Inhibition of macrophage migration inhibitory factor reduces endometriotic implant size in mice with experimentally induced disease

Journal of Endometriosis

Volumn 3, Issue 3, 2011, Pages 135-142

  Nothnick, Warren B ^a,b   Colvin, Arlene ^a   Cheng, Kai Fan ^c   Al Abed, Yousef ^c  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

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

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Endometriosis; ISO 1; Macrophage migration inhibitory factor; Uterus

Indexed keywords

MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; FEMALE; IMPLANT; MACROPHAGE MIGRATION INHIBITION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REPRODUCTION; VASCULARIZATION; WESTERN BLOTTING;

EID: 84255176133     PISSN: 20359969     EISSN: 2036282X     Source Type: Journal    
DOI: 10.5301/JE.2011.8910     Document Type: Article

References (39)

1. Halme J, Hammond MG, Hulka JF. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 1984; 64: 151-4.
2. Liu DTY, Hitchcock A. Endometriosis: Its association with retrograde menstruation, dysmenorrhea, and tubal pathology. Br J Obstet Gynaecol 1986; 93: 859-86.
3. Nothnick WB. Novel targets for the treatment of endometriosis. Expert Opin Ther Targets 2004; 5: 459-71.
4. Sinaii N, Cleary SD, Ballweg ML, Nieman LK, Stratton P. High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum Reprod 2002; 10: 2715-24.
5. Kyama CM, Mihalyi A, Simsa P, et al. Non-steroidal targets in the diagnosis and treatment of endometriosis. Curr Med Chem 2008; 10: 1006-17.
6. Santos LL and Morand EF. Macrophage migration inhibitory factor: a key cytokine in RA, SLE and atherosclerosis. Clin Chim Acta 2009; 399: 1-7.
7. Santos LL, Dacumos A, Yamana J, Sharma L, Morand EF. Reduced arthritis in MIF deficient mice is associated with reduced T cell activation: down-regulation of ERK MAP kinase phosphorylation. Clin Exp Immunol 2008; 152: 372-80.
8. Emonts M, Sweep FC, Grebenchtchikow N, et al. Association between high levels of blood macrophage migration inhibitory factor, inappropriate adrenal response, and early death in patients with severe sepsis. Clin Infect Dis 2007; 44: 1321-8.
9. Chesney J, Metz C, Bacher M, Peng T, Meinhardt A, Bucala R. An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med 1999; 5: 181-91.
10. Yang Y, Degranpré P, Kharfi A, Akoum 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: 4721-7.
11. 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: 883-9.
12. Akoum A, Metz CN, Al-Akoum M, Kats R. 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: 1379-85.
13. Kats R, Collette T, Metz CN, Akoum A. Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis. Fertil Steril 2002; 78: 69-76.
14. Morin M, Bellehumeur C, Therriault MJ, Metz C, Maheux R, Akoum A. Elevated levels of macrophage migration inhibitory factor in the peripheral blood of women with endometriosis. Fertil Steril 2005; 83: 865-72.
15. Akoum A, Kong J, Metz C, Beaumont MC. 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: 989-94.
16. Carli C, Metz CN, Al-Abed Y, Naccache PH, Akoum A. 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 2009; 150: 3128-37.
17. Veillat V, Carli C, Metz CN, Al-Abed Y, Naccache PH, Akoum A. Macrophage migration inhibitory factor elicits an angiogenic phenotype in human ectopic endometrial cells and triggers the production of major angiogenic factors viaCD44, CD74, and MAPK signaling pathways. J Clin Endocrinol Metab 2010; 95: 403-12.
18. Al-Abed Y, Dabideen D, Aljabari B, et al. ISO-1 binding to the tautomerase active site of MIF inhibits its pro-inflammatory activity and increases survival in severe sepsis. J Biol Chem 2005; 280: 36541-4.
19. Dagia NM, Kamath DV, Bhatt P, et al. A fluorinated analog of ISO-1 blocks the recognition and biological function of MIF and is orally efficacious in a murine model of colitis. Eur J Pharmacol 2009; 607: 201-12.
20. Meyer-Siegler KL, Vera PL, Iczkowski KA, et al. Macrophage migration inhibitory factor (MIF) gene polymorphisms are associated with increased prostate cancer incidence. Genes Immun 2007; 8: 646-52.
21. Nowak NM, Fischer OM, Gust TC, Fuhrmann U, Habenicht UF, Schmidt A. Intraperitoneal inflammation decreases endometriosis in a mouse model. Hum Reprod 2008; 23: 2466-74.
22. Nothnick WB. Disruption of the tissue inhibitor of metalloproteinase- 1 gene results in altered reproductive cyclicity and uterine morphology in reproductive-age female mice. Biol Reprod 2000; 63: 905-12.
23. Zhang X, Hoang E, Nothnick WB. Estrogen-induced uterine abnormalities in TIMP-1 deficient mice are associated with elevated plasmin activity and reduced expression of the novel uterine plasmin protease inhibitor serpinb7. Mol Reprod Dev 2009; 76: 160-72.
24. Al-Abed Y, Vanpatten S. MIF as a disease target: ISO-1 as a proof-of-concept therapeutic. Future Med Chem 2011; 3: 45-63.
25. Al-Abed Y, Dabideen D, Aljabari B, et al. ISO-1 binding to the tautomerase active site of MIF inhibits its pro-inflammatory activity and increases survival in severe sepsis. J Biol Chem 2005; 280: 36541-4.
26. Lubetsky, JB, Dios A, Han J, et al. The tautomerase active site of macrophage migration inhibitory factor is a potential target for discovery of novel anti-inflammatory agents. J Biol Chem 2002; 277: 24976-82.
27. Barrier BF. Immunology of endometriosis. Clin Obstet Gynecol 2010; 53: 397-402.
28. Matarese G, De Placido G, Nikas Y, Alviggi C. Pathogenesis of endometriosis: natural immunity dysfunction or autoimmune disease? Trends Mol Med 2003; 9: 223-8.
29. Greven D, Leng L, Bucala R. Autoimmune diseases: MIF as a therapeutic target. Expert Opin Ther Targets 2010; 14: 253-64.
30. Stosic-Grujicic S, Stojanovic I, Nicoletti F. MIF in autoimmunity and novel therapeutic approaches. Autoimmun Rev 2009; 8: 244-9.
31. Mitchell RA, Liao H, Chesney J, et al. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulator y role in the innate immune response. Proc Natl Acad Sci U S A 2002; 99: 345-50.
32. Nishihra J, Ishibashi T, Fukushima T, Sun B, Sato Y, Todo S. Macrophage migration inhibitory factor (MIF): its potential role in tumor growth and tumor-associated angiogenesis. Ann N Y Acad Sci 2003; 995: 171-82.
33. Onodera S, Kaneda K, Mizue Y, Koyama Y, Fujinaga M, Nishihira J. Macrophage migration inhibitory factor up-regulates expression of matrix metalloproteinases in synovial fibroblasts of rheumatoid arthritis. J Biol Chem 2002; 275: 444-50.
34. Saito T, Mizumoto H, Kuroki K, Fujii M, Mori S, Kudo R. Expression of MMP-3 and TIMP-1 in the endometriosis and influence of danazol. Nihon Sanka Fujinka Gakkai Zasshi 1995; 47: 495-6.
35. Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, Mc-Bean J, Osteen KG. Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab 2002; 87: 4782-91.
36. Bruner-Tran KL, Osteen KG, Duleba AJ. Simvastatin protects against the development of endometriosis in a nude mouse model. J Clin Endocrinol Metab 2009; 94: 2489-94.
37. Pelch KE, Schroder AL, Kimball PA, Sharpe-Timms KL, Wade-Davis J, Nagel SC. Aberrant gene expression profile in a mouse model of endometriosis mirrors that observed in women. Fertil Steril 2010; 93: 1615-27.
38. Mönckedieck V, Sannecke C, Husen B, et al. Progestins inhibit expression of MMPs and angiogenic factors in human ectopic endometrial lesions in a mouse model. Mol Hum Reprod 2009; 15: 633-43.
39. Paul S, Bhattacharya P, Das Mahapatra P, Swarnakar S. Melatonin protects against endometriosis via regulation of matrix metalloproteinase-3 and an apoptotic pathway. J Pineal Res 2010; 49: 156-68.