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

Volumn 9, Issue 10, 2014, Pages

  Rakhila, Halima ^a   Girard, Karine ^b   Leboeuf, Mathieu ^b   Lemyre, Madeleine ^b   Akoum, Ali ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; CD51 ANTIGEN; CYCLOOXYGENASE 2; MACROPHAGE MIGRATION INHIBITION FACTOR; ISOMERASE; MIF PROTEIN, MOUSE; PRIMER DNA;

ALPHAV INTEGRIN GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B CELL LYMPHOMA; BETA3 INTEGRIN GENE; CONTROLLED STUDY; COX2 GENE; DOWN REGULATION; ECTOPIC ENDOMETRIAL TISSUE GROWTH; ENDOMETRIOSIS; FEMALE; GENE; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MIF GENE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PROTO ONCOGENE; SURVIVAL RATE; TISSUE GROWTH; TISSUE INTERACTION; VEGF GENE; WEIGHT GAIN; WEIGHT REDUCTION; ANALYSIS OF VARIANCE; ANIMAL; ENDOMETRIUM; FLUORESCENCE MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PERITONEUM; REAL TIME POLYMERASE CHAIN REACTION;

ANALYSIS OF VARIANCE; ANIMALS; DNA PRIMERS; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HISTOLOGICAL TECHNIQUES; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; PERITONEUM; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84908132101     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110434     Document Type: Article

References (67)

1. Sampson J (1927) Peritoneal endometriosis due to menstrual dissemination of endometrial tisue into the peritoneal cavity. Am J Obstet Gynecol 14: 422-469.
2. Berbic M, Fraser IS (2013) Immunology of normal and abnormal menstruation. Womens Health (Lond Engl) 9: 387-395.
3. Khoufache K, Michaud N, Harir N, Kibangou Bondza P, Akoum A (2012) Anomalies in the inflammatory response in endometriosis and possible consequences: a review. Minerva Endocrinol 37: 75-92.
4. Veillat V, Sengers V, Metz CN, Roger T, Leboeuf M, et al. (2012) Macrophage migration inhibitory factor is involved in a positive feedback loop increasing aromatase expression in endometriosis. Am J Pathol 181: 917-927.
5. Leng L, Bucala R (2006) Insight into the biology of macrophage migration inhibitory factor (MIF) revealed by the cloning of its cell surface receptor. Cell Res 16: 162-168.
6. Bach JP, Rinn B, Meyer B, Dodel R, Bacher M (2008) Role of MIF in inflammation and tumorigenesis. Oncology 75: 127-133.
7. Bozza M, Satoskar AR, Lin G, Lu B, Humbles AA, et al. (1999) Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 189: 341-346.
8. Das R, Koo MS, Kim BH, Jacob ST, Subbian S, et al. (2013) Macrophage migration inhibitory factor (MIF) is a critical mediator of the innate immune response to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 110: E2997-3006.
9. Yang Y, Degranpre 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, et al. (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. Veillat V, Carli C, Metz CN, Al-Abed Y, Naccache PH, et al. (2010) 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 95: E403-412.
12. Asare Y, Schmitt M, Bernhagen J (2013) The vascular biology of macrophage migration inhibitory factor (MIF). Expression and effects in inflammation, atherogenesis and angiogenesis. Thromb Haemost 109: 391-398.
13. Akoum A, Kong J, Metz C, Beaumont MC (2002) 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 77: 989-994.
14. 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.
15. 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.
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.
17. Morin M, Bellehumeur C, Therriault MJ, Metz C, Maheux R, et al. (2005) Elevated levels of macrophage migration inhibitory factor in the peripheral blood of women with endometriosis. Fertil Steril 83: 865-872.
18. Lin W, Chen S, Li M, Wang B, Qu X, et al. Expression of macrophage migration inhibitory factor in human endometriosis: relation to disease stage, menstrual cycle and infertility. J Obstet Gynaecol Res 36: 344-351.
19. Seeber B, Sammel MD, Fan X, Gerton GL, Shaunik A, et al. (2008) Panel of markers can accurately predict endometriosis in a subset of patients. Fertil Steril 89: 1073-1081.
20. Mahutte NG, Matalliotakis IM, Goumenou AG, Koumantakis GE, Vassiliadis S, et al. (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.
21. Carli C, Metz CN, Al-Abed Y, Naccache PH, Akoum A (2009) Up-regulation 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.
22. Bondza PK, Metz CN, Akoum A (2008) Macrophage migration inhibitory factor up-regulates alpha(v)beta(3) integrin and vascular endothelial growth factor expression in endometrial adenocarcinoma cell line Ishikawa. J Reprod Immunol 77: 142-151.
23. Khoufache K, Bazin S, Girard K, Guillemette J, Roy MC, et al. Macrophage migration inhibitory factor antagonist blocks the development of endometriosis in vivo. PLoS One 7: e37264.
24. Kozak CA, Adamson MC, Buckler CE, Segovia L, Paralkar V, et al. (1995) Genomic cloning of mouse MIF (macrophage inhibitory factor) and genetic mapping of the human and mouse expressed gene and nine mouse pseudogenes. Genomics 27: 405-411.
25. Jensen JR, Witz CA, Schenken RS, Tekmal RR (2010) A potential role for colony-stimulating factor 1 in the genesis of the early endometriotic lesion. Fertil Steril 93: 251-256.
26. Khoufache K, Bazin S, Girard K, Guillemette J, Roy MC, et al. (2012) Macrophage migration inhibitory factor antagonist blocks the development of endometriosis in vivo. PLoS One 7: e37264.
27. Bondza PK, Metz CN, Akoum A (2008) Postgestational effects of macrophage migration inhibitory factor on embryonic implantation in mice. Fertil Steril 90: 1433-1443.
28. Al-Abed Y, Dabideen D, Aljabari B, Valster A, Messmer D, et al. (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.
29. Leng L, Chen L, Fan J, Greven D, Arjona A, et al. A small-molecule macrophage migration inhibitory factor antagonist protects against glomerulonephritis in lupus-prone NZB/NZW F1 and MRL/lpr mice. J Immunol 186: 527-538.
30. Heinrichs D, Knauel M, Offermanns C, Berres ML, Nellen A, et al. (2011) Macrophage migration inhibitory factor (MIF) exerts antifibrotic effects in experimental liver fibrosis via CD74. Proc Natl Acad Sci U S A 108: 17444-17449.
31. Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, et al. (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 13: 587-596.
32. Donnez J, Smoes P, Gillerot S, Casanas-Roux F, Nisolle M (1998) Vascular endothelial growth factor (VEGF) in endometriosis. Hum Reprod 13: 1686-1690.
33. Rakhila H, Carli C, Daris M, Lemyre M, Leboeuf M, et al. (2013) Identification of multiple and distinct defects in prostaglandin biosynthetic pathways in eutopic and ectopic endometrium of women with endometriosis. Fertil Steril 100: 1650-1659 e1651-1652.
34. 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.
35. Assoian RK (1997) Anchorage-dependent cell cycle progression. J Cell Biol 136: 1-4.
36. Nishihira J, Ishibashi T, Fukushima T, Sun B, Sato Y, et al. (2003) Macrophage migration inhibitory factor (MIF): Its potential role in tumor growth and tumorassociated angiogenesis. Ann N Y Acad Sci 995: 171-182.
37. Amin MA, Volpert OV, Woods JM, Kumar P, Harlow LA, et al. (2003) Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ Res 93: 321-329.
38. Bondza PK, Metz CN, Akoum A (2007) Postgestational effects of macrophage migration inhibitory factor on embryonic implantation in mice. Fertil Steril.
39. 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.
40. Leech M, Lacey D, Xue JR, Santos L, Hutchinson P, et al. (2003) Regulation of p53 by macrophage migration inhibitory factor in inflammatory arthritis. Arthritis Rheum 48: 1881-1889.
41. Petrenko O, Fingerle-Rowson G, Peng T, Mitchell RA, Metz CN (2003) Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation. J Biol Chem 278: 11078-11085.
42. Meyer-Siegler K (2000) Macrophage migration inhibitory factor increases MMP-2 activity in DU-145 prostate cells. Cytokine 12: 914-921.
43. Onodera S, Nishihira J, Iwabuchi K, Koyama Y, Yoshida K, et al. (2002) Macrophage migration inhibitory factor up-regulates matrix metalloproteinase-9 and -13 in rat osteoblasts. Relevance to intracellular signaling pathways. J Biol Chem 277: 7865-7874.
44. Taylor RN, Mueller MD (2004) Anti-angiogenic treatment of endometriosis: biochemical aspects. Gynecol Obstet Invest 57: 54-56.
45. Bruner-Tran KL, Herington JL, Duleba AJ, Taylor HS, Osteen KG (2013) Medical management of endometriosis: emerging evidence linking inflammation to disease pathophysiology. Minerva Ginecol 65: 199-213.
46. Hermanowski-Vosatka A, Mundt SS, Ayala JM, Goyal S, Hanlon WA, et al. (1999) Enzymatically inactive macrophage migration inhibitory factor inhibits monocyte chemotaxis and random migration. Biochemistry 38: 12841-12849.
47. Fingerle-Rowson G, Petrenko O, Metz CN, Forsthuber TG, Mitchell R, et al. (2003) The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting. Proc Natl Acad Sci U S A 100: 9354-9359.
48. Bevilacqua E, Paulesu L, Ferro EA, Ietta F, Faria MR, et al. (2014) Review: Putative roles for the macrophage migratory inhibitory factor at the maternal fetal interface. Placenta 35S: S51-S56.
49. Wu MH, Shoji Y, Chuang PC, Tsai SJ (2007) Endometriosis: disease pathophysiology and the role of prostaglandins. Expert Rev Mol Med 9: 1-20.
50. Banu SK, Lee J, Speights VO Jr, Starzinski-Powitz A, Arosh JA (2008) Cyclooxygenase-2 regulates survival, migration, and invasion of human endometriotic cells through multiple mechanisms. Endocrinology 149: 1180-1189.
51. Lee J, Banu SK, Subbarao T, Starzinski-Powitz A, Arosh JA (2011) 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 332: 306-313.
52. 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.
53. Sacco K, Portelli M, Pollacco J, Schembri-Wismayer P, Calleja-Agius J (2012) The role of prostaglandin E(2) in endometriosis. Gynecological endocrinology : the official journal of the International Society of Gynecological Endocrinology 28: 134-138.
54. Harada T, Taniguchi F, Izawa M, Ohama Y, Takenaka Y, et al. (2007) Apoptosis and endometriosis. Front Biosci 12: 3140-3151.
55. Abdalla-Ribeiro HS, Galvao MA, Aoki T, Aldrighi JM, Ribeiro PA (2013) Antiapoptotic activity in deep pelvic endometriosis. Histol Histopathol.
56. Reis FM, Petraglia F, Taylor RN (2013) Endometriosis: hormone regulation and clinical consequences of chemotaxis and apoptosis. Hum Reprod Update 19: 406-418.
57. Desgrosellier JS, Cheresh DA (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 10: 9-22.
58. Hii LL, Rogers PA (1998) Endometrial vascular and glandular expression of integrin alpha(v)beta3 in women with and without endometriosis. Hum Reprod 13: 1030-1035.
59. Brooks PC, Clark RA, Cheresh DA (1994) Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264: 569-571.
60. Adachi M, Nasu K, Tsuno A, Yuge A, Kawano Y, et al. (2011) Attachment to extracellular matrices is enhanced in human endometriotic stromal cells: a possible mechanism underlying the pathogenesis of endometriosis. Eur J Obstet Gynecol Reprod Biol 155: 85-88.
61. Kyama CM, Overbergh L, Mihalyi A, Meuleman C, Mwenda JM, et al. (2008) Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis. Fertil Steril 89: 301-310.
62. Young VJ, Brown JK, Saunders PT, Horne AW (2013) The role of the peritoneum in the pathogenesis of endometriosis. Hum Reprod Update 19: 558-569.
63. Kyama CM, Mihalyi A, Simsa P, Falconer H, Fulop V, et al. (2009) Role of cytokines in the endometrial-peritoneal cross-talk and development of endometriosis. Front Biosci (Elite Ed) 1: 444-454.
64. Van Calsteren K, Devlieger R, De Catte L, D'Hooghe T, Chai DC, et al. (2009) Feasibility of ultrasound-guided percutaneous samplings in the pregnant baboon: a model for studies on transplacental transport. Reprod Sci 16: 280-285.
65. Lucidi RS, Witz CA, Chrisco M, Binkley PA, Shain SA, et al. (2005) A novel in vitro model of the early endometriotic lesion demonstrates that attachment of endometrial cells to mesothelial cells is dependent on the source of endometrial cells. Fertil Steril 84: 16-21.
66. Groothuis PG, Koks CA, de Goeij AF, Dunselman GA, Arends JW, et al. (1999) Adhesion of human endometrial fragments to peritoneum in vitro. Fertil Steril 71: 1119-1124.
67. Chen PF, Luo YL, Wang W, Wang JX, Lai WY, et al. (2010) ISO-1, a macrophage migration inhibitory factor antagonist, inhibits airway remodeling in a murine model of chronic asthma. Molecular medicine 16: 400-408.