Regulation of miR-200 family microRNAs and ZEB transcription factors in ovarian cancer: Evidence supporting a mesothelial-to-epithelial transition

Gynecologic Oncology

Volumn 116, Issue 1, 2010, Pages 117-125

  Bendoraite, Ausra ^a   Knouf, Emily C ^a   Garg, Kavita S ^a   Parkin, Rachael K ^a   Kroh, Evan M ^a   O'Briant, Kathy C ^a   Ventura, Aviva P ^a   Godwin, Andrew K ^b   Karlan, Beth Y ^c   Drescher, Charles W ^a   Urban, Nicole ^a   Knudsen, Beatrice S ^a   Tewari, Muneesh ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Feedback loop; Mesothelial; MicroRNA; miR 200; Ovarian cancer; ZEB2

Indexed keywords

MICRORNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; UNCLASSIFIED DRUG;

ARTICLE; EPITHELIUM; MESOTHELIUM; OVARY CANCER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNTRANSLATED REGION;

CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICRORNAS; OVARIAN NEOPLASMS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

EID: 70749105757     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2009.08.009     Document Type: Article

References (47)

1. Filipowicz W., Bhattacharyya S.N., and Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev., Genet. 9 2 (2008 Feb) 102-114
2. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 2 (2004 Jan 23) 281-297
3. Harfe B.D. MicroRNAs in vertebrate development. Curr. Opin. Genet. Dev. 15 4 (2005 Aug) 410-415
4. Esquela-Kerscher A., and Slack F.J. Oncomirs-microRNAs with a role in cancer. Nat. Rev. Cancer 6 4 (2006 Apr) 259-269
5. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev., Cancer 2 6 (2002 Jun) 442-454
6. Bracken C.P., Gregory P.A., Kolesnikoff N., Bert A.G., Wang J., Shannon M.F., et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 68 19 (2008 Oct 1) 7846-7854
7. Burk U., Schubert J., Wellner U., Schmalhofer O., Vincan E., Spaderna S., et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9 6 (2008 Jun) 582-589
8. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10 5 (2008 May) 593-601
9. Hurteau G.J., Carlson J.A., Spivack S.D., and Brock G.J. Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res. 67 17 (2007 Sep 1) 7972-7976
10. Korpal M., Lee E.S., Hu G., and Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283 22 (2008 May 30) 14910-14914
11. Park S.M., Gaur A.B., Lengyel E., and Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22 7 (2008 Apr 1) 894-907
12. Griffiths-Jones S., Grocock R.J., van Dongen S., Bateman A., and Enright A.J. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34 Database issue (2006 Jan 1) D140-D144
13. Aigner K., Dampier B., Descovich L., Mikula M., Sultan A., Schreiber M., et al. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 26 49 (2007 Oct 25) 6979-6988
14. Christoffersen N.R., Silahtaroglu A., Orom U.A., Kauppinen S., and Lund A.H. miR-200b mediates post-transcriptional repression of ZFHX1B. Rna 13 8 (2007 Aug) 1172-1178
15. Spaderna S., Schmalhofer O., Wahlbuhl M., Dimmler A., Bauer K., Sultan A., et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 68 2 (2008 Jan 15) 537-544
16. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., et al. Cancer statistics, 2008. CA. Cancer J. Clin. 58 2 (2008 Mar-Apr) 71-96
17. Auersperg N., Wong A.S., Choi K.C., Kang S.K., and Leung P.C. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr. Rev. 22 2 (2001 Apr) 255-288
18. Levanon K., Crum C., and Drapkin R. New insights into the pathogenesis of serous ovarian cancer and its clinical impact. J. Clin. Oncol. 26 32 (2008 Nov 10) 5284-5293
19. Nam E.J., Yoon H., Kim S.W., Kim H., Kim Y.T., Kim J.H., et al. MicroRNA expression profiles in serous ovarian carcinoma. Clin. Cancer Res. 14 9 (2008 May 1) 2690-2695
20. Dahiya N., Sherman-Baust C.A., Wang T.L., Davidson B., Shih Ie M., Zhang Y., et al. MicroRNA expression and identification of putative miRNA targets in ovarian cancer. PLoS ONE 3 6 (2008) e2436
21. Iorio M.V., Visone R., Di Leva G., Donati V., Petrocca F., Casalini P., et al. MicroRNA signatures in human ovarian cancer. Cancer Res. 67 18 (2007 Sep 15) 8699-8707
22. Yang H., Kong W., He L., Zhao J.J., O'Donnell J.D., Wang J., et al. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 68 2 (2008 Jan 15) 425-433
23. Zhang L., Volinia S., Bonome T., Calin G.A., Greshock J., Yang N., et al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc. Natl. Acad. Sci. U. S. A. 105 19 (2008 May 13) 7004-7009
24. Riera J.R., Astengo-Osuna C., Longmate J.A., and Battifora H. The immunohistochemical diagnostic panel for epithelial mesothelioma: a reevaluation after heat-induced epitope retrieval. Am. J. Surg. Pathol. 21 12 (1997 Dec) 1409-1419
25. Dyck H.G., Hamilton T.C., Godwin A.K., Lynch H.T., Maines-Bandiera S., and Auersperg N. Autonomy of the epithelial phenotype in human ovarian surface epithelium: changes with neoplastic progression and with a family history of ovarian cancer. Int. J. Cancer 69 6 (1996 Dec 20) 429-436
26. Lewis B.P., Shih I.H., Jones-Rhoades M.W., Bartel D.P., and Burge C.B. Prediction of mammalian microRNA targets. Cell 115 7 (2003 Dec 26) 787-798
27. Matys V., Kel-Margoulis O.V., Fricke E., Liebich I., Land S., Barre-Dirrie A., et al. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 34 Database issue (2006 Jan 1) D108-D110
28. Remacle J.E., Kraft H., Lerchner W., Wuytens G., Collart C., Verschueren K., et al. New mode of DNA binding of multi-zinc finger transcription factors: deltaEF1 family members bind with two hands to two target sites. EMBO J. 18 18 (1999 Sep 15) 5073-5084
29. Thierry-Mieg D., and Thierry-Mieg J. AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol. 7 Suppl. 1 (2006) S12-1-4
30. Kuhn R.M., Karolchik D., Zweig A.S., Trumbower H., Thomas D.J., Thakkapallayil A., et al. The UCSC genome browser database: update 2007. Nucleic Acids Res. 35 Database issue (2007 Jan) D668-D673
31. Auersperg N., Pan J., Grove B.D., Peterson T., Fisher J., Maines-Bandiera S., et al. E-cadherin induces mesenchymal-to-epithelial transition in human ovarian surface epithelium. Proc. Natl. Acad. Sci. U. S. A. 96 11 (1999 May 25) 6249-6254
32. Sundfeldt K., Piontkewitz Y., Ivarsson K., Nilsson O., Hellberg P., Brannstrom M., et al. E-cadherin expression in human epithelial ovarian cancer and normal ovary. Int. J. Cancer 74 3 (1997 Jun 20) 275-280
33. Wu C., Cipollone J., Maines-Bandiera S., Tan C., Karsan A., Auersperg N., et al. The morphogenic function of E-cadherin-mediated adherens junctions in epithelial ovarian carcinoma formation and progression. Differentiation 76 2 (2008 Feb) 193-205
34. Comijn J., Berx G., Vermassen P., Verschueren K., van Grunsven L., Bruyneel E., et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell. 7 6 (2001 Jun) 1267-1278
35. Eger A., Aigner K., Sonderegger S., Dampier B., Oehler S., Schreiber M., et al. DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 24 14 (2005 Mar 31) 2375-2385
36. Shirakihara T., Saitoh M., and Miyazono K. Differential regulation of epithelial and mesenchymal markers by deltaEF1 proteins in epithelial mesenchymal transition induced by TGF-beta. Mol. Biol. Cell. 18 9 (2007 Sep) 3533-3544
37. Elloul S., Elstrand M.B., Nesland J.M., Trope C.G., Kvalheim G., Goldberg I., et al. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 103 8 (2005 Apr 15) 1631-1643
38. Elloul S., Silins I., Trope C.G., Benshushan A., Davidson B., and Reich R. Expression of E-cadherin transcriptional regulators in ovarian carcinoma. Virchows Arch. 449 5 (2006 Nov) 520-528
39. Sivertsen S., Hadar R., Elloul S., Vintman L., Bedrossian C., Reich R., et al. Expression of Snail, Slug and Sip1 in malignant mesothelioma effusions is associated with matrix metalloproteinase, but not with cadherin expression. Lung Cancer 54 3 (2006 Dec) 309-317
40. Faca V.M., Ventura A.P., Fitzgibbon M.P., Pereira-Faca S.R., Pitteri S.J., Green A.E., et al. Proteomic analysis of ovarian cancer cells reveals dynamic processes of protein secretion and shedding of extra-cellular domains. PLoS ONE 3 6 (2008) e2425
41. van Grunsven L.A., Taelman V., Michiels C., Opdecamp K., Huylebroeck D., and Bellefroid E.J. deltaEF1 and SIP1 are differentially expressed and have overlapping activities during Xenopus embryogenesis. Dev. Dyn. 235 6 (2006 Jun) 1491-1500
42. Ferrell Jr. J.E. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr. Opin. Cell. Biol. 14 2 (2002 Apr) 140-148
43. Tsang J., Zhu J., and van Oudenaarden A. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol. Cell. 26 5 (2007 Jun 8) 753-767
44. Ocana O.H., and Nieto M.A. A new regulatory loop in cancer-cell invasion. EMBO Rep. 9 6 (2008 Jun) 521-522
45. Moustakas A., and Heldin C.H. Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci. 98 10 (2007 Oct) 1512-1520
46. Bagnato A., and Rosano L. Epithelial-mesenchymal transition in ovarian cancer progression: a crucial role for the endothelin axis. Cells Tissues Organs 185 1-3 (2007) 85-94
47. Ahmed N., Thompson E.W., and Quinn M.A. Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm. J. Cell. Physiol. 213 3 (2007 Dec) 581-588