MicroRNA miR-145 inhibits proliferation, invasiveness, and stem cell phenotype of an in vitro endometriosis model by targeting multiple cytoskeletal elements and pluripotency factors

Fertility and Sterility

Volumn 99, Issue 5, 2013, Pages

  Adammek, Marlene ^a,b   Greve, Burkhard ^a   Kässens, Nadja ^a   Schneider, Cornelia ^a   Brüggemann, Kathrin ^a   Schüring, Andreas N ^a   Starzinski Powitz, Anna ^c   Kiesel, Ludwig ^a   Götte, Martin ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b SAXION UNIVERSITY OF APPLIED SCIENCES   (Netherlands)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Endometriosis; microRNA; MSI2; SOX2; stem cells

Indexed keywords

CYTOSKELETON PROTEIN; JUNCTIONAL ADHESION MOLECULE A; KRUPPEL LIKE FACTOR 4; MATRIGEL; MICRORNA 145; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2; TRANSGELIN;

ARTICLE; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOMETRIOSIS; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; STROMA CELL;

EID: 84875697812     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2012.11.055     Document Type: Article

References (43)

1. J.A. Sampson Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation Am J Pathol 3 1927 93 110
2. E.M.C. Ohlsson Teague, C.G. Print, and M.L. Hull The role of microRNAs in endometriosis and associated reproductive conditions Human Reprod Update 16 2010 142 165
3. T. Strowitzki, A. Germeyer, R. Popovici, and M. von Wolff The human endometrium as a fertility-determining factor Hum Reprod Update 12 2006 617 630
4. B.A. Lessey Assessment of endometrial receptivity Fertil Steril 96 2011 522 529
5. M. Götte, M. Wolf, A. Staebler, O. Buchweitz, R. Kelsch, and A.N. Schüring Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma J Pathol 215 2008 317 329
6. M. Götte, M. Wolf, A. Staebler, O. Buchweitz, L. Kiesel, and A.N. Schüring Aberrant expression of the pluripotency marker SOX-2 in endometriosis Fertil Steril 95 2011 338 341
7. I. Cervelló, A. Mas, C. Gil-Sanchis, L. Peris, A. Faus, and P.T. Saunders Reconstruction of endometrium from human endometrial side population cell lines PLoS One 6 2011 e21221
8. A.N. Schüring, N. Schulte, R. Kelsch, A. Röpke, L. Kiesel, and M. Götte Characterization of endometrial mesenchymal stem-like cells obtained by endometrial biopsy during routine diagnostics Fertil Steril 95 2011 423 426
9. O. Muneyyirci-Delale, N. Osei-Tutu, R.O. Parris, A. Chandrareddy, M. Dalloul, and P. Stratton Serum F11R/JAM-a levels in women with symptomatic endometriosis Fertil Steril 90 Suppl 2008 S145 S146
10. O. Muneyyirci-Delale, X.C. Jiang, M. Dalloul, Y.F. Fan, C. Charles, and V. Nacharaju F11R/JAM and SM levels in women with endometriosis on treatment with Lupron-Depot vs. norethindrone acetate Reprod Sci 17 3 Suppl 2010 94A
11. G. Dos Santos Hidalgo, J. Meola, E. Rosa, J.C. Silva, C.C. Paro de Paz, and R.A. Ferriani TAGLN expression is deregulated in endometriosis and may be involved in cell invasion, migration, and differentiation Fertil Steril 96 2011 700 703
12. J. Gilabert-Estellés, A. Estellés, J. Gilabert, R. Castelló, F. España, and C. Falcó Expression of several components of the plasminogen activator and matrix metalloproteinase systems in endometriosis Hum Reprod 18 2003 1516 1522
13. L.A. Ramón, J. Gilabert-Estellés, R. Cosín, J. Gilabert, F. España, and R. Castelló Plasminogen activator inhibitor-1 (PAI-1) 4G/5G polymorphism and endometriosis. Influence of PAI-1 polymorphism on PAI-1 antigen and mRNA expression Thromb Res 122 2008 854 860
14. S. Mechsner, A. Kaiser, A. Kopf, C. Gericke, A. Ebert, and J. Bartley A pilot study to evaluate the clinical relevance of endometriosis-associated nerve fibers in peritoneal endometriotic lesions Fertil Steril 92 2009 1856 1861
15. E.M.C. Ohlsson Teague, K.H. Van der Hoek, M.B. Van der Hoek, N. Perry, P. Wagaarachchi, and S.A. Robertson MicroRNA-regulated pathways associated with endometriosis Mol Endocrinol 23 2009 265 275
16. Q. Pan, X. Luo, T. Toloubeydokhti, and N. Chegini The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression Mol Hum Reprod 13 2007 797 806
17. N. Filigheddu, I. Gregnanin, P.E. Porporato, D. Surico, B. Perego, and L. Galli Differential expression of microRNAs between eutopic and ectopic endometrium in ovarian endometriosis J Biomed Biotechnol 2010 2010 369549
18. A. Revel, H. Achache, J. Stevens, Y. Smith, and R. Reich MicroRNAs are associated with human embryo implantation defects Hum Reprod 26 2011 2830 2840
19. C. Neubauer, L. Kiesel, and M. Götte MicroRNAs and the pathogenesis of endometriosis J Endometriosis 4 2012 1 16
20. M. Götte, C. Mohr, C.Y. Koo, C. Stock, A.K. Vaske, and M. Viola miR-145-dependent targeting of junctional adhesion molecule A and modulation of fascin expression are associated with reduced breast cancer cell motility and invasiveness Oncogene 29 2010 6569 6580
21. N. Xu, T. Papagiannakopoulos, G. Pan, J.A. Thomson, and K.S. Kosik MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells Cell 137 2009 647 658
22. A. Zeitvogel, R. Baumann, and A. Starzinski-Powitz Identification of an invasive, N-cadherin-expressing epithelial cell type in endometriosis using a new cell culture model Am J Pathol 159 2001 1839 1852
23. A. Agic, U. von Wussow, A. Starzinski-Powitz, K. Diedrich, P. Altevogt, and D. Hornung Inhibition of cell proliferation, adhesion, and invasion with an anti-L1-cell adhesion molecule monoclonal antibody in an in vitro endometriosis model Fertil Steril 94 2010 1102 1104
24. American Society for Reproductive Medicine Revised American Society for Reproductive Medicine classification of endometriosis: 1996 Fertil Steril 67 1997 817 821
25. M. Götte, B. Greve, R. Kelsch, H. Müller-Uthoff, K. Weiss, and B. Kharabi Masouleh The adult stem cell marker musashi-1 modulates endometrial carcinoma cell cycle progression and apoptosis via notch-1 and p21(WAF1/CIP1) Int J Cancer 129 2011 2042 2049
26. D. Betel, M. Wilson, A. Gabow, D.S. Marks, and C. Sander The microRNA.org resource: targets and expression Nucleic Acids Res 36 2008 D149 D153
27. B. Greve, R. Kelsch, K. Spaniol, H.T. Eich, and M. Götte Flow cytometry in cancer stem cell analysis and separation Cytometry A 81 2012 284 293
28. M. Megraw, P. Sethupathy, B. Corda, and A.G. Hatzigeorgiou miRGen: a database for the study of animal microRNA genomic organization and function Nucleic Acids Res 35 Database Issue 2007 D149 D155
29. M. Sachdeva, S. Zhu, F. Wu, H. Wu, V. Wali, and S. Kumar p53 represses c-Myc through induction of the tumor suppressor miR-145 Proc Natl Acad Sci U S A 106 2009 3207 3212
30. M.G. Kharas, C.J. Lengner, F. Al-Shahrour, L. Bullinger, B. Ball, and S. Zaidi Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia Nat Med 16 2010 903 908
31. W.M. Schopperle, and W.C. DeWolf The TRA-1-60 and TRA-1-81 human pluripotent stem cell markers are expressed on podocalyxin in embryonal carcinoma Stem Cells 25 2007 723 730
32. S.K. Banu, J. Lee, A. Starzinski-Powitz, and J.A. Arosh Gene expression profiles and functional characterization of human immortalized endometriotic epithelial and stromal cells Fertil Steril 90 2008 972 987
33. J. Lee, S.K. Banu, R. Rodriguez, A. Starzinski-Powitz, and J.A. Arosh Selective blockade of prostaglandin E2 receptors EP2 and EP4 signaling inhibits proliferation of human endometriotic epithelial cells and stromal cells through distinct cell cycle arrest Fertil Steril 93 2010 2498 2506
34. S.J. Kim, J.S. Oh, J.Y. Shin, K.D. Lee, K.W. Sung, and S.J. Nam Development of microRNA-145 for therapeutic application in breast cancer J Control Release 155 2011 427 434
35. A.F. Ibrahim, U. Weirauch, M. Thomas, A. Grünweller, R.K. Hartmann, and A. Aigner MicroRNA replacement therapy for miR-145 and miR-33a is efficacious in a model of colon carcinoma Cancer Res 71 2011 5214 5224
36. A. Collison, J. Mattes, M. Plank, and P.S. Foster Inhibition of house dust mite-induced allergic airways disease by antagonism of microRNA-145 is comparable to glucocorticoid treatment J Allergy Clin Immunol 128 2011 160 167
37. P. Nava, C.T. Capaldo, S. Koch, K. Kolegraff, C.R. Rankin, and A.E. Farkas JAM-A regulates epithelial proliferation through Akt/β-catenin signalling EMBO Rep 12 2011 314 320
38. M. Fuse, N. Nohata, S. Kojima, S. Sakamoto, T. Chiyomaru, and K. Kawakami Restoration of miR-145 expression suppresses cell proliferation, migration and invasion in prostate cancer by targeting FSCN1 Int J Oncol 38 2011 1093 1101
39. S. Stolzenburg, M.G. Rots, A.S. Beltran, A.G. Rivenbark, X. Yuan, and H. Qian Targeted silencing of the oncogenic transcription factor SOX2 in breast cancer Nucleic Acids Res 40 2012 6725 6740
40. S. Kabukcuoglu, U. Oner, S.S. Ozalp, E. Dundar, O.T. Yalcin, and E. Colak Prognostic significance of fascin expression in endometrioid carcinoma Eur J Gynaecol Oncol 27 2006 481 486
41. M.A. Bortolini, O. Shynlova, H.P. Drutz, R.A. Castro, M.J. Girão, and S. Lye Expression of genes encoding smooth muscle contractile proteins in vaginal tissue of women with and without pelvic organ prolapse Neurourol Urodyn 31 2012 109 114
42. C.E. Gargett, K.E. Schwab, R.M. Zillwood, H.P. Nguyen, and D. Wu Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium Biol Reprod 80 2009 1136 1145
43. Y. Wu, S. Liu, H. Xin, J. Jiang, E. Younglai, and S. Sun Up-regulation of microRNA-145 promotes differentiation by repressing OCT4 in human endometrial adenocarcinoma cells Cancer 117 2011 3989 3998