Up-regulation of microRNA-210 inhibits proliferation of hepatocellular carcinoma cells by targeting Yes1

World Journal of Gastroenterology

Volumn 21, Issue 46, 2015, Pages 13030-13041

  Tan, Weiqi ^a   Lim, Seng Gee ^b   Tan, Theresa M C ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b Dept Medicine Endocrinol Diabet   (Singapore)

Author keywords

Hepatocellular carcinoma; MicroRNA 210; Proliferation; Yes1

Indexed keywords

MICRORNA 210; NOCODAZOLE; PROTEIN; PROTEIN YES1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; MICRORNA; MIRN210 MICRORNA, HUMAN; PROTEIN KINASE YES; YES1 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ADULT; AGED; ARTICLE; CANCER TISSUE; CARCINOMA CELL; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL POPULATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HEPATOCELLULAR CARCINOMA CELL LINE; HEPG2 CELL LINE; HUH7 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL CARCINOMA; LUCIFERASE ASSAY; MALE; MIDDLE AGED; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; BINDING SITE; ENZYMOLOGY; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; GENETICS; HEP-G2 CELL LINE; LIVER TUMOR; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR;

3' UNTRANSLATED REGIONS; ADULT; AGED; BINDING SITES; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MICRORNAS; MIDDLE AGED; PROTO-ONCOGENE PROTEINS C-YES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84950266247     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v21.i46.13030     Document Type: Article

References (56)

1. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004;23:4051-4060 [PMID: 15372072]
2. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, Kim VN. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003;425:415-419 [PMID: 14508493]
3. Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004;18:3016-3027 [PMID: 15574589]
4. Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science 2004;303:95-98 [PMID: 14631048]
5. Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001;293:834-838 [PMID: 11452083]
6. Billy E, Brondani V, Zhang H, Müller U, Filipowicz W. Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc Natl Acad Sci USA 2001;98:14428-14433 [PMID: 11724966]
7. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005;123:631-640 [PMID: 16271387]
8. Maniataki E, Mourelatos Z. A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes Dev 2005;19:2979-2990 [PMID: 16357216]
9. Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002;297:2056-2060 [PMID: 12154197]
10. Yekta S, Shih IH, Bartel DP. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004;304:594-596 [PMID: 15105502]
11. Doench JG, Petersen CP, Sharp PA. siRNAs can function as miRNAs. Genes Dev 2003;17:438-442 [PMID: 12600936]
12. Camps C, Buffa FM, Colella S, Moore J, Sotiriou C, Sheldon H, Harris AL, Gleadle JM, Ragoussis J. hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 2008;14:1340-1348 [PMID: 18316553 DOI: 10.1158/1078-0432. CCR-07-1755]
13. Giannakakis A, Sandaltzopoulos R, Greshock J, Liang S, Huang J, Hasegawa K, Li C, O'Brien-Jenkins A, Katsaros D, Weber BL, Simon C, Coukos G, Zhang L. miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer. Cancer Biol Ther 2008;7:255-264 [PMID: 18059191]
14. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, Davuluri R, Liu CG, Croce CM, Negrini M, Calin GA, Ivan M. A microRNA signature of hypoxia. Mol Cell Biol 2007;27:1859-1867 [PMID: 17194750]
15. Pulkkinen K, Malm T, Turunen M, Koistinaho J, Ylä-Herttuala S. Hypoxia induces microRNA miR-210 in vitro and in vivo ephrin-A3 and neuronal pentraxin 1 are potentially regulated by miR-210. FEBS Lett 2008;582:2397-2401 [PMID: 18539147 DOI: 10.1016/j.febslet.2008.05.048]
16. Fasanaro P, D'Alessandra Y, Di Stefano V, Melchionna R, Romani S, Pompilio G, Capogrossi MC, Martelli F. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 2008;283:15878-15883 [PMID: 18417479 DOI: 10.1074/jbc. M800731200]
17. Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB, Zhang Y. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One 2006;1:e116 [PMID: 17205120]
18. Crosby ME, Kulshreshtha R, Ivan M, Glazer PM. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res 2009;69:1221-1229 [PMID: 19141645 DOI: 10.1158/0008-5472. CAN-08-2516]
19. Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J. MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab 2009;10:273-284 [PMID: 19808020 DOI: 10.1016/j.cmet.2009.08.015]
20. Fasanaro P, Greco S, Lorenzi M, Pescatori M, Brioschi M, Kulshreshtha R, Banfi C, Stubbs A, Calin GA, Ivan M, Capogrossi MC, Martelli F. An integrated approach for experimental target identification of hypoxia-induced miR-210. J Biol Chem 2009;284:35134-35143 [PMID: 19826008 DOI: 10.1074/jbc. M109.052779]
21. Favaro E, Ramachandran A, McCormick R, Gee H, Blancher C, Crosby M, Devlin C, Blick C, Buffa F, Li JL, Vojnovic B, Pires Das Neves R, Glazer P, Iborra F, Ivan M, Ragoussis J, Harris AL. MicroRNA-210 regulates mitochondrial free radical response to hypoxia and krebs cycle in cancer cells by targeting iron sulfur cluster protein ISCU. PLoS One 2010;5:e10345 [PMID: 20436681 DOI: 10.1371/journal.pone.0010345]
22. Chen Z, Li Y, Zhang H, Huang P, Luthra R. Hypoxia-regulated microRNA-210 modulates mitochondrial function and decreases ISCU and COX10 expression. Oncogene 2010;29:4362-4368 [PMID: 20498629 DOI: 10.1038/onc.2010.193]
23. Puisségur MP, Mazure NM, Bertero T, Pradelli L, Grosso S, Robbe-Sermesant K, Maurin T, Lebrigand K, Cardinaud B, Hofman V, Fourre S, Magnone V, Ricci JE, Pouysségur J, Gounon P, Hofman P, Barbry P, Mari B. miR-210 is overexpressed in late stages of lung cancer and mediates mitochondrial alterations associated with modulation of HIF-1 activity. Cell Death Differ 2011;18:465-478 [PMID: 20885442 DOI: 10.1038/cdd.2010.119]
24. Kim HW, Haider HK, Jiang S, Ashraf M. Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J Biol Chem 2009;284:33161-33168 [PMID: 19721136 DOI: 10.1074/jbc. M109.020925]
25. Yang W, Sun T, Cao J, Liu F, Tian Y, Zhu W. Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res 2012;318:944-954 [PMID: 22387901 DOI: 10.1016/j.yexcr.2012.02.010]
26. He J, Wu J, Xu N, Xie W, Li M, Li J, Jiang Y, Yang BB, Zhang Y. MiR-210 disturbs mitotic progression through regulating a group of mitosis-related genes. Nucleic Acids Res 2013;41:498-508 [PMID: 23125370 DOI: 10.1093/nar/gks995]
27. Biswas S, Roy S, Banerjee J, Hussain SR, Khanna S, Meenakshisundaram G, Kuppusamy P, Friedman A, Sen CK. Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds. Proc Natl Acad Sci USA 2010;107:6976-6981 [PMID: 20308562 DOI: 10.1073/pnas.1001653107]
28. Tsuchiya S, Fujiwara T, Sato F, Shimada Y, Tanaka E, Sakai Y, Shimizu K, Tsujimoto G. MicroRNA-210 regulates cancer cell proliferation through targeting fibroblast growth factor receptorlike 1 (FGFRL1). J Biol Chem 2011;286:420-428 [PMID: 21044961 DOI: 10.1074/jbc. M110.170852]
29. Zhang Z, Sun H, Dai H, Walsh RM, Imakura M, Schelter J, Burchard J, Dai X, Chang AN, Diaz RL, Marszalek JR, Bartz SR, Carleton M, Cleary MA, Linsley PS, Grandori C. MicroRNA miR-210 modulates cellular response to hypoxia through the MYC antagonist MNT. Cell Cycle 2009;8:2756-2768 [PMID: 19652553]
30. Devlin C, Greco S, Martelli F, Ivan M. miR-210: More than a silent player in hypoxia. IUBMB Life 2011;63:94-100 [PMID: 21360638 DOI: 10.1002/iub.427]
31. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Ménard S, Palazzo JP, Rosenberg A, Musiani P, Volinia S, Nenci I, Calin GA, Querzoli P, Negrini M, Croce CM. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005;65:7065-7070 [PMID: 16103053]
32. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006;103:2257-2261 [PMID: 16461460]
33. Foekens JA, Sieuwerts AM, Smid M, Look MP, De Weerd V, Boersma AW, Klijn JG, Wiemer EA, Martens JW. Four miRNAs associated with aggressiveness of lymph node-negative, estrogen receptorpositive human breast cancer. Proc Natl Acad Sci USA 2008;105:13021-13026 [PMID: 18755890 DOI: 10.1073/pnas.0803304105]
34. Zhang L, Huang J, Yang N, Greshock J, Megraw MS, Giannakakis A, Liang S, Naylor TL, Barchetti A, Ward MR, Yao G, Medina A, O'brien-Jenkins A, Katsaros D, Hatzigeorgiou A, Gimotty PA, Weber BL, Coukos G. microRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci USA 2006;103:9136-9141 [PMID: 16754881]
35. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007;133:647-658 [PMID: 17681183]
36. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y, Zhuang SM. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 2009;69:1135-1142 [PMID: 19155302 DOI: 10.1158/0008-5472. CAN-08-2886]
37. Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, Mazzaferro V, Lowe SW, Croce CM, Dejean A. miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA 2010;107:264-269 [PMID: 20018759 DOI: 10.1073/pnas.0907904107]
38. Li Y, Tan W, Neo TW, Aung MO, Wasser S, Lim SG, Tan TM. Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci 2009;100:1234-1242 [PMID: 19486339 DOI: 10.1111/j.1349-7006.2009.01164.x]
39. 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 [PMID: 11846609]
40. miRBase. Available from: URL: http://microrna.sanger.ac.uk/targets/v4
41. microRNA.org. Available from: URL: http://cbio.mskcc.org/microrna-previous
42. Maiorano D, Cuvier O, Danis E, Méchali M. MCM8 is an MCM2-7-related protein that functions as a DNA helicase during replication elongation and not initiation. Cell 2005;120:315-328 [PMID: 15707891]
43. Clump DA, Qazi IH, Sudol M, Flynn DC. c-Yes response to growth factor activation. Growth Factors 2005;23:263-272 [PMID: 16338789]
44. Summy JM, Sudol M, Eck MJ, Monteiro AN, Gatesman A, Flynn DC. Specificity in signaling by c-Yes. Front Biosci 2003;8:s185-s205 [PMID: 12456296]
45. Park J, Cartwright CA. Src activity increases and Yes activity decreases during mitosis of human colon carcinoma cells. Mol Cell Biol 1995;15:2374-2382 [PMID: 7739521]
46. Kuga T, Nakayama Y, Hoshino M, Higashiyama Y, Obata Y, Matsuda D, Kasahara K, Fukumoto Y, Yamaguchi N. Differential mitotic activation of endogenous c-Src, c-Yes, and Lyn in HeLa cells. Arch Biochem Biophys 2007;466:116-124 [PMID: 17692281]
47. Yoshida M, Kawai S, Toyoshima K. Unifected avian cells contain structurally unrelated progenitors of viral sarcoma genes. Nature 1980;287:653-654 [PMID: 6253807]
48. Sukegawa J, Semba K, Yamanashi Y, Nishizawa M, Miyajima N, Yamamoto T, Toyoshima K. Characterization of cDNA clones for the human c-yes gene. Mol Cell Biol 1987;7:41-47 [PMID: 2436037]
49. Sudol M, Hanafusa H. Cellular proteins homologous to the viral yes gene product. Mol Cell Biol 1986;6:2839-2846 [PMID: 3491292]
50. Werdich XQ, Penn JS. Src, Fyn and Yes play differential roles in VEGF-mediated endothelial cell events. Angiogenesis 2005;8:315-326 [PMID: 16400523]
51. Twamley-Stein GM, Pepperkok R, Ansorge W, Courtneidge SA. The Src family tyrosine kinases are required for platelet-derived growth factor-mediated signal transduction in NIH 3T3 cells. Proc Natl Acad Sci USA 1993;90:7696-7700 [PMID: 8356071]
52. Sato A, Sekine M, Virgona N, Ota M, Yano T. Yes is a central mediator of cell growth in malignant mesothelioma cells. Oncol Rep 2012;28:1889-1893 [PMID: 22948717 DOI: 10.3892/or.2012.2010]
53. Zhang GL, Li YX, Zheng SQ, Liu M, Li X, Tang H. Suppression of hepatitis B virus replication by microRNA-199a-3p and microRNA-210. Antiviral Res 2010;88:169-175 [PMID: 20728471 DOI: 10.1016/j.antiviral.2010.08.008]
54. Nonomura T, Masaki T, Morishita A, Jian G, Uchida N, Himoto T, Izuishi K, Iwama H, Yoshiji H, Watanabe S, Kurokohchi K, Kuriyama S. Identification of c-Yes expression in the nuclei of hepatocellular carcinoma cells: involvement in the early stages of hepatocarcinogenesis. Int J Oncol 2007;30:105-111 [PMID: 17143518]
55. Feng H, Masaki T, Nonomura T, Morishita A, Jian G, Nakai S, Deguchi A, Uchida N, Himoto T, Iwama H, Usuki H, Wakabayashi H, Izuishi K, Yoshiji H, Kurokohchi K, Kuriyama S. Activation of c-Yes in hepatocellular carcinoma: a preliminary study. World J Gastroenterol 2006;12:5743-5745 [PMID: 17007035 DOI: 10.3748/wjg.v12.i35.5733]
56. Ying Q, Liang L, Guo W, Zha R, Tian Q, Huang S, Yao J, Ding J, Bao M, Ge C, Yao M, Li J, He X. Hypoxia-inducible microRNA-210 augments the metastatic potential of tumor cells by targeting vacuole membrane protein 1 in hepatocellular carcinoma. Hepatology 2011;54:2064-2075 [PMID: 22144109 DOI: 10.1002/hep. 24614]