The reciprocal regulation loop of Notch2 pathway and miR-23b in controlling gastric carcinogenesis

Oncotarget

Volumn 6, Issue 20, 2015, Pages 18012-18026

  Huang, Tzu Ting ^a   Ping, Yueh Hsin ^a   Wang, An Ming ^a   Ke, Chia Chi ^a   Fang, Wen Liang ^a,b   Huang, Kuo Hung ^a,b   Lee, Hsin Chen ^a   Chi, Chin Wen ^a,b   Yeh, Tien Shun ^a,c  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

E2F1; Ets1; Gastric carcinogenesis; miR 23b; Notch2 receptor

Indexed keywords

HERMES ANTIGEN; MICRORNA; MICRORNA 23B; NERVE CELL ADHESION MOLECULE; NOTCH2 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; ONCOPROTEIN; PLAKOGLOBIN; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; UVOMORULIN; V ETS ERYTHROBLASTOSIS VIRUS E26 ONCOGENE HOMOLOG 1; VIMENTIN; 3' UNTRANSLATED REGION; E2F1 PROTEIN, HUMAN; ETS1 PROTEIN, HUMAN; MIRN23 MICRORNA, HUMAN; NOTCH2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR ETS 1;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL VIABILITY; CLINICAL ARTICLE; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG METASTASIS; MALE; MOUSE; NONHUMAN; PROTEIN FUNCTION; STOMACH ADENOCARCINOMA; STOMACH CARCINOGENESIS; UPREGULATION; ADENOCARCINOMA; ANIMAL; BAGG ALBINO MOUSE; CANCER STEM CELL; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; GENE THERAPY; GENETIC TRANSFECTION; GENETICS; LUNG NEOPLASMS; METABOLISM; NONOBESE DIABETIC MOUSE; NUDE MOUSE; PATHOLOGY; PLURIPOTENT STEM CELL; SCID MOUSE; SECONDARY; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TIME FACTOR; TUMOR CELL LINE; TUMOR INVASION;

3' UNTRANSLATED REGIONS; ADENOCARCINOMA; ANIMALS; BINDING SITES; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; E2F1 TRANSCRIPTION FACTOR; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC THERAPY; HUMANS; LUNG NEOPLASMS; MALE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PLURIPOTENT STEM CELLS; PROTO-ONCOGENE PROTEIN C-ETS-1; RECEPTOR, NOTCH2; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TIME FACTORS; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84938674682     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4000     Document Type: Article

References (45)

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015; 136:E359-386.
2. Yin L, Velazquez OC, Liu ZJ. Notch signaling: emerging molecular targets for cancer therapy. Biochem Pharmacol. 2010; 80:690-701.
3. Andersson ER, Lendahl U. Therapeutic modulation of Notch signalling-are we there yet? Nat Rev Drug Discov. 2014; 13:357-378.
4. Tseng YC, Tsai YH, Tseng MJ, Hsu KW, Yang MC, Huang KH, Li AF, Chi CW, Hsieh RH, Ku HH, Yeh TS. Notch2-induced COX-2 expression enhancing gastric cancer progression. Mol Carcinog. 2012; 51:939-951.
5. Yeh TS, Wu CW, Hsu KW, Liao WJ, Yang MC, Li AF, Wang AM, Kuo ML, Chi CW. The activated Notch1 signal pathway is associated with gastric cancer progression through cyclooxygenase-2. Cancer Res. 2009; 69:5039-5048.
6. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, Brown M, Viens P, Xerri L, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 2009; 69:1302-1313.
7. Li Z, Rana TM. Therapeutic targeting of microRNAs: Current status and future challenges. Nat Rev Drug Discov. 2014; 13:622-638.
8. Garzon R, Marcucci G, Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov. 2010; 9:775-789.
9. Thiel A, Ristimäki A. Gastric cancer: basic aspects. Helicobacter. 2012; 17:26-29.
10. Wang Z, Li Y, Kong D, Ahmad A, Banerjee S, Sarkar FH. Cross-talk between miRNA and Notch signaling pathways in tumor development and progression. Cancer Lett. 2010; 292:141-148.
11. Mo YY, Tang H, Miele L. Notch-associated microRNAs in cancer. Curr Drug Targets. 2013; 14:1157-1166.
12. Kefas B, Comeau L, Floyd DH, Seleverstov O, Godlewski J, Schmittgen T, Jiang J, diPierro CG, Li Y, Chiocca EA, Lee J, Fine H, Abounader R, et al. The neuronal microRNA miR-326 acts in a feedback loop with notch and has therapeutic potential against brain tumors. J Neurosci. 2009; 29:15161-15168.
13. Kumar V, Palermo R, Talora C, Campese AF, Checquolo S, Bellavia D, Tottone L, Testa G, Miele E, Indraccolo S, Amadori A, Ferretti E, Gulino A, et al. Notch and NF-kB signaling pathways regulate miR-223/FBXW7 axis in T-cell acute lymphoblastic leukemia. Leukemia. 2014; 28:2324-2335.
14. Ji Q, Hao X, Meng Y, Zhang M, DeSano J, Fan D, Xu L. Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer. 2008; 8:266.
15. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, Desano JT, Bommer GT, Fan D, Fearon ER, Lawrence TS, Xu L. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One. 2009; 4:e6816.
16. Chen L, Chen XR, Zhang R, Li P, Liu Y, Yan K, Jiang XD. MicroRNA-107 inhibits glioma cell migration and invasion by modulating Notch2 expression. J Neurooncol. 2013; 112:59-66.
17. Chen L, Zhang R, Li P, Liu Y, Qin K, Fa ZQ, Liu YJ, Ke YQ, Jiang XD. P53-induced microRNA-107 inhibits proliferation of glioma cells and down-regulates the expression of CDK6 and Notch-2. Neurosci Lett. 2013; 534:327-332.
18. Chao CH, Chang CC, Wu MJ, Ko HW, Wang D, Hung MC, Yang JY, Chang CJ. MicroRNA-205 signaling regulates mammary stem cell fate and tumorigenesis. J Clin Invest. 2014; 124:3093-3106.
19. Meng P, Ghosh R. Transcription addiction: can we garner the Yin and Yang functions of E2F1 for cancer therapy? Cell Death Dis. 2014; 5:e1360.
20. Wu JG, Yu JW, Wu HB, Zheng LH, Ni XC, Li XQ, Du GY, Jiang BJ. Expressions and clinical significances of c-MET, p-MET and E2f-1 in human gastric carcinoma. BMC Res Notes. 2014; 7:6.
21. Zheng L, Pu J, Qi T, Qi M, Li D, Xiang X, Huang K, Tong Q. miRNA-145 targets v-ets erythroblastosis virus E26 oncogene homolog 1 to suppress the invasion, metastasis, and angiogenesis of gastric cancer cells. Mol Cancer Res. 2013; 11:182-193.
22. Messeguer X, Escudero R, Farre D, Nunez O, Martinez J, Alba MM. PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics. 2002; 18:333-334.
23. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV, Ignatieva EV, Ananko EA, Podkolodnaya OA, Kolpakov FA, Podkolodny NL, Kolchanov NA. Databases on transcriptional regulation: TRANSFAC, TRRD, and COMPEL. Nucleic Acids Res. 1998; 26:362-367.
24. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller KI, De Marzo AM, Van Eyk JE, Mendell JT, Dang CV. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature. 2009; 458:762-765.
25. Klinakis A, Szabolcs M, Politi K, Kiaris H, Artavanis-Tsakonas S, Efstratiadis A. Myc is a Notch1 transcriptional target and a requisite for Notch1-induced mammary tumorigenesis in mice. Proc Natl Acad Sci U S A. 2006; 103:9262-9267.
26. Weng AP, Millholland JM, Yashiro-Ohtani Y, Arcangeli ML, Lau A, Wai C, Del Bianco C, RodriguezCG, Sai H, TobiasJ, Li Y, Wolfe MS, Shachaf C, et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 2006; 20:2096-2109.
27. Palomero T, Lim WK, Odom DT, Sulis ML, Real PJ, Margolin A, Barnes KC, O'Neil J, Neuberg D, Weng AP, Aster JC, Sigaux F, Soulier J, et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc Natl Acad Sci U S A. 2006; 103:18261-18266.
28. Liao WR, Hsieh RH, Hsu KW, Wu MZ, Tseng MJ, Mai RT, Lee YH, Yeh TS. The CBF1-independent Notch1 signal pathway activates human c-myc expression partially via transcription factor YY1. Carcinogenesis. 2007; 28:1867-1876.
29. Leone G, DeGregori J, Sears R, Jakoi L, Nevins JR. Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature. 1997; 387:422-426.
30. Matsumura I, Tanaka H, Kanakura Y. E2F1 and c-Myc in cell growth and death. Cell Cycle. 2003; 2:333-338.
31. Wang AM, Huang TT, Hsu KW, Huang KH, Fang WL, Yang MH, Lo SS, Chi CW, Lin JJ, Yeh TS. Yin Yang 1 is a target of microRNA-34 family and contributes to gastric carcinogenesis. Oncotarget. 2014; 5:5002-5016.
32. Ell B, Qiu Q, Wei Y, Mercatali L, Ibrahim T, Amadori D, Kang Y. The microRNA-23b/27b/24 cluster promotes breast cancer lung metastasis by targeting metastasis-suppressive gene prosaposin. J Biol Chem. 2014; 289:21888-21895.
33. Jin L, Wessely O, Marcusson EG, Ivan C, Calin GA, Alahari SK. Prooncogenic factors miR-23b and miR-27b are regulated by Her2/Neu, EGF, and TNF-α in breast cancer. Cancer Res. 2013; 73:2884-2896.
34. Ishteiwy RA, Ward TM, Dykxhoorn DM, Burnstein KL. The microRNA-23b/-27b cluster suppresses the metastatic phenotype of castration-resistant prostate cancer cells. PLoS One. 2012; 7:e52106.
35. Zhang H, Hao Y, Yang J, Zhou Y, Li J, Yin S, Sun C, Ma M, Huang Y, Xi JJ. Genome-wide functional screening of miR-23b as a pleiotropic modulator suppressing cancer metastasis. Nat Commun. 2011; 2:554.
36. Salvi A, Sabelli C, Moncini S, Venturin M, Arici B, Riva P, Portolani N, Giulini SM, De Petro G, Barlati S. MicroRNA-23b mediates urokinase and c-met downmodulation and a decreased migration of human hepatocellular carcinoma cells. FEBS J. 2009; 276:2966-2982.
37. Pellegrino L, Stebbing J, Braga VM, Frampton AE, Jacob J, Buluwela L, Jiao LR, Periyasamy M, Madsen CD, Caley MP, Ottaviani S, Roca-Alonso L, El-Bahrawy M, et al. miR-23b regulates cytoskeletal remodeling, motility and metastasis by directly targeting multiple transcripts. Nucleic Acids Res. 2013; 41:5400-5412.
38. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011; 17:211-215.
39. Oettgen P, Barcinski M, Boltax J, Stolt P, Akbarali Y, Libermann TA. Genomic organization of the human ELF3 (ESE-1/ESX) gene, a member of the Ets transcription factor family, and identification of a functional promoter. Genomics. 1999; 55:358-362.
40. Hsu KW, Wang AM, Ping YH, Huang KH, Huang TT, Lee HC, Lo SS, Chi CW, Yeh TS. Down-regulation of tumor suppressor MBP-1 by microRNA-363 in gastric carcinogenesis. Carcinogenesis. 2014; 35:208-217.
41. Zhou R, Hu G, Gong AY, Chen XM. Binding of NF-kappaB p65 subunit to the promoter elements is involved in LPS-induced transactivation of miRNA genes in human biliary epithelial cells. Nucleic Acids Res. 2010; 38:3222-3232.
42. Chang CC, Hsu WH, Wang CC, Chou CH, Kuo MY, Lin BR, Chen ST, Tai SK, Kuo ML, Yang MH. Connective tissue growth factor activates pluripotency genes and mesenchymal-epithelial transition in head and neck cancer cells. Cancer Res. 2013; 73:4147-4157.
43. Hsu KW, Hsieh RH, Lee YH, Chao CH, Wu KJ, Tseng MJ, Yeh TS. The activated Notch1 receptor cooperates with alpha-enolase and MBP-1 in modulating c-myc activity. Mol Cell Biol. 2008; 28:4829-4842.
44. Hsu KW, Hsieh RH, Wu CW, Chi CW, Lee YH, Kuo ML, Wu KJ, Yeh TS. MBP-1 suppresses growth and metastasis of gastric cancer cells through COX-2. Mol Biol Cell. 2009; 20:5127-5137.
45. Wang AM, Ku HH, Liang YC, Chen YC, Hwu YM, Yeh TS. The autonomous notch signal pathway is activated by baicalin and baicalein but is suppressed by niclosamide in K562 cells. J Cell Biochem. 2009; 106:682-692.