MicroRNA 31 functions as an endometrial cancer oncogene by suppressing Hippo tumor suppressor pathway

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Mitamura, Takashi ^a   Watari, Hidemichi ^a   Wang, Lei ^a   Kanno, Hiromi ^a   Kitagawa, Makiko ^a   Hassan, Mohamed K ^a,b   Kimura, Taichi ^a   Tanino, Mishie ^a   Nishihara, Hiroshi ^a   Tanaka, Shinya ^a   Sakuragi, Noriaki ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Port Said University   (Egypt)

Author keywords

cyclin D1; Endometrial cancer; Hippo pathway; LATS2; microRNA 31

Indexed keywords

CYCLIN D1; LATS2 PROTEIN; LUCIFERASE; MICRORNA 31; TRANSCRIPTION FACTOR YAP1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; CCND1 PROTEIN, HUMAN; HIPPO PROTEIN, HUMAN; LATS2 PROTEIN, HUMAN; MICRORNA; MIRN31 MICRORNA, HUMAN; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER SURVIVAL; CANCER TISSUE; CARCINOGENESIS; CELL NUCLEUS; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENDOMETRIUM CANCER; ENZYME REPRESSION; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LOW RISK PATIENT; LUCIFERASE ASSAY; NUCLEAR LOCALIZATION SIGNAL; ONCOGENE; PHENOTYPE; RECURRENCE RISK; SIGNAL TRANSDUCTION; ADULT; AGED; APOPTOSIS; BIOSYNTHESIS; ENDOMETRIUM TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; TUMOR CELL LINE; TUMOR RECURRENCE; TUMOR SUPPRESSOR GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT; AGED; APOPTOSIS; CELL LINE, TUMOR; CYCLIN D1; ENDOMETRIAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; MICRORNAS; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84902545225     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-97     Document Type: Article

References (46)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90. 10.3322/caac.20107, 21296855.
2. Amant F, Moerman P, Neven P, Timmerman D, Van Limbergen E, Vergote I. Endometrial cancer. Lancet 2005, 366:491-505. 10.1016/S0140-6736(05)67063-8, 16084259.
3. Pecorelli S. Revised FIGO staging for carcinoma of the vulva, cervix, and endometrium. Int J Gynaecol Obstet 2009, 105:103-104. 10.1016/j.ijgo.2009.02.012, 19367689.
4. Creasman WT, Morrow CP, Bundy BN, Homesley HD, Graham JE, Heller PB. Surgical pathologic spread patterns of endometrial cancer. A Gynecologic Oncology Group Study. Cancer 1987, 60:2035-2041. 10.1002/1097-0142(19901015)60:8+<2035::AID-CNCR2820601515>3.0.CO;2-8, 3652025.
5. Sakuragi N, Hareyama H, Todo Y, Yamada H, Yamamoto R, Fujino T, Sagawa T, Fujimoto S. Prognostic significance of serous and clear cell adenocarcinoma in surgically staged endometrial carcinoma. Acta Obstet Gynecol Scand 2000, 79:311-316. 10.1080/j.1600-0412.2000.079004311.x, 10746848.
6. Carey MS, O'Connell GJ, Johanson CR, Goodyear MD, Murphy KJ, Daya DM, Schepansky A, Peloquin A, Lumsden BJ. Good outcome associated with a standardized treatment protocol using selective postoperative radiation in patients with clinical stage I adenocarcinoma of the endometrium. Gynecol Oncol 1995, 57:138-144. 10.1006/gyno.1995.1115, 7729725.
7. Randall ME, Filiaci VL, Muss H, Spirtos NM, Mannel RS, Fowler J, Thigpen JT, Benda JA. Randomized phase III trial of whole-abdominal irradiation versus doxorubicin and cisplatin chemotherapy in advanced endometrial carcinoma: a Gynecologic Oncology Group Study. J Clin Oncol 2006, 24:36-44. 10.1200/JCO.2004.00.7617, 16330675.
8. Aoki Y, Kase H, Watanabe M, Sato T, Kurata H, Tanaka K. Stage III endometrial cancer: analysis of prognostic factors and failure patterns after adjuvant chemotherapy. Gynecol Oncol 2001, 83:1-5. 10.1006/gyno.2001.6321, 11585406.
9. Kurman RJ, Ellenson L, Ronnett B. Blaustein's Pathology of the Female Genital Tract 2011, New York: Springer, 6.
10. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 10.1016/j.cell.2009.01.002, 3794896, 19167326.
11. Chou YT, Lin HH, Lien YC, Wang YH, Hong CF, Kao YR, Lin SC, Chang YC, Lin SY, Chen SJ, Chen HC, Yeh SD, Wu CW. EGFR promotes lung tumorigenesis by activating miR-7 through a Ras/ERK/Myc pathway that targets the Ets2 transcriptional repressor ERF. Cancer Res 2010, 70:8822-8831. 10.1158/0008-5472.CAN-10-0638, 20978205.
12. Kong W, He L, Coppola M, Guo J, Esposito NN, Coppola D, Cheng JQ. MicroRNA-155 regulates cell survival, growth, and chemosensitivity by targeting FOXO3a in breast cancer. J Biol Chem 2010, 285:17869-17879. 10.1074/jbc.M110.101055, 2878550, 20371610.
13. Li N, Kaur S, Greshock J, Lassus H, Zhong X, Wang Y, Leminen A, Shao Z, Hu X, Liang S, Katsaros D, Huang Q, Butzow R, Weber BL, Coukos G, Zhang L. A combined array-based comparative genomic hybridization and functional library screening approach identifies mir-30d as an oncomir in cancer. Cancer Res 2012, 72:154-164. 10.1158/0008-5472.CAN-11-2484, 22058146.
14. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, Yuen ST, Chan TL, Kwong DL, Au GK, Liu CG, Calin GA, Croce CM, Harris CC. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008, 299:425-436. 2614237, 18230780.
15. Tsuruta T, Kozaki K, Uesugi A, Furuta M, Hirasawa A, Imoto I, Susumu N, Aoki D, Inazawa J. miR-152 is a tumor suppressor microRNA that is silenced by DNA hypermethylation in endometrial cancer. Cancer Res 2011, 71:6450-6462. 10.1158/0008-5472.CAN-11-0364, 21868754.
16. Dong P, Kaneuchi M, Watari H, Hamada J, Sudo S, Ju J, Sakuragi N. MicroRNA-194 inhibits epithelial to mesenchymal transition of endometrial cancer cells by targeting oncogene BMI-1. Mol Cancer 2011, 10:99. 10.1186/1476-4598-10-99, 3173388, 21851624.
17. Hiroki E, Suzuki F, Akahira J, Nagase S, Ito K, Sugawara J, Miki Y, Suzuki T, Sasano H, Yaegashi N. MicroRNA-34b functions as a potential tumor suppressor in endometrial serous adenocarcinoma. Int J Cancer 2012, 131:E395-404. 10.1002/ijc.27345, 22052540.
18. Chung TK, Lau TS, Cheung TH, Yim SF, Lo KW, Siu NS, Chan LK, Yu MY, Kwong J, Doran G, Barroilhet LM, Ng AS, Wong RR, Wang VW, Mok SC, Smith DI, Berkowitz RS, Wong YF. Dysregulation of microRNA-204 mediates migration and invasion of endometrial cancer by regulating FOXC1. Int J Cancer 2012, 130:1036-1045. 10.1002/ijc.26060, 21400511.
19. Wu Y, Liu S, Xin H, Jiang J, Younglai E, Sun S, Wang H. Up-regulation of microRNA-145 promotes differentiation by repressing OCT4 in human endometrial adenocarcinoma cells. Cancer 2011, 117:3989-3998. 10.1002/cncr.25944, 21365617.
20. Huang YW, Liu JC, Deatherage DE, Luo J, Mutch DG, Goodfellow PJ, Miller DS, Huang TH. Epigenetic repression of microRNA-129-2 leads to overexpression of SOX4 oncogene in endometrial cancer. Cancer Res 2009, 69:9038-9046. 10.1158/0008-5472.CAN-09-1499, 2789184, 19887623.
21. Jiang F, Liu T, He Y, Yan Q, Chen X, Wang H, Wan X. MiR-125b promotes proliferation and migration of type II endometrial carcinoma cells through targeting TP53INP1 tumor suppressor in vitro and in vivo. BMC Cancer 2011, 11:425. 10.1186/1471-2407-11-425, 3210504, 21970405.
22. Sun D, Yu F, Ma Y, Zhao R, Chen X, Zhu J, Zhang CY, Chen J, Zhang J. MicroRNA-31 Activates the RAS Pathway and Functions as an Oncogenic MicroRNA in Human Colorectal Cancer by Repressing RAS p21 GTPase Activating Protein 1 (RASA1). J Biol Chem 2013, 288:9508-9518. 10.1074/jbc.M112.367763, 3611019, 23322774.
23. Alder H, Taccioli C, Chen H, Jiang Y, Smalley KJ, Fadda P, Ozer HG, Huebner K, Farber JL, Croce CM, Fong LY. Dysregulation of miR-31 and miR-21 induced by zinc deficiency promotes esophageal cancer. Carcinogenesis 2012, 33:1736-1744. 10.1093/carcin/bgs204, 3514898, 22689922.
24. Liu X, Sempere LF, Ouyang H, Memoli VA, Andrew AS, Luo Y, Demidenko E, Korc M, Shi W, Preis M, Dragnev KH, Li H, Direnzo J, Bak M, Freemantle SJ, Kauppinen S, Dmitrovsky E. MicroRNA-31 functions as an oncogenic microRNA in mouse and human lung cancer cells by repressing specific tumor suppressors. J Clin Invest 2010, 120:1298-1309. 10.1172/JCI39566, 2846041, 20237410.
25. Liu CJ, Lin SC, Yang CC, Cheng HW, Chang KW. Exploiting salivary miR-31 as a clinical biomarker of oral squamous cell carcinoma. Head Neck 2012, 34:219-224. 10.1002/hed.21713, 22083872.
26. Liu CJ, Tsai MM, Hung PS, Kao SY, Liu TY, Wu KJ, Chiou SH, Lin SC, Chang KW. miR-31 ablates expression of the HIF regulatory factor FIH to activate the HIF pathway in head and neck carcinoma. Cancer Res 2010, 70:1635-1644. 10.1158/0008-5472.CAN-09-2291, 20145132.
27. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szasz AM, Wang ZC, Brock JE, Richardson AL, Weinberg RA. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 2009, 137:1032-1046. 10.1016/j.cell.2009.03.047, 2766609, 19524507.
28. Zhang Y, Guo J, Li D, Xiao B, Miao Y, Jiang Z, Zhuo H. Down-regulation of miR-31 expression in gastric cancer tissues and its clinical significance. Med Oncol 2010, 27:685-689. 10.1007/s12032-009-9269-x, 19598010.
29. Ivanov SV, Goparaju CM, Lopez P, Zavadil J, Toren-Haritan G, Rosenwald S, Hoshen M, Chajut A, Cohen D, Pass HI. Pro-tumorigenic effects of miR-31 loss in mesothelioma. J Biol Chem 2010, 285:22809-22817. 10.1074/jbc.M110.100354, 2906272, 20463022.
30. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 2010, 24:862-874. 10.1101/gad.1909210, 2861185, 20439427.
31. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai ZC, Guan KL. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007, 21:2747-2761. 10.1101/gad.1602907, 2045129, 17974916.
32. Steinhardt AA, Gayyed MF, Klein AP, Dong J, Maitra A, Pan D, Montgomery EA, Anders RA. Expression of Yes-associated protein in common solid tumors. Hum Pathol 2008, 39:1582-1589. 10.1016/j.humpath.2008.04.012, 2720436, 18703216.
33. Zhao B, Li L, Wang L, Wang CY, Yu J, Guan KL. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev 2012, 26:54-68. 10.1101/gad.173435.111, 3258966, 22215811.
34. Liu X, Cheng Y, Chen X, Yang J, Xu L, Zhang C. MicroRNA-31 regulated by the extracellular regulated kinase is involved in vascular smooth muscle cell growth via large tumor suppressor homolog 2. J Biol Chem 2011, 286:42371-42380. 10.1074/jbc.M111.261065, 3234904, 22020941.
35. Augoff K, McCue B, Plow EF, Sossey-Alaoui K. miR-31 and its host gene lncRNA LOC554202 are regulated by promoter hypermethylation in triple-negative breast cancer. Mol Cancer 2012, 11:5. 10.1186/1476-4598-11-5, 3298503, 22289355.
36. Xu RS, Wu XD, Zhang SQ, Li CF, Yang L, Li DD, Zhang BG, Zhang Y, Jin JP, Zhang B. The tumor suppressor gene RhoBTB1 is a novel target of miR-31 in human colon cancer. Int J Oncol 2013, 42:676-682.
37. Goulev Y, Fauny JD, Gonzalez-Marti B, Flagiello D, Silber J, Zider A. SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr Biol 2008, 18:435-441. 10.1016/j.cub.2008.02.034, 18313299.
38. Hamaratoglu F, Willecke M, Kango-Singh M, Nolo R, Hyun E, Tao C, Jafar-Nejad H, Halder G. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 2006, 8:27-36. 10.1038/ncb1339, 16341207.
39. Wang Y, Xie C, Li Q, Xu K, Wang E. Clinical and prognostic significance of Yes-associated protein in colorectal cancer. Tumour Biol 2013, 34:2169-2174. 10.1007/s13277-013-0751-x, 23558963.
40. Thompson BJ, Cohen SM. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 2006, 126:767-774. 10.1016/j.cell.2006.07.013, 16923395.
41. Aylon Y, Ofir-Rosenfeld Y, Yabuta N, Lapi E, Nojima H, Lu X, Oren M. The Lats2 tumor suppressor augments p53-mediated apoptosis by promoting the nuclear proapoptotic function of ASPP1. Genes Dev 2010, 24:2420-2429. 10.1101/gad.1954410, 2964752, 21041410.
42. Vigneron AM, Ludwig RL, Vousden KH. Cytoplasmic ASPP1 inhibits apoptosis through the control of YAP. Genes Dev 2010, 24:2430-2439. 10.1101/gad.1954310, 2964753, 21041411.
43. Sakuragi N, Watari H, Ebina Y, Yamamoto R, Steiner E, Koelbl H, Yano M, Tada M, Moriuchi T. Functional analysis of p53 gene and the prognostic impact of dominant-negative p53 mutation in endometrial cancer. Int J Cancer 2005, 116:514-519. 10.1002/ijc.21097, 15825182.
44. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
45. Mitamura T, Watari H, Wang L, Kanno H, Hassan MK, Miyazaki M, Katoh Y, Kimura T, Tanino M, Nishihara H, Tanaka S, Sakuragi N. Downregulation of miRNA-31 induces taxane resistance in ovarian cancer cells through increase of receptor tyrosine kinase MET. Oncogenesis 2013, 2:e40. 10.1038/oncsis.2013.3, 3641356, 23552883.
46. Komuro A, Nagai M, Navin NE, Sudol M. WW domain-containing protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J Biol Chem 2003, 278:33334-33341. 10.1074/jbc.M305597200, 12807903.