Id-1, a protein repressed by miR-29b, facilitates the TGFβ1-induced epithelial-mesenchymal transition in human ovarian cancer cells

Cellular Physiology and Biochemistry

Volumn 33, Issue 3, 2014, Pages 717-730

  Teng, Yue ^a   Zhao, Le ^a   Zhang, Yan ^a   Chen, Wei ^a   Li, Xu ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

Epithelial Mesenchymal Transition (EMT); Inhibitor of DNA binding 1 (Id 1); Micro RNAs; Ovarian Cancer; Transforming Growth Factor Beta 1 (TGF 1)

Indexed keywords

INHIBITOR OF DIFFERENTIATION 1; MESSENGER RNA; MICRORNA 29B; NERVE CELL ADHESION MOLECULE; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN; ID1 PROTEIN, HUMAN; MICRORNA; MIRN29 MICRORNA, HUMAN; RNA; TGFB1 PROTEIN, HUMAN; TUMOR PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; CELL MIGRATION; CELL MIGRATION ASSAY; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; OVARY CANCER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; WESTERN BLOTTING; WOUND HEALING; FEMALE; METABOLISM; OVARY TUMOR; PATHOLOGY; TUMOR CELL LINE; CELL INVASION; CELL MOTILITY; GENE REPRESSION; GENE SILENCING; OVARIAN CANCER CELL LINE; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; TRANSCRIPTION REGULATION;

CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; MICRORNAS; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; RNA, NEOPLASM; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84896426416     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000358647     Document Type: Article

References (63)

1. Siegel R, Naishadham D, Jemal A: Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
2. Eskander RN, Tewari KS: Epithelial cell-adhesion molecule-directed trifunctional antibody immunotherapy for symptom management of advanced ovarian cancer. Clin Pharmacol 2013;5:S55-61.
3. Huang RY, Chung VY, Thiery JP: Targeting pathways contributing to epithelial-mesenchymal transition (EMT) in epithelial ovarian cancer. Curr Drug Targets 2012;13:1649-1653.
4. Cano A, Portillo F: An emerging role for class I bHLH E2-2 proteins in EMT regulation and tumor progression. Cell Adh Migr 2010;4:56-60.
5. Mallini P, Lennard T, Kirby J, Meeson A: Epithelial-to-mesenchymal transition: What is the impact on breast cancer stem cells and drug resistance. Cancer Treat Rev 2014;40:341-348.
6. Lopez-Novoa JM, Nieto MA: Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 2009;1:303-314.
7. Fabregat I, Fernando J, Mainez J, Sancho P: TGF-Beta Signaling in Cancer Treatment. Curr Pharm Des 2013 [Epub ahead of print]
8. Wang Y, Wu B, Chamberlain AA, Lui W, Koirala P, Susztak K, Klein D, Taylor V, Zhou B: Endocardial to myocardial notch-wnt-bmp axis regulates early heart valve development. PLoS One 2013;8:e60244.
9. Song Q, Sheng W, Zhang X, Jiao S, Li F: ILEI drives epithelial to mesenchymal transition and metastatic progression in the lung cancer cell line A549. Tumour Biol 2014;35:1377-1382.
10. Kim HD, Meyer AS, Wagner JP, Alford SK, Wells A, Gertler FB, Lauffenburger DA: Signaling network state predicts twist-mediated effects on breast cell migration across diverse growth factor contexts. Mol Cell Proteomics 2011;10:M111.008433.
11. Roberts AB: Molecular and cell biology of TGF-β. Miner Electrolyte Metab 1998;24:111-119.
12. Kingsley DM: The TGF-beta superfamily: New members, new receptors, and new genetic tests of function in different organisms. Genes Dev 1994;8:133-146.
13. Thiery JP, Acloque H, Huang RY, Nieto MA: Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-890.
14. Levy L, Hill CS: Alterations in components of the TGF-b superfamily signaling pathways in human cancer. Cytokine Growth Factor 2006;17:41-58.
15. Miettinen PJ, Ebner R, Lopez AR, Derynck R: TGF-β induced trans-differentiation of mammary epithelial cells to mesenchymal cells: Involvement of type I receptors. J. Cell Biol 1994;127:2021-36.
16. Zhang YE: Non-Smad pathways in TGF-beta signaling. Cell Res 2009;19:128-139.
17. Zavadil J, Narasimhan M, Blumenberg M, Schneider RJ: Transforming Growth Factor-β and microRNA:mRNA Regulatory Networks in Epithelial Plasticity. Cells Tissues Organs 2007;185:157-161.
18. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ: The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008;10:593-601.
19. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H: The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990;61:49-59.
20. Perk J, Iavarone A, Benezra R: Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 2005;5:603-614.
21. Benezra R, Rafii S, Lyden D: The Id proteins and angiogenesis. Oncogene 2001;20:8334-8341.
22. Ruzinova MB, Benezra R: Id proteins in development, cell cycle and cancer. Trends Cell Biol 2003;13:410-418.
23. Maw MK, Fujimoto J, Tamaya T: Overexpression of inhibitor of DNA-binding (ID)-1 protein related to angiogenesis in tumor advancement of ovarian cancers. BMC Cancer 2009;9:430.
24. Schindl M, Schoppmann SF, Ströbel T, Heinzl H, Leisser C, Horvat R, Birner P: Level of Id-1 protein expression correlates with poor differentiation, enhanced malignant potential, and more aggressive clinical behavior of epithelial ovarian tumors. Clin Cancer Res 2003;9:779-785.
25. Hu H, Wang YL, Wang GW, Wong YC, Wang XF, Wang Y, Xu KX: A novel role of Id-1 in regulation of epithelial-to-mesenchymal transition in bladder cancer. Urol Oncol 2013;31:1242-1253.
26. Cheung PY, Yip YL, Tsao SW, Ching YP, Cheung AL: Id-1 induces cell invasiveness in immortalized epithelial cells by regulating cadherin switching and Rho GTPases. J Cell Biochem 2011;112:157-168.
27. Jordà M, Vinyals A, Marazuela A, Cubillo E, Olmeda D, Valero E, Cano A, Fabra A: Id-1 is induced in MDCK epithelial cells by activated Erk/MAPK pathway in response to expression of the Snail and E47 transcription factors. Exp Cell Res 2007;313:2389-2403.
28. Slack FJ, Weidhaas JB: MicroRNA in cancer prognosis. N Engl J Med 2008;359:2720-2722.
29. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R: Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 2006;20:515-524.
30. Guo H, Ingolia NT, Weissman JS, Bartel DP: Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010;466:835-840.
31. Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-297.
32. Ambros V: The functions of animal microRNAs. Nature 2004;431:350-355.
33. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y, Takahashi T: A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005;65:9628-9632.
34. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR: MicroRNA expression profiles classify human cancers. Nature 2005;435:834-838.
35. Garzon R, Heaphy CE, Havelange V, Fabbri M, Volinia S, Tsao T, Zanesi N, Kornblau SM, Marcucci G, Calin GA, Andreeff M, Croce CM: MicroRNA 29b functions in acute myeloid leukemia. Blood 2009;114:5331-5341.
36. Sekiya Y, Ogawa T, Yoshizato K, Ikeda K, Kawada N: Suppression of hepatic stellate cell activation by microRNA-29b. Biochem Biophys Res Commun 2011;412:74-79.
37. Xu F, Zhang Q, Cheng W, Zhang Z, Wang J, Ge J: Effect of miR-29b-1 and miR-29c knockdown on cell growth of the bladder cancer cell line T24. J Int Med Res 2013;41:1803-1810.
38. Poudyal D, Cui X, Le PM, Hofseth AB, Windust A, Nagarkatti M, Nagarkatti PS, Schetter AJ, Harris CC, Hofseth LJ: A key role of microRNA-29b for the suppression of colon cancer cell migration by American ginseng. PLoS One 2013;8:e75034.
39. Flavin R, Smyth P, Barrett C, Russell S, Wen H, Wei J, Laios A, O'Toole S, Ring M, Denning K, Li J, Aherne S, Sammarae D, Aziz NA, Alhadi A, Finn SP, Loda M, B S, Sheils O, O'Leary JJ: miR-29b expression is associated with disease-free survival in patients with ovarian serous carcinoma. Int J Gynecol Cancer 2009;19:641-647.
40. Dai F, Zhang Y, Zhu X, Shan N, Chen Y: Anticancer role of MUC1 aptamer-miR-29b chimera in epithelial ovarian carcinoma cells through regulation of PTEN methylation. Target Oncol 2012;7:217-225.
41. Ramdas V, McBride M, Denby L, Baker AH: Canonical Transforming Growth Factor-β Signaling Regulates Disintegrin Metalloprotease Expression in Experimental Renal Fibrosis via miR-29. Am J Pathol 2013;183:1885-1896.
42. Wang G, Kwan BC, Lai FM, Chow KM, Li PK, Szeto CC: Urinary miR-21, miR-29, and miR-93: novel biomarkers of fibrosis. Am J Nephrol 2012;36:412-418.
43. Roderburg C, Urban GW, Bettermann K, Vucur M, Zimmermann H, Schmidt S, Janssen J, Koppe C, Knolle P, Castoldi M, Tacke F, Trautwein C, Luedde T: Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 2011;53:209-218.
44. De Craene B, Berx G: Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013;13:97-110.
45. Strong N, Millena AC, Walker L, Chaudhary J, Khan SA: Inhibitor of differentiation 1 (Id1) and Id3 proteins play different roles in TGFβ effects on cell proliferation and migration in prostate cancer cells. Prostate 2013;73:624-633.
46. Ponz-Sarvisé M, Castañón E, Panizo-Santos A, Redrado M, López I, Rosell D, Gil-Aldea I, Calvo A, Nguewa PA, Gil-Bazo I: Differential Tumor Expression of Inhibitor of Differentiation-1 in Prostate Cancer Patients With Extreme Clinical Phenotypes and Prognostic Implications. Clin Genitourin Cancer DOI:pii: S1558-7673(13)00210-3.
47. Sun L, Li X, Liu G: Expression of Id1 and Id3 in endometrial carcinoma and their roles in regulating biological behaviors of endometrial carcinoma cells in vitro. Nan Fang Yi Ke Da Xue Xue Bao 2013;33:812-818.
48. Padua D, Zhang XH, Wang Q, Nadal C, Gerald WL, Gomis RR, Massagué J: TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like4. Cell 2008;133:66-77.
49. McManus MT: MicroRNAs and cancer. Semin Cancer Biol 2003;13:253-258.
50. Rothschild SI, Tschan MP, Federzoni EA, Jaggi R, Fey MF, Gugger M, Gautschi O: MicroRNA-29b is involved in the Src-ID1 signaling pathway and is dysregulated in human lung adenocarcinoma. Oncogene 2012;31:4221-4232.
51. Walter BA, Valera VA, Pinto PA, Merino MJ: Comprehensive microRNA Profiling of Prostate Cancer. J Cancer 2013;4:350-357.
52. Wu Y, Crawford M, Mao Y, Lee RJ, Davis IC, Elton TS, Lee LJ, Nana-Sinkam SP: Therapeutic Delivery of MicroRNA-29b by Cationic Lipoplexes for Lung Cancer. Mol Ther Nucleic Acids DOI: 10.1038/mtna.2013.14.
53. Wang C, Bian Z, Wei D, Zhang JG: miR-29b regulates migration of human breast cancer cells. Mol Cell Biochem 2011;352:197-207.
54. Chou J, Lin JH, Brenot A, Kim JW, Provot S, Werb Z: GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol 2012;15:201-213.
55. Melo SA, Kalluri R: miR-29b moulds the tumour microenvironment to repress metastasis. Nat Cell Biol 2012;15:139-140.
56. Fang JH, Zhou HC, Zeng C, Yang J, Liu Y, Huang X, Zhang JP, Guan XY, Zhuang SM: MicroRNA-29b suppresses tumor angiogenesis, invasion, and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology 2011;54:1729-1740.
57. Wang C, Bian Z, Wei D, Zhang JG: miR-29b regulates migration of human breast cancer cells. Mol Cell Biochem 2011;352:197-207.
58. Wang G, Kwan BC, Lai FM, Chow KM, Li PK, Szeto CC: Urinary miR-21, miR-29, and miR-93: novel biomarkers of fibrosis. Am J Nephrol 2012;36:412-418.
59. Vergara D, Merlot B, Lucot JP, Collinet P, Vinatier D, Fournier I, Salzet M: Epithelial-mesenchymal transition in ovarian cancer. Cancer Lett 2010;291:59-66.
60. Qin W, Chung AC, Huang XR, Meng XM, Hui DS, Yu CM, Sung JJ, Lan HY: TGF-β/Smad3 signaling promotes renal fibrosis by inhibiting miR-29. J Am Soc Nephrol 2011;22:1462-1474.
61. Cushing L, Kuang PP, Qian J, Shao F, Wu J, Little F, Thannickal VJ, Cardoso WV, Lü J: miR-29 is a major regulator of genes associated with pulmonary fibrosis. Am J Respir Cell Mol Biol 2011;45:287-294.
62. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN: Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA 2008;105:13027-13032.
63. Roderburg C, Urban GW, Bettermann K, Vucur M, Zimmermann H, Schmidt S, Janssen J, Koppe C, Knolle P, Castoldi M, Tacke F, Trautwein C, Luedde T: Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 2011;53:209-218.