MicroRNA-101 inhibits human hepatocellular carcinoma progression through EZH2 downregulation and increased cytostatic drug sensitivity

Journal of Hepatology

Volumn 60, Issue 3, 2014, Pages 590-598

  Xu, Leibo ^a,b,c   Beckebaum, Susanne ^a,b   Iacob, Speranta ^a,d   Wu, Gang ^a,b   Kaiser, Gernot M ^b   Radtke, Arnold ^a,b   Liu, Chao ^c   Kabar, Iyad ^a   Schmidt, Hartmut H ^a   Zhang, Xiaoyong ^b,e   Lu, Mengji ^b   Cicinnati, Vito R ^a,b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

^c SUN YAT SEN MEMORIAL HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^d FUNDENI CLINICAL INSTITUTE   (Romania)

^e FIRST MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Autophagy; HCC; microRNA; Target gene

Indexed keywords

EZH2 PROTEIN, HUMAN; MICRORNA; MIRN101 MICRORNA, HUMAN; POLYCOMB REPRESSIVE COMPLEX 2;

ANIMAL; APOPTOSIS; AUTOPHAGY; BAGG ALBINO MOUSE; CARCINOMA, HEPATOCELLULAR; DISEASE COURSE; DOWN REGULATION; FEMALE; GENETICS; HEPG2 CELL LINE; HUMAN; LIVER NEOPLASMS; PATHOLOGY; PHYSIOLOGY; TUMOR INVASION;

ANIMALS; APOPTOSIS; AUTOPHAGY; CARCINOMA, HEPATOCELLULAR; DISEASE PROGRESSION; DOWN-REGULATION; FEMALE; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MICE, INBRED BALB C; MICRORNAS; NEOPLASM INVASIVENESS; POLYCOMB REPRESSIVE COMPLEX 2;

EID: 84894038116     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2013.10.028     Document Type: Article

References (33)

1. J. Ferlay, H.R. Shin, F. Bray, D. Forman, C. Mathers, and D.M. Parkin Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008 Int J Cancer 127 2010 2893 2917
2. E.P. Simard, E.M. Ward, R. Siegel, and A. Jemal Cancers with increasing incidence trends in the United States: 1999 through 2008 CA Cancer J Clin 62 2012 118 128
3. J.M. Llovet, S. Ricci, V. Mazzaferro, P. Hilgard, E. Gane, and J.F. Blanc et al. Sorafenib in advanced hepatocellular carcinoma N Engl J Med 359 2008 378 390
4. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
5. M.V. Iorio, and C.M. Croce MicroRNA involvement in human cancer Carcinogenesis 33 2012 1126 1133
6. J. Hou, L. Lin, W. Zhou, Z. Wang, G. Ding, and Q. Dong et al. Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma Cancer Cell 19 2011 232 243
7. J.G. Zhang, J.F. Guo, D.L. Liu, Q. Liu, and J.J. Wang MicroRNA-101 exerts tumor-suppressive functions in non-small cell lung cancer through directly targeting enhancer of zeste homolog 2 J Thorac Oncol 6 2011 671 678
8. H. Su, J.R. Yang, T. Xu, J. Huang, L. Xu, and Y. Yuan et al. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity Cancer Res 69 2009 1135 1142
9. M.E. Valk-Lingbeek, S.W. Bruggeman, and M. van Lohuizen Stem cells and cancer; the polycomb connection Cell 118 2004 409 418
10. T. Mahmoudi, and C.P. Verrijzer Chromatin silencing and activation by Polycomb and trithorax group proteins Oncogene 20 2001 3055 3066
11. S. Varambally, S.M. Dhanasekaran, M. Zhou, T.R. Barrette, C. Kumar-Sinha, and M.G. Sanda et al. The polycomb group protein EZH2 is involved in progression of prostate cancer Nature 419 2002 624 629
12. Y. Matsukawa, S. Semba, H. Kato, A. Ito, K. Yanagihara, and H. Yokozaki Expression of the enhancer of zeste homolog 2 is correlated with poor prognosis in human gastric cancer Cancer Sci 97 2006 484 491
13. J.D. Raman, N.P. Mongan, S.K. Tickoo, S.A. Boorjian, D.S. Scherr, and L.J. Gudas Increased expression of the polycomb group gene, EZH2, in transitional cell carcinoma of the bladder Clin Cancer Res 11 2005 8570 8576
14. C.G. Kleer, Q. Cao, S. Varambally, R. Shen, I. Ota, and S.A. Tomlins et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells Proc Natl Acad Sci U S A 100 2003 11606 11611
15. T. Sudo, T. Utsunomiya, K. Mimori, H. Nagahara, K. Ogawa, and H. Inoue et al. Clinicopathological significance of EZH2 mRNA expression in patients with hepatocellular carcinoma Br J Cancer 92 2005 1754 1758
16. M. Sasaki, H. Ikeda, K. Itatsu, J. Yamaguchi, S. Sawada, and H. Minato et al. The overexpression of polycomb group proteins Bmi1 and EZH2 is associated with the progression and aggressive biological behavior of hepatocellular carcinoma Lab Invest 88 2008 873 882
17. M.Y. Cai, J.H. Hou, H.L. Rao, R.Z. Luo, M. Li, and X.Q. Pei et al. High expression of H3K27me3 in human hepatocellular carcinomas correlates closely with vascular invasion and predicts worse prognosis in patients Mol Med 17 2011 12 20
18. M.Y. Cai, Z.T. Tong, F. Zheng, Y.J. Liao, Y. Wang, and H.L. Rao et al. EZH2 protein: a promising immunomarker for the detection of hepatocellular carcinomas in liver needle biopsies Gut 60 2011 967 976
19. S. Varambally, Q. Cao, R.S. Mani, S. Shankar, X. Wang, and B. Ateeq et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer Science 322 2008 1695 1699
20. J.M. Friedman, G. Liang, C.C. Liu, E.M. Wolff, Y.C. Tsai, and W. Ye et al. The putative tumor suppressor microRNA-101 modulates the cancer epigenome by repressing the polycomb group protein EZH2 Cancer Res 69 2009 2623 2629
21. S.J. Cherra, S.M. Kulich, G. Uechi, M. Balasubramani, J. Mountzouris, and B.W. Day et al. Regulation of the autophagy protein LC3 by phosphorylation J Cell Biol 190 2010 533 539
22. F. Jimenez, S. Aiba-Masago, I. Al Hashimi, N. Vela-Roch, G. Fernandes, and C.K. Yeh et al. Activated caspase 3 and cleaved poly(ADP-ribose)polymerase in salivary epithelium suggest a pathogenetic mechanism for Sjögren's syndrome Rheumatology (Oxford) 41 2002 338 342
23. S.L. Au, C.C. Wong, J.M. Lee, D.N. Fan, F.H. Tsang, and I.O. Ng et al. Enhancer of zeste homolog 2 epigenetically silences multiple tumor suppressor microRNAs to promote liver cancer metastasis Hepatology 56 2012 622 631
24. L. Wang, X. Zhang, L.T. Jia, S.J. Hu, J. Zhao, and J.D. Yang et al. c-Myc-mediated epigenetic silencing of microRNA-101 contributes to dysregulation of multiple pathways in hepatocellular carcinoma Hepatology 2013 10.1002/hep.26720 [Epub ahead of print]
25. M. Garofalo, G. Romano, G. Di Leva, G. Nuovo, Y.J. Jeon, and A. Ngankeu et al. EGFR and MET receptor tyrosine kinase-altered microRNA expression induces tumorigenesis and gefitinib resistance in lung cancers Nat Med 18 2012 74 82
26. A. Kuma, M. Hatano, M. Matsui, A. Yamamoto, H. Nakaya, and T. Yoshimori et al. The role of autophagy during the early neonatal starvation period Nature 432 2004 1032 1036
27. Y. Chang, W. Yan, X. He, L. Zhang, C. Li, and H. Huang et al. MiR-375 inhibits autophagy and reduces viability of hepatocellular carcinoma cells under hypoxic conditions Gastroenterology 143 2012 e178
28. L. English, M. Chemali, and M. Desjardins Nuclear membrane-derived autophagy, a novel process that participates in the presentation of endogenous viral antigens during HSV-1 infection Autophagy 5 2009 1026 1029
29. M. Jiang, W.G. Jerome, and S.W. Hayward Autophagy in nuclear receptor PPARgamma-deficient mouse prostatic carcinogenesis Autophagy 6 2010 175 176
30. R. Mathew, S. Kongara, B. Beaudoin, C.M. Karp, K. Bray, and K. Degenhardt et al. Autophagy suppresses tumor progression by limiting chromosomal instability Genes Dev 21 2007 1367 1381
31. N. Chen, and V. Karantza Autophagy as a therapeutic target in cancer Cancer Biol Ther 11 2011 157 168
32. J. Xiao, X. Zhu, B. He, Y. Zhang, B. Kang, and Z. Wang et al. MiR-204 regulates cardiomyocyte autophagy induced by ischemia-reperfusion through LC3-II J Biomed Sci 18 2011 35
33. L.B. Frankel, J. Wen, M. Lees, M. Høyer-Hansen, T. Farkas, and A. Krogh et al. MicroRNA-101 is a potent inhibitor of autophagy EMBO J 30 2011 4628 4641