Function and clinical potential of microRNAs in hepatocellular carcinoma (Review)
- Authors:
- Lijuan Wang
- Yongfang Yue
- Xian Wang
- Hongchuan Jin
-
Affiliations: Department of Hematology, Hematology Laboratory, Linyi People's Hospital, Shandong University, Linyi, Shandong 276003, P.R. China, Department of Medical Oncology, Institute of Clinical Science, Sir Run Run Shaw Hospital, Medical School of Zhejiang University, Hangzhou, Zhejiang 310000, P.R. China - Published online on: September 29, 2015 https://doi.org/10.3892/ol.2015.3759
- Pages: 3345-3353
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Abstract
Forner A, Llovet JM and Bruix J: Hepatocellular carcinoma. Lancet. 379:1245–1255. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lai EC and Lau WY: The continuing challenge of hepatic cancer in Asia. Surgeon. 3:210–215. 2005. View Article : Google Scholar : PubMed/NCBI | |
Sotillo E and Thomas-Tikhonenko A: Shielding the messenger (RNA): microRNA-based anticancer therapies. Pharmacol Ther. 131:18–32. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI | |
Friedman RC, Farh KK, Burge CB and Bartel DP: Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19:92–105. 2009. View Article : Google Scholar : PubMed/NCBI | |
Li Y and Kowdley KV: Cellular microRNA and the tumorigenesis of hepatocellular carcinoma. Ann Hepatol. 11:272–274. 2012.PubMed/NCBI | |
Pauli A, Rinn JL and Schier AF: Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet. 12:136–149. 2011. View Article : Google Scholar : PubMed/NCBI | |
Poy MN, Eliasson L, Krutzfeldt J, et al: A pancreatic islet-specific microRNA regulates insulin secretion. Nature. 432:226–230. 2004. View Article : Google Scholar : PubMed/NCBI | |
Chen CZ: MicroRNAs as oncogenes and tumor suppressors. N Engl J Med. 353:1768–1771. 2005. View Article : Google Scholar : PubMed/NCBI | |
Esquela-Kerscher A and Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006. View Article : Google Scholar : PubMed/NCBI | |
Hammond SM: MicroRNAs as tumor suppressors. Nat Genet. 39:582–583. 2007. View Article : Google Scholar : PubMed/NCBI | |
Iorio MV and Croce CM: MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med. 4:143–159. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lee RC, Feinbaum RL and Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75:843–854. 1993. View Article : Google Scholar : PubMed/NCBI | |
Reinhart BJ, Slack FJ, Basson M, et al: The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 403:901–906. 2000. View Article : Google Scholar : PubMed/NCBI | |
Fabian MR and Sonenberg N: The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol. 19:586–593. 2012. View Article : Google Scholar : PubMed/NCBI | |
Filipowicz W, Bhattacharyya SN and Sonenberg N: Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 9:102–114. 2008. View Article : Google Scholar : PubMed/NCBI | |
Rinn JL and Chang HY: Genome regulation by long noncoding RNAs. Annu Rev Biochem. 81:145–166. 2012. View Article : Google Scholar : PubMed/NCBI | |
Garzon R, Calin GA and Croce CM: MicroRNAs in cancer. Annu Rev Med. 60:167–179. 2009. View Article : Google Scholar : PubMed/NCBI | |
Borchert GM, Lanier W and Davidson BL: RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol. 13:1097–1101. 2006. View Article : Google Scholar : PubMed/NCBI | |
Cai X, Hagedorn CH and Cullen BR: Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA. 10:1957–1966. 2004. View Article : Google Scholar : PubMed/NCBI | |
Lee Y, Kim M, Han J, et al: MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23:4051–4060. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kim VN, Han J and Siomi MC: Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 10:126–139. 2009. View Article : Google Scholar : PubMed/NCBI | |
Berezikov E, Chung WJ, Willis J, Cuppen E and Lai EC: Mammalian mirtron genes. Mol Cell. 28:328–336. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lee Y, Ahn C, Han J, et al: The nuclear RNase III Drosha initiates microRNA processing. Nature. 425:415–419. 2003. View Article : Google Scholar : PubMed/NCBI | |
Ruby JG, Jan CH and Bartel DP: Intronic microRNA precursors that bypass Drosha processing. Nature. 448:83–86. 2007. View Article : Google Scholar : PubMed/NCBI | |
Berezikov E, Guryev V and Cuppen E: Exploring conservation of transcription factor binding sites with CONREAL. Methods Mol Biol. 395:437–448. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hinton A, Afrikanova I, Wilson M, et al: A distinct microRNA signature for definitive endoderm derived from human embryonic stem cells. Stem Cells Dev. 19:797–807. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kim Y and Kim VN: MicroRNA factory: RISC assembly from precursor microRNAs. Mol Cell. 46:384–386. 2012. View Article : Google Scholar : PubMed/NCBI | |
Si-Tayeb K, Lemaigre FP and Duncan SA: Organogenesis and development of the liver. Dev Cell. 18:175–189. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chen Y and Verfaillie CM: MicroRNAs: the fine modulators of liver development and function. Liver Int. 34:976–990. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fu S, Fei Q, Jiang H, et al: Involvement of histone acetylation of Sox17 and Foxa2 promoters during mouse definitive endoderm differentiation revealed by microRNA profiling. PLoS One. 6:e279652011. View Article : Google Scholar : PubMed/NCBI | |
Kim N, Kim H, Jung I, Kim Y, Kim D and Han YM: Expression profiles of miRNAs in human embryonic stem cells during hepatocyte differentiation. Hepatol Res. 41:170–183. 2011. View Article : Google Scholar : PubMed/NCBI | |
Laudadio I, Manfroid I, Achouri Y, et al: A feedback loop between the liver-enriched transcription factor network and miR-122 controls hepatocyte differentiation. Gastroenterology. 142:119–129. 2012. View Article : Google Scholar : PubMed/NCBI | |
Xu H, He JH, Xiao ZD, et al: Liver-enriched transcription factors regulate microRNA-122 that targets CUTL1 during liver development. Hepatology. 52:1431–1442. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gailhouste L, Gomez-Santos L, Hagiwara K, et al: miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology. 58:1153–1165. 2013. View Article : Google Scholar : PubMed/NCBI | |
Allen RM, Marquart TJ, Albert CJ, et al: miR-33 controls the expression of biliary transporters, and mediates statin- and diet-induced hepatotoxicity. EMBO Mol Med. 4:882–895. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hand NJ, Master ZR, Le Lay J and Friedman JR: Hepatic function is preserved in the absence of mature microRNAs. Hepatology. 49:618–626. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yang YM, Seo SY, Kim TH and Kim SG: Decrease of microRNA-122 causes hepatic insulin resistance by inducing protein tyrosine phosphatase 1B, which is reversed by licorice flavonoid. Hepatology. 56:2209–2220. 2012. View Article : Google Scholar : PubMed/NCBI | |
Rieger JK, Klein K, Winter S and Zanger UM: Expression variability of absorption, distribution, metabolism, excretion-related microRNAs in human liver: influence of nongenetic factors and association with gene expression. Drug Metab Dispos. 41:1752–1762. 2013. View Article : Google Scholar : PubMed/NCBI | |
Chai ZT, Kong J, Zhu XD, Zhang YY, Lu L, Zhou JM, Wang LR, Zhang KZ, Zhang QB, Ao JY, et al: MicroRNA-26a inhibits angiogenesis by down-regulating VEGFA through the PIK3C2α/Akt/HIF-1α pathway in hepatocellular carcinoma. PLoS One. 8:e779572013. View Article : Google Scholar : PubMed/NCBI | |
Yang H, Cho ME, Li TW, Peng H, Ko KS, Mato JM and Lu SC: MicroRNAs regulate methionine adenosyltransferase 1A expression in hepatocellular carcinoma. J Clin Invest. 123:285–98. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Yang P and Wang XF: Microenvironmental regulation of cancer metastasis by miRNAs. Trends Cell Biol. 24:153–60. 2014. View Article : Google Scholar : PubMed/NCBI | |
Huang S and He X: The role of microRNAs in liver cancer progression. Br J Cancer. 104:235–240. 2011. View Article : Google Scholar : PubMed/NCBI | |
El-Serag HB and Rudolph KL: Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 132:2557–2576. 2007. View Article : Google Scholar : PubMed/NCBI | |
Coussens LM and Werb Z: Inflammation and cancer. Nature. 420:860–867. 2002. View Article : Google Scholar : PubMed/NCBI | |
Park EJ, Lee JH, Yu GY, et al: Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell. 140:197–208. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hatziapostolou M, Polytarchou C, Aggelidou E, et al: An HNF4α-miRNA inflammatory feedback circuit regulates hepatocellular oncogenesis. Cell. 147:1233–1247. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ma S, Chan KW, Hu L, et al: Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 132:2542–2556. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ma S, Lee TK, Zheng BJ, Chan KW and Guan XY: CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene. 27:1749–1758. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Yu Y, Tsuyada A, et al: Transforming growth factor-β regulates the sphere-initiating stem cell-like feature in breast cancer through miRNA-181 and ATM. Oncogene. 30:1470–1480. 2011. View Article : Google Scholar : PubMed/NCBI | |
Gupta PB, Onder TT, Jiang G, et al: Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 138:645–659. 2009. View Article : Google Scholar : PubMed/NCBI | |
Morrison R, Schleicher SM, Sun Y, et al: Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J Oncol. 2011:9418762011. View Article : Google Scholar : PubMed/NCBI | |
Pardal R, Clarke MF and Morrison SJ: Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 3:895–902. 2003. View Article : Google Scholar : PubMed/NCBI | |
Oishi N and Wang XW: Novel therapeutic strategies for targeting liver cancer stem cells. Int J Biol Sci. 7:517–535. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ji J, Yamashita T, Budhu A, et al: Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology. 50:472–480. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kota J, Chivukula RR, O'Donnell KA, et al: Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell. 137:1005–1017. 2009. View Article : Google Scholar : PubMed/NCBI | |
Gramantieri L, Ferracin M, Fornari F, et al: Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res. 67:6092–6099. 2007. View Article : Google Scholar : PubMed/NCBI | |
Fornari F, Gramantieri L, Giovannini C, et al: MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res. 69:5761–5767. 2009. View Article : Google Scholar : PubMed/NCBI | |
Furuta M, Kozaki KI, Tanaka S, Arii S, Imoto I and Inazawa J: miR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis. 31:766–776. 2010. View Article : Google Scholar : PubMed/NCBI | |
Shimizu S, Takehara T, Hikita H, et al: The let-7 family of microRNAs inhibits Bcl-xL expression and potentiates sorafenib-induced apoptosis in human hepatocellular carcinoma. J Hepatol. 52:698–704. 2010. View Article : Google Scholar : PubMed/NCBI | |
Xiong Y, Fang JH, Yun JP, et al: Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology. 51:836–845. 2010.PubMed/NCBI | |
Gramantieri L, Fornari F, Ferracin M, et al: MicroRNA-221 targets Bmf in hepatocellular carcinoma and correlates with tumor multifocality. Clin Cancer Res. 15:5073–5081. 2009. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Tan W, Neo TW, et al: Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci. 100:1234–1242. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yang L, Ma Z, Wang D, Zhao W, Chen L and Wang G: MicroRNA-602 regulating tumor suppressive gene RASSF1A is overexpressed in hepatitis B virus-infected liver and hepatocellular carcinoma. Cancer Biol Ther. 9:803–808. 2010. View Article : Google Scholar : PubMed/NCBI | |
Garofalo M, Di Leva G, Romano G, et al: miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell. 16:498–509. 2009. View Article : Google Scholar : PubMed/NCBI | |
Gramantieri L, Fornari F, Callegari E, et al: MicroRNA involvement in hepatocellular carcinoma. J Cell Mol Med. 12:2189–2204. 2008. View Article : Google Scholar : PubMed/NCBI | |
Coulouarn C, Factor VM, Andersen JB, Durkin ME and Thorgeirsson SS: Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene. 28:3526–3536. 2009. View Article : Google Scholar : PubMed/NCBI | |
Li N, Fu H, Tie Y, et al: miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett. 275:44–53. 2009. View Article : Google Scholar : PubMed/NCBI | |
Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST and Patel T: MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 133:647–658. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lin SL, Miller JD and Ying SY: Intronic microRNA (miRNA). J Biomed Biotechnol. 2006:268182006. View Article : Google Scholar : PubMed/NCBI | |
Li Q, Ding C, Chen C, et al: miR-224 promotes cell migration and invasion by targeting Homeobox D 10 gene in human hepatocellular carcinoma. J Gastroenterol Hepatol. 29:835–842. 2014. View Article : Google Scholar : PubMed/NCBI | |
Varnholt H, Drebber U, Schulze F, et al: MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology. 47:1223–1232. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ladeiro Y, Couchy G, Balabaud C, et al: MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology. 47:1955–1963. 2008. View Article : Google Scholar : PubMed/NCBI | |
Yang F, Yin Y, Wang F, et al: miR-17-5p Promotes migration of human hepatocellular carcinoma cells through the p38 mitogen-activated protein kinase-heat shock protein 27 pathway. Hepatology. 51:1614–1623. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ding J, Huang S, Wu S, et al: Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat Cell Biol. 12:390–399. 2010. View Article : Google Scholar : PubMed/NCBI | |
Yao J, Liang L, Huang S, et al: MicroRNA-30d promotes tumor invasion and metastasis by targeting Galphai2 in hepatocellular carcinoma. Hepatology. 51:846–856. 2010.PubMed/NCBI | |
Sato M, Tateishi R, Yasunaga H, et al: Mortality and morbidity of hepatectomy, radiofrequency ablation, and embolization for hepatocellular carcinoma: a national survey of 54,145 patients. J Gastroenterol. 47:1125–1133. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ray K: Liver cancer: The promise of new approaches in the management of hepatocellular carcinoma - adding to the toolbox? Nat Rev Gastroenterol Hepatol. 10:1952013. View Article : Google Scholar : PubMed/NCBI | |
Qu KZ, Zhang K, Li H, Afdhal NH and Albitar M: Circulating microRNAs as biomarkers for hepatocellular carcinoma. J Clin Gastroenterol. 45:355–360. 2011. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Ba Y, Ma L, et al: Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 18:997–1006. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ji F, Yang B, Peng X, Ding H, You H and Tien P: Circulating microRNAs in hepatitis B virus-infected patients. J Viral Hepat. 18:e242–e251. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mitchell PS, Parkin RK, Kroh EM, et al: Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 105:10513–10518. 2008. View Article : Google Scholar : PubMed/NCBI | |
Li LM, Hu ZB, Zhou ZX, et al: Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res. 70:9798–9807. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhou J, Yu L, Gao X, et al: Plasma microRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma. J Clin Oncol. 29:4781–4788. 2011. View Article : Google Scholar : PubMed/NCBI | |
Niu D, Feng H and Chen WN: Proteomic analysis of HBV-associated HCC: insights on mechanisms of disease onset and biomarker discovery. J Proteomics. 73:1283–1290. 2010. View Article : Google Scholar : PubMed/NCBI | |
Aguirre-Gamboa R and Trevino V: SurvMicro: assessment of miRNA-based prognostic signatures for cancer clinical outcomes by multivariate survival analysis. Bioinformatics. 30:1630–1632. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zhu HT, Dong QZ, Sheng YY, et al: MicroRNA-29a-5p is a novel predictor for early recurrence of hepatitis B virus-related hepatocellular carcinoma after surgical resection. PLoS One. 7:e523932012. View Article : Google Scholar : PubMed/NCBI | |
Hoshida Y, Villanueva A, Kobayashi M, et al: Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med. 359:1995–2004. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sherman M: Recurrence of hepatocellular carcinoma. N Engl J Med. 359:2045–2047. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tomimaru Y, Eguchi H, Nagano H, et al: MicroRNA-21 induces resistance to the anti-tumour effect of interferon-α/5-fluorouracil in hepatocellular carcinoma cells. Br J Cancer. 103:1617–1626. 2010. View Article : Google Scholar : PubMed/NCBI | |
Pineau P, Volinia S, McJunkin K, et al: miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA. 107:264–269. 2010. View Article : Google Scholar : PubMed/NCBI | |
Xu Y, Xia F, Ma L, et al: MicroRNA-122 sensitizes HCC cancer cells to adriamycin and vincristine through modulating expression of MDR and inducing cell cycle arrest. Cancer Lett. 310:160–169. 2011.PubMed/NCBI | |
Ma K, He Y, Zhang H, et al: DNA methylation-regulated miR-193a-3p dictates resistance of hepatocellular carcinoma to 5-fluorouracil via repression of SRSF2 expression. J Biol Chem. 287:5639–5649. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tomokuni A, Eguchi H, Tomimaru Y, et al: miR-146a suppresses the sensitivity to interferon-α in hepatocellular carcinoma cells. Biochem Biophys Res Commun. 414:675–680. 2011. View Article : Google Scholar : PubMed/NCBI | |
Weidhaas JB, Babar I, Nallur SM, et al: MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Res. 67:11111–11116. 2007. View Article : Google Scholar : PubMed/NCBI | |
Mutharasan RK, Nagpal V, Ichikawa Y and Ardehali H: microRNA-210 is upregulated in hypoxic cardiomyocytes through Akt- and p53-dependent pathways and exerts cytoprotective effects. Am J Physiol Heart Circ Physiol. 301:H1519–1530. 2011. View Article : Google Scholar : PubMed/NCBI | |
Xie Q, Lin T, Zhang Y, Zheng J and Bonanno JA: Molecular cloning and characterization of a human AIF-like gene with ability to induce apoptosis. J Biol Chem. 280:19673–19681. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kumar MS, Erkeland SJ, Pester RE, et al: Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci USA. 105:3903–3908. 2008. View Article : Google Scholar : PubMed/NCBI | |
Choi WY, Giraldez AJ and Schier AF: Target protectors reveal dampening and balancing of Nodal agonist and antagonist by miR-430. Science. 318:271–274. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hatakeyama H, Murata M, Sato Y, et al: The systemic administration of an anti-miRNA oligonucleotide encapsulated pH-sensitive liposome results in reduced level of hepatic microRNA-122 in mice. J Controlled Release. 173:43–50. 2014. View Article : Google Scholar | |
El Tayebi HM, Hosny KA, Esmat G, Breuhahn K and Abdelaziz AI: miR-615-5p is restrictedly expressed in cirrhotic and cancerous liver tissues and its overexpression alleviates the tumorigenic effects in hepatocellular carcinoma. FEBS Lett. 586:3309–3316. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fornari F, Milazzo M, Chieco P, et al: In hepatocellular carcinoma miR-519d is up-regulated by p53 and DNA hypomethylation and targets CDKN1A/p21, PTEN, AKT3 and TIMP2. J Pathol. 227:275–285. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jiang X, Xiang G, Wang Y, et al: MicroRNA-590-5p regulates proliferation and invasion in human hepatocellular carcinoma cells by targeting TGF-β RII. Mol Cells. 33:545–551. 2012. View Article : Google Scholar : PubMed/NCBI | |
Liu WH, Yeh SH, Lu CC, et al: MicroRNA-18a prevents estrogen receptor-alpha expression, promoting proliferation of hepatocellular carcinoma cells. Gastroenterology. 136:683–693. 2009. View Article : Google Scholar : PubMed/NCBI | |
Notarbartolo M, Giannitrapani L, Vivona N, et al: Frequent alteration of the Yin Yang 1/Raf-1 kinase inhibitory protein ratio in hepatocellular carcinoma. OMOICS. 15:267–272. 2011. View Article : Google Scholar | |
Santhekadur PK, Das SK, Gredler R, et al: Multifunction protein staphylococcal nuclease domain containing 1 (SND1) promotes tumor angiogenesis in human hepatocellular carcinoma through novel pathway that involves nuclear factor κB and miR-221. J Biol Chem. 287:13952–13958. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yang W, Sun T, Cao J, Liu F, Tian Y and Zhu W: Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res. 318:944–954. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Wei W, Cheng N, et al: Hepatitis C virus-induced up-regulation of microRNA-155 promotes hepatocarcinogenesis by activating Wnt signaling. Hepatology. 56:1631–1640. 2012. View Article : Google Scholar : PubMed/NCBI | |
Au SL, Wong CC, Lee JM, et al: Enhancer of zeste homolog 2 epigenetically silences multiple tumor suppressor microRNAs to promote liver cancer metastasis. Hepatology. 56:622–631. 2012. View Article : Google Scholar : PubMed/NCBI | |
Buurman R, Gurlevik E, Schaffer V, et al: Histone deacetylases activate hepatocyte growth factor signaling by repressing microRNA-449 in hepatocellular carcinoma cells. Gastroenterol. 143:811–820. 2012. View Article : Google Scholar | |
Di Fazio P, Montalbano R, Neureiter D, et al: Downregulation of HMGA2 by the pan-deacetylase inhibitor panobinostat is dependent on hsa-let-7b expression in liver cancer cell lines. Exp Cell Res. 318:1832–1843. 2012. View Article : Google Scholar : PubMed/NCBI | |
Huang N, Lin J, Ruan J, et al: MiR-219-5p inhibits hepatocellular carcinoma cell proliferation by targeting glypican-3. FEBS Lett. 586:884–891. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lang Q and Ling C: MiR-124 suppresses cell proliferation in hepatocellular carcinoma by targeting PIK3CA. Biochem Biophys Res Commun. 426:247–252. 2012. View Article : Google Scholar : PubMed/NCBI | |
Li D, Yang P, Li H, et al: MicroRNA-1 inhibits proliferation of hepatocarcinoma cells by targeting endothelin-1. Life Sci. 91:440–447. 2012. View Article : Google Scholar : PubMed/NCBI | |
Shah YM, Morimura K, Yang Q, Tanabe T, Takagi M and Gonzalez FJ: Peroxisome proliferator-activated receptor alpha regulates a microRNA-mediated signaling cascade responsible for hepatocellular proliferation. Mol Cell Biol. 27:4238–4247. 2007. View Article : Google Scholar : PubMed/NCBI | |
Tsang WP and Kwok TT: Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis. 13:1215–1222. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Lin S, Li JJ, et al: MYC protein inhibits transcription of the microRNA cluster MC-let-7a-1~let-7d via noncanonical E-box. J Biol Chem. 286:39703–39714. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wei W, Wanjun L, Hui S, Dongyue C, Xinjun Y and Jisheng Z: miR-203 inhibits proliferation of HCC cells by targeting survivin. Cell Biochem Funct. 31:82–85. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wong QW, Lung RW, Law PT, et al: MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology. 135:257–269. 2008. View Article : Google Scholar : PubMed/NCBI | |
Yuan JH, Yang F, Chen BF, et al: The histone deacetylase 4/SP1/microrna-200a regulatory network contributes to aberrant histone acetylation in hepatocellular carcinoma. Hepatology. 54:2025–2035. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zheng Y, Yin L, Chen H, et al: miR-376a suppresses proliferation and induces apoptosis in hepatocellular carcinoma. FEBS Lett. 586:2396–2403. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhu XM, Wu LJ, Xu J, Yang R and Wu FS: Let-7c microRNA expression and clinical significance in hepatocellular carcinoma. J Int Med Res. 39:2323–2329. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Lee AT, Ma JZ, et al: Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis inhibitor-5 as a microRNA-224-specific target. J Biol Chem. 283:13205–13215. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Toh HC, Chow P, et al: MicroRNA-224 is up-regulated in hepatocellular carcinoma through epigenetic mechanisms. FASEB J. 26:3032–3041. 2012. View Article : Google Scholar : PubMed/NCBI | |
Alpini G, Glaser SS, Zhang JP, et al: Regulation of placenta growth factor by microRNA-125b in hepatocellular cancer. J Hepatol. 55:1339–1345. 2011. View Article : Google Scholar : PubMed/NCBI | |
Fan DN, Tsang FH, Tam AH, et al: Histone lysine methyltransferase, suppressor of variegation 3-9 homolog 1, promotes hepatocellular carcinoma progression and is negatively regulated by microRNA-125b. Hepatology. 57:637–647. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ji J, Zhao L, Budhu A, et al: Let-7g targets collagen type I alpha2 and inhibits cell migration in hepatocellular carcinoma. J Hepatol. 52:690–697. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lan FF, Wang H, Chen YC, et al: Hsa-let-7g inhibits proliferation of hepatocellular carcinoma cells by downregulation of c-Myc and upregulation of p16 (INK4A). Int J cancer. 128:319–331. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lin CJ, Gong HY, Tseng HC, Wang WL and Wu JL: miR-122 targets an anti-apoptotic gene, Bcl-w, in human hepatocellular carcinoma cell lines. Biochem Biophys Res Commun. 375:315–320. 2008. View Article : Google Scholar : PubMed/NCBI | |
Reddi HV, Madde P, Milosevic D, et al: The putative PAX8/PPARγ fusion oncoprotein exhibits partial tumor suppressor activity through up-regulation of micro-RNA-122 and dominant-negative PPARγ activity. Genes Cancer. 2:46–55. 2011. View Article : Google Scholar : PubMed/NCBI | |
Su H, Yang JR, Xu T, et al: MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res. 69:1135–1142. 2009. View Article : Google Scholar : PubMed/NCBI | |
Tsai WC, Hsu PW, Lai TC, et al: MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology. 49:1571–1582. 2009. View Article : Google Scholar : PubMed/NCBI | |
Xu J, Zhu X, Wu L, et al: MicroRNA-122 suppresses cell proliferation and induces cell apoptosis in hepatocellular carcinoma by directly targeting Wnt/β-catenin pathway. Liver Int. 32:752–760. 2012. View Article : Google Scholar : PubMed/NCBI | |
Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP and Zhuang SM: MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology. 50:113–121. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yang X, Yu J, Yin J, Xiang Q, Tang H and Lei X: MiR-195 regulates cell apoptosis of human hepatocellular carcinoma cells by targeting LATS2. Pharmazie. 67:645–651. 2012.PubMed/NCBI | |
Zhang Y, Guo X, Xiong L, et al: MicroRNA-101 suppresses SOX9-dependent tumorigenicity and promotes favorable prognosis of human hepatocellular carcinoma. FEBS Lett. 586:4362–4370. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhao A, Zeng Q, Xie X, et al: MicroRNA-125b induces cancer cell apoptosis through suppression of Bcl-2 expression. J Genet Genomics. 39:29–35. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wang W, Zhao LJ, Tan YX, Ren H and Qi ZT: MiR-138 induces cell cycle arrest by targeting cyclin D3 in hepatocellular carcinoma. Carcinogenesis. 33:1113–1120. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Wang J, Ma H, Zhang J and Zhou X: Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer. Med Oncol. 29:919–927. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wu N, Liu X, Xu X, et al: MicroRNA-373, a new regulator of protein phosphatase 6, functions as an oncogene in hepatocellular carcinoma. FEBS J. 278:2044–2054. 2011. View Article : Google Scholar : PubMed/NCBI | |
Odar K, Boštjančič E, Gale N, Glavač D and Zidar N: Differential expression of microRNAs miR-21, miR-31, miR-203, miR-125a-5p and miR-125b and proteins PTEN and p63 in verrucous carcinoma of the head and neck. Histopathology. 61:257–265. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fan Q, He M, Deng X, et al: Derepression of c-Fos caused by microRNA-139 down-regulation contributes to the metastasis of human hepatocellular carcinoma. Cell Biochem Funct. 31:319–324. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wong CC, Wong CM, Tung EK, et al: The microRNA miR-139 suppresses metastasis and progression of hepatocellular carcinoma by down-regulating Rho-kinase 2. Gastroenterology. 140:322–331. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Chen J, Li F, et al: miR-214 inhibits cell growth in hepatocellular carcinoma through suppression of β-catenin. Biochem Biophys Res Commun. 428:525–531. 2012. View Article : Google Scholar : PubMed/NCBI | |
Xia H, Ooi LL and Hui KM: miR-214 targets β-catenin pathway to suppress invasion, stem-like traits and recurrence of human hepatocellular carcinoma. PLoS One. 7:e442062012. View Article : Google Scholar : PubMed/NCBI | |
Fang Y, Xue JL, Shen Q, Chen J and Tian L: MicroRNA-7 inhibits tumor growth and metastasis by targeting the phosphoinositide 3-kinase/Akt pathway in hepatocellular carcinoma. Hepatology. 55:1852–1862. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yang P, Li QJ, Feng Y, et al: TGF-β-miR-34a-CCL22 signaling-induced Treg cell recruitment promotes venous metastases of HBV-positive hepatocellular carcinoma. Cancer Cell. 22:291–303. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jiang C, Pecha J, Hoshino I, Ankrapp D and Xiao H: TIP30 mutant derived from hepatocellular carcinoma specimens promotes growth of HepG2 cells through up-regulation of N-cadherin. Cancer Res. 67:3574–3582. 2007. View Article : Google Scholar : PubMed/NCBI | |
Tian Q, Liang L, Ding J, et al: MicroRNA-550a acts as a pro-metastatic gene and directly targets cytoplasmic polyadenylation element-binding protein 4 in hepatocellular carcinoma. PLoS One. 7:e489582012. View Article : Google Scholar : PubMed/NCBI | |
Zhou P, Jiang W, Wu L, Chang R, Wu K and Wang Z: miR-301a is a candidate oncogene that targets the homeobox gene Gax in human hepatocellular carcinoma. Dig Dis Sci. 57:1171–1180. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhu Q, Wang Z, Hu Y, et al: miR-21 promotes migration and invasion by the miR-21-PDCD4-AP-1 feedback loop in human hepatocellular carcinoma. Oncol Rep. 27:1660–1668. 2012.PubMed/NCBI | |
Li QJ, Zhou L, Yang F, et al: MicroRNA-10b promotes migration and invasion through CADM1 in human hepatocellular carcinoma cells. Tumour Biol. 33:1455–1465. 2012. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Guo W, Shi J, et al: MicroRNA-135a contributes to the development of portal vein tumor thrombus by promoting metastasis in hepatocellular carcinoma. J Hepatol. 56:389–396. 2012. View Article : Google Scholar : PubMed/NCBI | |
Long MJ, Wu FX, Li P, Liu M, Li X and Tang H: MicroRNA-10a targets CHL1 and promotes cell growth, migration and invasion in human cervical cancer cells. Cancer Lett. 324:186–196. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wang B, Hsu SH, Majumder S, et al: TGFbeta-mediated upregulation of hepatic miR-181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene. 29:1787–1797. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wang J, Li J, Shen J, Wang C, Yang L and Zhang X: MicroRNA-182 downregulates metastasis suppressor 1 and contributes to metastasis of hepatocellular carcinoma. BMC Cancer. 12:2272012. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Liu S, Hu T, Liu S, He Y and Sun S: Up-regulated microRNA-143 transcribed by nuclear factor kappa B enhances hepatocarcinoma metastasis by repressing fibronectin expression. Hepatology. 50:490–499. 2009. View Article : Google Scholar : PubMed/NCBI |