Selective inhibition of prostaglandin E2 receptors EP2 and EP4 inhibits invasion of human immortalized endometriotic epithelial and stromal cells through suppression of metalloproteinases

Molecular and Cellular Endocrinology

Volumn 332, Issue 1-2, 2011, Pages 306-313

  Lee, JeHoon ^a   Banu, Sakhila K ^a   Subbarao, Thenmozhi ^a   Starzinski Powitz, Anna ^b   Arosh, Joe A ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Endometriosis; EP2 and EP4; Human; Invasion; MMPs; PGE2

Indexed keywords

BETA ARRESTIN 1; CD147 ANTIGEN; G PROTEIN COUPLED RECEPTOR; GELATINASE A; INTERSTITIAL COLLAGENASE; MATRILYSIN; PROSTAGLANDIN E RECEPTOR; PROTEIN EP4; STEROID RECEPTOR COACTIVATOR 1; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TISSUE INHIBITOR OF METALLOPROTEINASE 4; UNCLASSIFIED DRUG;

ARTICLE; CELL IMMORTALIZATION; CELL INVASION; CELL MIGRATION; CELL SPECIFICITY; CONTROLLED STUDY; ENDOMETRIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; FEMALE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STROMA CELL;

CELL MOVEMENT; CELLS, CULTURED; DINOPROSTONE; ENDOMETRIOSIS; ENDOMETRIUM; EPITHELIAL CELLS; FEMALE; HUMANS; MATRIX METALLOPROTEINASES; RECEPTORS, PROSTAGLANDIN E, EP2 SUBTYPE; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; RNA, SMALL INTERFERING; STROMAL CELLS; TISSUE INHIBITOR OF METALLOPROTEINASES;

EID: 78650520313     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.11.022     Document Type: Article

References (77)

1. Alfranca A., et al. PGE2 induces angiogenesis via MT1-MMP-mediated activation of the TGFbeta/Alk5 signaling pathway. Blood 2008, 112:1120-1128.
2. American Society for Reproductive Medicine Revised American Society for Reproductive Medicine Classification of Endometriosis: 1996. Fertil. Steril. 1997, 67:817-821.
3. Attar E., et al. Prostaglandin E2 via steroidogenic factor-1 coordinately regulates transcription of steroidogenic genes necessary for estrogen synthesis in endometriosis. J. Clin. Endocrinol. Metab. 2008, 94:623-631.
4. Banu S.K., et al. Selective inhibition of prostaglandin E2 receptors EP2 and EP4 induces apoptosis of human endometriotic cells through suppression of ERK1/2, AKT, NFkB and b-catenin pathways and activation of intrinsic apoptotic mechanisms. Mol. Endocrinol. 2009, 23:1291-1305.
5. Banu S.K., et al. Cyclooxygenase-2 regulates survival, migration and invasion of human endometriotic cells through multiple mechanisms. Endocrinology 2008, 149:1180-1189.
6. Banu S.K., et al. Gene expression profiles and functional characterization of human immortalized endometriotic epithelial and stromal cells. Fertil. Steril. 2008, 90:972-987.
7. Banu S.K., et al. Induction of peritoneal endometriosis in nude mice using human immortalized endometriosis epithelial and stromal cells: a potential experimental tool to study molecular pathogenesis of endometriosis in human. Fertil. Steril. 2009, 91:2199-2209.
8. Bellosta S., et al. Inhibition of MMP-2 activation and release as a novel mechanism for HDL-induced cardioprotection. FEBS Lett. 2006, 580:5974-5978.
9. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
10. Braundmeier A.G., et al. Extracellular matrix metalloproteinase inducer regulates metalloproteinases in human uterine endometrium. J. Clin. Endocrinol. Metab. 2006, 91:2358-2365.
11. Bruner-Tran K.L., et al. Down-regulation of endometrial matrix metalloproteinase-3 and -7 expression in vitro and therapeutic regression of experimental endometriosis in vivo by a novel nonsteroidal progesterone receptor agonist, tanaproget. J. Clin. Endocrinol. Metab. 2006, 91:1554-1560.
12. Bruner K.L., et al. Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice. J. Clin. Invest. 1997, 99:2851-2857.
13. Bulun S.E. Endometriosis. N. Engl. J. Med. 2009, 360:268-279.
14. Chang W., et al. Cordycepin inhibits vascular smooth muscle cell proliferation. Eur. J. Pharmacol. 2008, 597:64-69.
15. Chung H.W., et al. Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium. Fertil. Steril. 2002, 78:787-795.
16. Chung H.W., et al. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-3 mRNA expression in ectopic and eutopic endometrium in women with endometriosis: a rationale for endometriotic invasiveness. Fertil. Steril. 2001, 75:152-159.
17. Cobellis L., et al. The treatment with a COX-2 specific inhibitor is effective in the management of pain related to endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 2004, 116:100-102.
18. Coleman R.A., et al. International Union of Pharmacology classification of prostanoid receptors: properties, distribution, and structure of the receptors and their subtypes. Pharmacol. Rev. 1994, 46:205-229.
19. Collette T., et al. Evidence for an increased release of proteolytic activity by the eutopic endometrial tissue in women with endometriosis and for involvement of matrix metalloproteinase-9. Hum. Reprod. 2004, 19:1257-1264.
20. Collette T., et al. Increased expression of matrix metalloproteinase-9 in the eutopic endometrial tissue of women with endometriosis. Hum. Reprod. 2006, 21:3059-3067.
21. Crider J.Y., et al. Endogenous EP4 prostaglandin receptors coupled positively to adenylyl cyclase in Chinese hamster ovary cells: pharmacological characterization. Prostaglandins Leukot. Essent. Fatty Acids 2000, 62:21-26.
22. Curry T.E., Osteen K.G. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr. Rev. 2003, 24:428-465.
23. De Leon F.D., et al. Peritoneal fluid volume, estrogen, progesterone, prostaglandin, and epidermal growth factor concentrations in patients with and without endometriosis. Obstet. Gynecol. 1986, 68:189-194.
24. Egawa N., et al. Membrane type 1 matrix metalloproteinase (MT1-MMP/MMP-14) cleaves and releases a 22-kDa extracellular matrix metalloproteinase inducer (EMMPRIN) fragment from tumor cells. J. Biol. Chem. 2006, 281:37576-37585.
25. Gilabert-Estelles J., et al. Expression of several components of the plasminogen activator and matrix metalloproteinase systems in endometriosis. Hum. Reprod. 2003, 18:1516-1522.
26. Giudice L.C., Kao L.C. Endometriosis. Lancet 2004, 364:1789-1799.
27. Gomez-Hernandez A., et al. Effect of intensive atorvastatin therapy on prostaglandin E2 levels and metalloproteinase-9 activity in the plasma of patients with non-ST-elevation acute coronary syndrome. Am. J. Cardiol. 2008, 102:12-18.
28. Guo H., et al. EMMPRIN (CD147), an inducer of matrix metalloproteinase synthesis, also binds interstitial collagenase to the tumor cell surface. Cancer Res. 2000, 60:888-891.
29. Han Y.J., et al. Haplotype analysis of the matrix metalloproteinase-9 gene associated with advanced-stage endometriosis. Fertil. Steril. 2009, 91:2324-2330.
30. Hernandez-Barrantes S., et al. Regulation of membrane type-matrix metalloproteinases. Semin. Cancer Biol. 2002, 12:131-138.
31. Huang H.F., et al. Matrix metalloproteinase 2 is associated with changes in steroid hormones in the sera and peritoneal fluid of patients with endometriosis. Fertil. Steril. 2004, 81:1235-1239.
32. Huang Z., et al. EMMPRIN expression in tongue squamous cell carcinoma. J. Oral. Pathol. Med. 2009, 38:518-523.
33. Itatsu K., et al. Cyclooxygenase-2 is involved in the up-regulation of matrix metalloproteinase-9 in cholangiocarcinoma induced by tumor necrosis factor-alpha. Am. J. Pathol. 2009, 174:829-841.
34. Ito H., et al. Prostaglandin E2 enhances pancreatic cancer invasiveness through an Ets-1-dependent induction of matrix metalloproteinase-2. Cancer Res. 2004, 64:7439-7446.
35. Jiang J.L., Tang J. CD147 and its interacting proteins in cellular functions. Sheng Li Xue Bao 2007, 59:517-523.
36. Kim C.H., et al. PGE2 induces the gene expression of bone matrix metalloproteinase-1 in mouse osteoblasts by cAMP-PKA signaling pathway. Int. J. Biochem. Cell Biol. 2005, 37:375-385.
37. Kim Y.A., et al. Gonadotropin-releasing hormone agonist reduces aromatase cytochrome P450 and cyclooxygenase-2 in ovarian endometrioma and eutopic endometrium of patients with endometriosis. Gynecol. Obstet. Invest. 2009, 68:73-81.
38. Kumagai N., et al. Active matrix metalloproteinases in the tear fluid of individuals with vernal keratoconjunctivitis. J. Allergy Clin. Immunol. 2002, 110:489-491.
39. Langlois S., et al. Membrane-type 1 matrix metalloproteinase stimulates cell migration through epidermal growth factor receptor transactivation. Mol. Cancer Res. 2007, 5:569-583.
40. Laschke M.W., et al. Selective cyclo-oxygenase-2 inhibition induces regression of autologous endometrial grafts by down-regulation of vascular endothelial growth factor-mediated angiogenesis and stimulation of caspase-3-dependent apoptosis. Fertil. Steril. 2007, 87:163-171.
41. Laudanski P., et al. Matrix metalloproteinase-13 and membrane type-1 matrix metalloproteinase in peritoneal fluid of women with endometriosis. Gynecol. Endocrinol. 2005, 21:106-110.
42. Lee E.J., et al. Cyclooxygenase-2 promotes cell proliferation, migration and invasion in U2OS human osteosarcoma cells. Exp. Mol. Med. 2007, 39:469-476.
43. Lee J., et al. Selective blockade of prostaglandin E2 receptor EP2 and EP4 signaling inhibits proliferation of human endometriotic epithelial cells and stromal cells through distinct cell cycle arrest. Fertil. Steril. 2010, 15:2498-2506.
44. Lu X.E., et al. Vascular endothelial growth factor and matrix metalloproteinase-2 expedite formation of endometriosis in the early stage ICR mouse model. Fertil. Steril. 2006, 86:1175-1181.
45. Matsuzaki S., et al. Cyclooxygenase-2 selective inhibitor prevents implantation of eutopic endometrium to ectopic sites in rats. Fertil. Steril. 2004, 82:1609-1615.
46. Molloy E.S., et al. Mechanism of basic calcium phosphate crystal-stimulated matrix metalloproteinase-13 expression by osteoarthritic synovial fibroblasts: inhibition by prostaglandin E2. Ann. Rheum. Dis. 2008, 67:1773-1779.
47. Nabeshima K., et al. Emmprin (basigin/CD147): matrix metalloproteinase modulator and multifunctional cell recognition molecule that plays a critical role in cancer progression. Pathol. Int. 2006, 56:359-367.
48. Nabeshima K., et al. Expression of emmprin and matrix metalloproteinases (MMPs) in peripheral nerve sheath tumors: emmprin and membrane-type (MT)1-MMP expressions are associated with malignant potential. Anticancer Res. 2006, 26:1359-1367.
49. Narumiya S., et al. Prostanoid receptors: structures, properties, and functions. Physiol. Rev. 1999, 79:1193-1226.
50. Nisolle M., et al. Morphometric study of the stromal vascularization in peritoneal endometriosis. Fertil. Steril. 1993, 59:681-684.
51. Nisolle M., et al. Immunohistochemical analysis of proliferative activity and steroid receptor expression in peritoneal and ovarian endometriosis. Fertil. Steril. 1997, 68:912-919.
52. Noguchi Y., et al. Identification and characterization of extracellular matrix metalloproteinase inducer in human endometrium during the menstrual cycle in vivo and in vitro. J. Clin. Endocrinol. Metab. 2003, 88:6063-6072.
53. Nyalendo C., et al. Impaired tyrosine phosphorylation of membrane type 1-matrix metalloproteinase reduces tumor cell proliferation in three-dimensional matrices and abrogates tumor growth in mice. Carcinogenesis 2008, 29:1655-1664.
54. Nyalendo C., et al. Src-dependent phosphorylation of membrane type I matrix metalloproteinase on cytoplasmic tyrosine 573: role in endothelial and tumor cell migration. J. Biol. Chem. 2007, 282:15690-15699.
55. Olivares C., et al. Effects of a selective cyclooxygenase-2 inhibitor on endometrial epithelial cells from patients with endometriosis. Hum. Reprod. 2008, 23:2701-2708.
56. Osenkowski P., et al. Processing, shedding, and endocytosis of membrane type 1-matrix metalloproteinase (MT1-MMP). J. Cell. Physiol. 2004, 200:2-10.
57. Osteen K.G., et al. Matrix metalloproteinases and endometriosis. Semin. Reprod. Med. 2003, 21:155-164.
58. Pan H., et al. Increased expression of c-fos protein associated with increased matrix metalloproteinase-9 protein expression in the endometrium of endometriotic patients. Fertil. Steril. 2008, 90:1000-1007.
59. Pavlovic S., et al. Targeting prostaglandin E2 receptors as an alternative strategy to block cyclooxygenase-2-dependent extracellular matrix-induced matrix metalloproteinase-9 expression by macrophages. J. Biol. Chem. 2006, 281:3321-3328.
60. Pitsos M., Kanakas N. The role of matrix metalloproteinases in the pathogenesis of endometriosis. Reprod. Sci. 2009, 16:717-726.
61. Salata I.M., et al. Gelatinase A (MM-2), gelatinase B (MMP-9) and their inhibitors (TIMP 1, TIMP-2) in serum of women with endometriosis: significant correlation between MMP-2, MMP-9 and their inhibitors without difference in levels of matrix metalloproteinases and tissue inhibitors of metalloproteinases in relation to the severity of endometriosis. Gynecol. Endocrinol. 2008, 24:326-330.
62. Shaco-Levy R., et al. Matrix metalloproteinases 2 and 9, E-cadherin, and beta-catenin expression in endometriosis, low-grade endometrial carcinoma and non-neoplastic eutopic endometrium. Eur. J. Obstet. Gynecol. Reprod. Biol. 2008, 139:226-232.
63. Sier C.F., et al. EMMPRIN-induced MMP-2 activation cascade in human cervical squamous cell carcinoma. Int. J. Cancer 2006, 118:2991-2998.
64. Smedts A.M., et al. Expression of an extracellular matrix metalloproteinase inducer (basigin) in the human ovary and ovarian endometriosis. Fertil. Steril. 2006, 86:535-542.
65. Sun J., Hemler M.E. Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metalloproteinase inducer interactions. Cancer Res. 2001, 61:2276-2281.
66. Suzuki S., et al. Direct cell-cell interaction enhances pro-MMP-2 production and activation in co-culture of laryngeal cancer cells and fibroblasts: involvement of EMMPRIN and MT1-MMP. Exp. Cell Res. 2004, 293:259-266.
67. Szamatowicz J., et al. Matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1: a possible role in the pathogenesis of endometriosis. Hum. Reprod. 2002, 17:284-288.
68. Ueda M., et al. Gene expression of adhesion molecules and matrix metalloproteinases in endometriosis. Gynecol. Endocrinol. 2002, 16:391-402.
69. Uzan C., et al. Eutopic endometrium and peritoneal, ovarian and bowel endometriotic tissues express a different profile of matrix metalloproteinases-2, -3 and -11, and of tissue inhibitor metalloproteinases-1 and -2. Virchows Arch. 2004, 445:603-609.
70. Warner T.D., et al. Cyclo-oxygenase-2 inhibitors and cardiovascular events. Lancet 2002, 360:1700-1701.
71. Wolber E.M., et al. Differential induction of matrix metalloproteinase 1 and 2 in ectopic endometrium. Reprod. Biomed. Online 2003, 6:238-243.
72. Woodward D.F., et al. 6-Isopropoxy-9-oxoxanthene-2-carboxylic acid (AH 6809), a human EP2 receptor antagonist. Biochem. Pharmacol. 1995, 50:1731-1733.
73. Wu M.H., et al. Endometriosis: disease pathophysiology and the role of prostaglandins. Expert. Rev. Mol. Med. 2007, 9:1-20.
74. Wu Y., et al. Trichostatin A, a histone deacetylase inhibitor, attenuates invasiveness and reactivates E-cadherin expression in immortalized endometriotic cells. Reprod. Sci. 2007, 14:374-382.
75. Zeitvogel A., et al. Identification of an invasive, N-cadherin-expressing epithelial cell type in endometriosis using a new cell culture model. Am. J. Pathol. 2001, 159:1839-1852.
76. Zhou H.E., Nothnick W.B. The relevancy of the matrix metalloproteinase system to the pathophysiology of endometriosis. Front. Biosci. 2005, 10:569-575.
77. Zhou J., et al. Involvement of CD147 in overexpression of MMP-2 and MMP-9 and enhancement of invasive potential of PMA-differentiated THP-1. BMC Cell Biol. 2005, 6:25.