vassiliadis S, Arici A 2004 Elevations in peritoneal fluid macrophage migration inhibitory factor are independent of the depth of invasion or stage of endometriosis. Fertil Steril 82:97-101 (Pubitemid 38968784)
27. Munaut C, Boniver J, Foidart JM, Deprez M 2002 Macrophage migration inhibitory factor (MIF) expression in human glioblastomas correlates with vascular endothelial growth factor (VEGF) expression. Neuropathol Appl Neurobiol 28:452-460 (Pubitemid 35425598)
28. Xu X, Wang B, Ye C, Yao C, Lin Y, Huang X, Zhang Y, Wang S 2008 Overexpression of macrophage migration inhibitory factor induces angiogenesis in human breast cancer. Cancer Lett 261:147-157 (Pubitemid 351253721)
29. 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)
30. Folkman J 1995 Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27-31
31. Donnez J, Smoes P, Gillerot S, Casanas-Roux F, Nisolle M 1998 Vascular endothelial growth factor (VEGF) in endometriosis. Hum Reprod 13:1686-1690
32. Ulukus M, Ulukus EC, Tavmergen Goker EN, Tavmergen E, Zheng W, Arici A 2009 Expression of interleukin-8 and monocyte chemotactic protein 1 in women with endometriosis. Fertil Steril 91:687-693
33. Jolicoeur C, Boutouil M, Drouin R, Paradis I, Lemay A, Akoum A 1998 Increased expression of monocyte chemotactic protein-1 in the endometrium of women with endometriosis. Am J Pathol 152:125-133
34. + T cells promotes Akt and ERK activation and costimulates IFN-γ production. J Immunol 184:545-549
35. Tsai CY, Lee TS, Kou YR, Wu YL 2009 Glucosamine inhibits IL-1β-mediated IL-8 production in prostate cancer cells by MAPK attenuation. J Cell Biochem 108:489-498
36. Hashimoto K, Ichiyama T, Hasegawa M, Hasegawa S, Matsubara T, Furukawa S 2009 Cysteinyl leukotrienes induce monocyte chemoattractant protein-1 in human monocyte/macrophages via mitogen- activated protein kinase and nuclear factor-κB pathways. Int Arch Allergy Immunol 149:275-282
37. 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
38. Grund EM, Kagan D, Tran CA, Zeitvogel A, Starzinski-Powitz A, Nataraja S, Palmer SS 2008 Tumor necrosis factor-α regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor κB in human endometriotic epithelial cells. Mol Pharmacol 73:1394-1404
39. Hu X, Mendoza FJ, Sun J, Banerji V, Johnston JB, Gibson SB 2008 Lysophosphatidic acid (LPA) induces the expression of VEGF leading to protection against apoptosis in B-cell derived malignancies. Cell Signal 20:1198-1208
40. Liu P, Li H, Cepeda J, Xia Y, Kempf JA, Ye H, Zhang LQ, Ye SQ 2009 Regulation of inflammatory cytokine expression in pulmonary epithelial cells by pre-B-cell colony-enhancing factor via a nonenzymatic and AP-1-dependent mechanism. J Biol Chem 284:27344-27351