Review Article

Role of MicroRNA in the Diagnosis and Management of Hepatocellular Carcinoma

Author(s): Ioannis A. Ziogas, Georgios Sioutas, Konstantinos S. Mylonas and Georgios Tsoulfas*

Volume 9, Issue 1, 2020

Page: [25 - 40] Pages: 16

DOI: 10.2174/2211536608666190619155406

Abstract

Introduction: Hepatocellular Carcinoma (HCC) is one of the most common malignant tumors in the world and comes third in cancer-induced mortality. The need for improved and more specific diagnostic methods that can detect early-stage disease is immense, as it is amenable to curative modalities, while advanced HCC is associated with low survival rates. microRNA (miRNA) expression is deregulated in HCC and this can be implemented both diagnostically and therapeutically.

Objective: To provide a concise review on the role of miRNA in diagnosis, prognosis, and treatment of HCC.

Methods: We conducted a comprehensive review of the PubMed bibliographic database.

Results: Multiple miRNAs are involved in the pathogenesis of HCC. Measurement of the levels of these miRNAs either in tumor tissue or in the blood constitutes a promising diagnostic, as well as prognostic tool. OncomiRs are miRNAs that promote tumorigenesis, thus inhibiting them by administering antagomiRs is a promising treatment option. Moreover, replacement of the depleted miRNAs is another potential therapeutic approach for HCC. Modification of miRNA levels may also regulate sensitivity to chemotherapeutic agents.

Conclusion: miRNA play a pivotal role in HCC pathogenesis and once the underlying mechanisms are elucidated, they will become part of everyday clinical practice against HCC.

Keywords: Biomarkers, diagnosis, HCC, hepatocellular carcinoma, management, MicroRNA, prognosis, treatment.

Graphical Abstract
[1]
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015; 65(2): 87-108.
[http://dx.doi.org/10.3322/caac.21262] [PMID: 25651787]
[2]
Hayes CN, Chayama K. MicroRNAs as biomarkers for liver disease and hepatocellular carcinoma. Int J Mol Sci 2016; 17(3): 280.
[http://dx.doi.org/10.3390/ijms17030280] [PMID: 26927063]
[3]
Sanyal AJ, Yoon SK, Lencioni R. The etiology of hepatocellular carcinoma and consequences for treatment. Oncologist 2010; 15(Suppl. 4): 14-22.
[http://dx.doi.org/10.1634/theoncologist.2010-S4-14] [PMID: 21115577]
[4]
Akinyemiju T, Abera S, Ahmed M, et al. Global burden of disease liver cancer collaboration. The burden of primary liver cancer and underlying etiologies from 1990 to 2015 at the global, regional, and national level: results from the global burden of disease study 2015. JAMA Oncol 2017; 3(12): 1683-91.
[http://dx.doi.org/10.1001/jamaoncol.2017.3055] [PMID: 28983565]
[5]
Tannus RK, Almeida-Carvalho SR, Loureiro-Matos CA, et al. Evaluation of survival of patients with hepatocellular carcinoma: a comparative analysis of prognostic systems. PLoS One 2018; 13(4)e0194922
[http://dx.doi.org/10.1371/journal.pone.0194922] [PMID: 29617435]
[6]
Schafer DF, Sorrell MF. Hepatocellular carcinoma. Lancet 1999; 353(9160): 1253-7.
[http://dx.doi.org/10.1016/S0140-6736(98)09148-X] [PMID: 10217098]
[7]
Qi J, Wang J, Katayama H, Sen S, Liu SM. Circulating microRNAs (cmiRNAs) as novel potential biomarkers for hepatocellular carcinoma. Neoplasma 2013; 60(2): 135-42.
[http://dx.doi.org/10.4149/neo_2013_018] [PMID: 23259781]
[8]
Zinkin NT, Grall F, Bhaskar K, et al. Serum proteomics and biomarkers in hepatocellular carcinoma and chronic liver disease. Clin Cancer Res 2008; 14(2): 470-7.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-0586] [PMID: 18223221]
[9]
Marrero JA, Su GL, Wei W, et al. Des-gamma carboxyprothrombin can differentiate hepatocellular carcinoma from nonmalignant chronic liver disease in American patients. Hepatology 2003; 37(5): 1114-21.
[http://dx.doi.org/10.1053/jhep.2003.50195] [PMID: 12717392]
[10]
Bruix J, Llovet JM. Prognostic prediction and treatment strategy in hepatocellular carcinoma. Hepatology 2002; 35(3): 519-24.
[http://dx.doi.org/10.1053/jhep.2002.32089] [PMID: 11870363]
[11]
He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5(7): 522-31.
[http://dx.doi.org/10.1038/nrg1379] [PMID: 15211354]
[12]
Ambros V. microRNAs: tiny regulators with great potential. Cell 2001; 107(7): 823-6.
[http://dx.doi.org/10.1016/S0092-8674(01)00616-X] [PMID: 11779458]
[13]
Friedman RC, Farh KK-H, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19(1): 92-105.
[http://dx.doi.org/10.1101/gr.082701.108] [PMID: 18955434]
[14]
Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120(1): 15-20.
[15]
Yin W, Zhao Y, Ji YJ, Tong LP, Liu Y, He SX, et al. Serum/Plasma micrornas as biomarkers for HBV-related hepatocellular carcinoma in China. BioMed Res Int 2015; 52: 1-8.
[16]
Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med 2014; 20(8): 460-9.
[http://dx.doi.org/10.1016/j.molmed.2014.06.005] [PMID: 25027972]
[17]
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 2008; 18(10): 997-1006.
[http://dx.doi.org/10.1038/cr.2008.282] [PMID: 18766170]
[18]
Anwar SL, Lehmann U. MicroRNAs: emerging novel clinical biomarkers for hepatocellular carcinomas. J Clin Med 2015; 4(8): 1631-50.
[http://dx.doi.org/10.3390/jcm4081631] [PMID: 26295264]
[19]
Cai X, Hagedorn CH, Cullen BR. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 2004; 10(12): 1957-66.
[http://dx.doi.org/10.1261/rna.7135204] [PMID: 15525708]
[20]
Han J, Lee Y, Yeom K-H, Kim Y-K, Jin H, Kim VN. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004; 18(24): 3016-27.
[http://dx.doi.org/10.1101/gad.1262504] [PMID: 15574589]
[21]
Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 2005; 6(5): 376-85.
[http://dx.doi.org/10.1038/nrm1644] [PMID: 15852042]
[22]
Lund E, Dahlberg JE. Substrate selectivity of exportin 5 and Dicer in the biogenesis of microRNAs. Cold Spring Harb Symp Quant Biol 2006; 71: 59-66.
[http://dx.doi.org/10.1101/sqb.2006.71.050] [PMID: 17381281]
[23]
Orban TI, Izaurralde E. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 2005; 11(4): 459-69.
[http://dx.doi.org/10.1261/rna.7231505] [PMID: 15703439]
[24]
Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res 2011; 39(16): 7223-33.
[http://dx.doi.org/10.1093/nar/gkr254] [PMID: 21609964]
[25]
Lawrie CH, Gal S, Dunlop HM, et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008; 141(5): 672-5.
[http://dx.doi.org/10.1111/j.1365-2141.2008.07077.x] [PMID: 18318758]
[26]
Liu AM, Zhang C, Burchard J, et al. Global regulation on microRNA in hepatitis B virus-associated hepatocellular carcinoma. OMICS 2011; 15(3): 187-91.
[http://dx.doi.org/10.1089/omi.2010.0098] [PMID: 21319996]
[27]
Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA. MicroRNAs in body fluids--the mix of hormones and biomarkers. Nat Rev Clin Oncol 2011; 8(8): 467-77.
[http://dx.doi.org/10.1038/nrclinonc.2011.76] [PMID: 21647195]
[28]
Shwetha S, Gouthamchandra K, Chandra M, Ravishankar B, Khaja MN, Das S. Circulating miRNA profile in HCV infected serum: novel insight into pathogenesis. Sci Rep 2013; 3: 1555.
[http://dx.doi.org/10.1038/srep01555] [PMID: 23549102]
[29]
Novellino L, Rossi RL, Bonino F, et al. Circulating hepatitis B surface antigen particles carry hepatocellular microRNAs. PLoS One 2012; 7(3)e31952
[http://dx.doi.org/10.1371/journal.pone.0031952] [PMID: 22470417]
[30]
Giordano S, Columbano A. MicroRNAs: new tools for diagnosis, prognosis, and therapy in hepatocellular carcinoma? Hepatology 2013; 57(2): 840-7.
[http://dx.doi.org/10.1002/hep.26095] [PMID: 23081718]
[31]
Arrese M, Eguchi A, Feldstein AE. Circulating microRNAs: emerging biomarkers of liver disease. Semin Liver Dis 2015; 35(1): 43-54.
[http://dx.doi.org/10.1055/s-0034-1397348] [PMID: 25632934]
[32]
Hou J, Lin L, Zhou W, et al. Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. Cancer Cell 2011; 19(2): 232-43.
[http://dx.doi.org/10.1016/j.ccr.2011.01.001] [PMID: 21316602]
[33]
Jopling C. Liver-specific microRNA-122: biogenesis and function. RNA Biol 2012; 9(2): 137-42.
[http://dx.doi.org/10.4161/rna.18827] [PMID: 22258222]
[34]
Tsai W-C, Hsu S-D, Hsu C-S, et al. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest 2012; 122(8): 2884-97.
[http://dx.doi.org/10.1172/JCI63455] [PMID: 22820290]
[35]
Gamazon ER, Innocenti F, Wei R, et al. A genome-wide integrative study of microRNAs in human liver. BMC Genomics 2013; 14: 395.
[http://dx.doi.org/10.1186/1471-2164-14-395] [PMID: 23758991]
[36]
Sharma S, Eghbali M. Influence of sex differences on microRNA gene regulation in disease. Biol Sex Differ 2014; 5(1): 3.
[http://dx.doi.org/10.1186/2042-6410-5-3] [PMID: 24484532]
[37]
Zhang Y, Wu L, Wang Y, et al. Protective role of estrogen-induced miRNA-29 expression in carbon tetrachloride-induced mouse liver injury. J Biol Chem 2012; 287(18): 14851-62.
[http://dx.doi.org/10.1074/jbc.M111.314922] [PMID: 22393047]
[38]
Zhu K, Dai Z, Zhou J. Biomarkers for hepatocellular carcinoma: progression in early diagnosis, prognosis, and personalized therapy. Biomark Res 2013; 1(1): 10.
[http://dx.doi.org/10.1186/2050-7771-1-10] [PMID: 24252133]
[39]
Negrini M, Gramantieri L, Sabbioni S, Croce CM. microRNA involvement in hepatocellular carcinoma. Anticancer Agents Med Chem 2011; 11(6): 500-21.
[http://dx.doi.org/10.2174/187152011796011037] [PMID: 21554203]
[40]
Schütte K, Schulz C, Link A, Malfertheiner P. Current biomarkers for hepatocellular carcinoma: Surveillance, diagnosis and prediction of prognosis. World J Hepatol 2015; 7(2): 139-49.
[http://dx.doi.org/10.4254/wjh.v7.i2.139] [PMID: 25729470]
[41]
Zhang YC, Xu Z, Zhang TF, Wang YL. Circulating microRNAs as diagnostic and prognostic tools for hepatocellular carcinoma. World J Gastroenterol 2015; 21(34): 9853-62.
[http://dx.doi.org/10.3748/wjg.v21.i34.9853] [PMID: 26379392]
[42]
Yao D-F, Dong Z-Z, Yao M. Specific molecular markers in hepatocellular carcinoma. HBPD INT 2007; 6(3): 241-7.
[PMID: 17548245]
[43]
He S, Zhang D-C, Wei C. MicroRNAs as biomarkers for hepatocellular carcinoma diagnosis and prognosis. Clin Res Hepatol Gastroenterol 2015; 39(4): 426-34.
[http://dx.doi.org/10.1016/j.clinre.2015.01.006] [PMID: 25746139]
[44]
Tomimaru Y, Eguchi H, Nagano H, et al. Circulating microRNA-21 as a novel biomarker for hepatocellular carcinoma. J Hepatol 2012; 56(1): 167-75.
[http://dx.doi.org/10.1016/j.jhep.2011.04.026] [PMID: 21749846]
[45]
Qu KZ, Zhang K, Li H, Afdhal NH, Albitar M. Circulating microRNAs as biomarkers for hepatocellular carcinoma. J Clin Gastroenterol 2011; 45(4): 355-60.
[http://dx.doi.org/10.1097/MCG.0b013e3181f18ac2] [PMID: 21278583]
[46]
Yau WL, Lam CSC, Ng L, et al. Over-expression of miR-106b promotes cell migration and metastasis in hepatocellular carcinoma by activating epithelial-mesenchymal transition process. PLoS One 2013; 8(3)e57882
[http://dx.doi.org/10.1371/journal.pone.0057882] [PMID: 23483935]
[47]
Sadri Nahand J, Bokharaei-Salim F, Salmaninejad A, Nesaei A, Mohajeri F, Moshtzan A, et al. microRNAs: key players in virus-associated hepatocellular carcinoma. J Cell Physiol 2019; 234(8): 12188-225.
[PMID: 30536673]
[48]
Braconi C, Henry JC, Kogure T, Schmittgen T, Patel T. The role of microRNAs in human liver cancers. Semin Oncol 2011; 38(6): 752-63.
[http://dx.doi.org/10.1053/j.seminoncol.2011.08.001] [PMID: 22082761]
[49]
Abdalla MA, Haj-Ahmad Y. Promising candidate urinary microRNA biomarkers for the early detection of hepatocellular carcinoma among high-risk hepatitis C Virus Egyptian patients. J Cancer 2012; 3: 19-31.
[http://dx.doi.org/10.7150/jca.3.19] [PMID: 22211142]
[50]
Sun W, Ma J, Wu S, et al. Characterization of the liver Tissue Interstitial Fluid (TIF) proteome indicates potential for application in liver disease biomarker discovery. J Proteome Res 2010; 9(2): 1020-31.
[http://dx.doi.org/10.1021/pr9009172] [PMID: 20038183]
[51]
Jiang L, Cheng Q, Zhang B-H, Zhang M-Z. Circulating microRNAs as biomarkers in hepatocellular carcinoma screening: a validation set from China. Medicine (Baltimore) 2015; 94(10)e603
[http://dx.doi.org/10.1097/MD.0000000000000603] [PMID: 25761179]
[52]
Qi P, Cheng SQ, Wang H, Li N, Chen YF, Gao CF. Serum microRNAs as biomarkers for hepatocellular carcinoma in Chinese patients with chronic hepatitis B virus infection. PLoS One 2011; 6(12)e28486
[http://dx.doi.org/10.1371/journal.pone.0028486] [PMID: 22174818]
[53]
Xu J, Wu C, Che X, et al. Circulating microRNAs, miR-21, miR-122, and miR-223, in patients with hepatocellular carcinoma or chronic hepatitis. Mol Carcinog 2011; 50(2): 136-42.
[http://dx.doi.org/10.1002/mc.20712] [PMID: 21229610]
[54]
Zhou J, Yu L, Gao X, et al. Plasma microRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma. J Clin Oncol 2011; 29(36): 4781-8.
[http://dx.doi.org/10.1200/JCO.2011.38.2697] [PMID: 22105822]
[55]
Tan Y, Ge G, Pan T, et al. A serum microRNA panel as potential biomarkers for hepatocellular carcinoma related with hepatitis B virus. PLoS One 2014; 9(9)e107986
[http://dx.doi.org/10.1371/journal.pone.0107986] [PMID: 25238238]
[56]
Zhang ZQ, Meng H, Wang N, et al. Serum microRNA 143 and microRNA 215 as potential biomarkers for the diagnosis of chronic hepatitis and hepatocellular carcinoma. Diagn Pathol 2014; 9: 135.
[http://dx.doi.org/10.1186/1746-1596-9-135] [PMID: 24993656]
[57]
Oksuz Z, Serin MS, Kaplan E, et al. Serum microRNAs; miR-30c-5p, miR-223-3p, miR-302c-3p and miR-17-5p could be used as novel non-invasive biomarkers for HCV-positive cirrhosis and hepatocellular carcinoma. Mol Biol Rep 2015; 42(3): 713-20.
[http://dx.doi.org/10.1007/s11033-014-3819-9] [PMID: 25391771]
[58]
Bharali D, Jebur HB, Baishya D, et al. Expression analysis of serum microRNA-34a and microRNA-183 in hepatocellular carcinoma. Asian Pac J Cancer Prev 2018; 19(9): 2561-8.
[PMID: 30256056]
[59]
Liang Z, Gao Y, Shi W, et al. Expression and significance of microRNA-183 in hepatocellular carcinoma. Sci World J 2013; 2013381874
[http://dx.doi.org/10.1155/2013/381874] [PMID: 24222732]
[60]
Li L, Guo Z, Wang J, Mao Y, Gao Q. Serum miR-18a: a potential marker for hepatitis B virus-related hepatocellular carcinoma screening. Dig Dis Sci 2012; 57(11): 2910-6.
[http://dx.doi.org/10.1007/s10620-012-2317-y] [PMID: 22865399]
[61]
Yin J, Hou P, Wu Z, Wang T, Nie Y. Circulating miR-375 and miR-199a-3p as potential biomarkers for the diagnosis of hepatocellular carcinoma. Tumour Biol 2015; 36(6): 4501-7.
[http://dx.doi.org/10.1007/s13277-015-3092-0] [PMID: 25618599]
[62]
Wen Y, Han J, Chen J, et al. Plasma miRNAs as early biomarkers for detecting hepatocellular carcinoma. Int J Cancer 2015; 137(7): 1679-90.
[http://dx.doi.org/10.1002/ijc.29544] [PMID: 25845839]
[63]
Bihrer V, Waidmann O, Friedrich-Rust M, et al. Serum microRNA-21 as marker for necroinflammation in hepatitis C patients with and without hepatocellular carcinoma. PLoS One 2011; 6(10)e26971
[http://dx.doi.org/10.1371/journal.pone.0026971] [PMID: 22066022]
[64]
Li L-M, Hu Z-B, Zhou Z-X, et al. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res 2010; 70(23): 9798-807.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1001] [PMID: 21098710]
[65]
Lin X-J, Chong Y, Guo Z-W, et al. A serum microRNA classifier for early detection of hepatocellular carcinoma: a multicentre, retrospective, longitudinal biomarker identification study with a nested case-control study. Lancet Oncol 2015; 16(7): 804-15.
[http://dx.doi.org/10.1016/S1470-2045(15)00048-0] [PMID: 26088272]
[66]
Shen J, Wang A, Wang Q, et al. Exploration of genome-wide circulating microRNA in hepatocellular carcinoma: miR-483-5p as a potential biomarker. Cancer Epidemiol Biomarkers Prev 2013; 22(12): 2364-73.
[http://dx.doi.org/10.1158/1055-9965.EPI-13-0237] [PMID: 24127413]
[67]
Gui J, Tian Y, Wen X, et al. Serum microRNA characterization identifies miR-885-5p as a potential marker for detecting liver pathologies. Clin Sci 2011; 120(5): 183-93.
[http://dx.doi.org/10.1042/CS20100297] [PMID: 20815808]
[68]
Shigoka M, Tsuchida A, Matsudo T, et al. Deregulation of miR-92a expression is implicated in hepatocellular carcinoma development. Pathol Int 2010; 60(5): 351-7.
[http://dx.doi.org/10.1111/j.1440-1827.2010.02526.x] [PMID: 20518884]
[69]
Tarek M, Louka ML, Khairy E, Ali-Labib R, Zakaria Zaky D, Montasser IF. Role of microRNA-7 and selenoprotein P in hepatocellular carcinoma. Tumour Biol 2017; 39(5)1010428317698372
[http://dx.doi.org/10.1177/1010428317698372] [PMID: 28459371]
[70]
Shen X, Xue Y, Cong H, Wang X, Ju S. Dysregulation of serum microRNA-574-3p and its clinical significance in hepatocellular carcinoma. Ann Clin Biochem 2018; 55(4): 478-84.
[http://dx.doi.org/10.1177/0004563217741908] [PMID: 29065698]
[71]
Jiang L, Li X, Cheng Q, Zhang B-H. Plasma microRNA might as a potential biomarker for hepatocellular carcinoma and chronic liver disease screening. Tumour Biol 2015; 36(9): 7167-74.
[http://dx.doi.org/10.1007/s13277-015-3446-7] [PMID: 25894380]
[72]
Liu AM, Yao T-J, Wang W, et al. Circulating miR-15b and miR-130b in serum as potential markers for detecting hepatocellular carcinoma: a retrospective cohort study. BMJ Open 2012; 2(2)e000825
[http://dx.doi.org/10.1136/bmjopen-2012-000825] [PMID: 22403344]
[73]
Huang X, Yuan T, Tschannen M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics 2013; 14: 319.
[http://dx.doi.org/10.1186/1471-2164-14-319] [PMID: 23663360]
[74]
Conde-Vancells J, Rodriguez-Suarez E, Embade N, et al. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res 2008; 7(12): 5157-66.
[http://dx.doi.org/10.1021/pr8004887] [PMID: 19367702]
[75]
Kogure T, Lin W-L, Yan IK, Braconi C, Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011; 54(4): 1237-48.
[http://dx.doi.org/10.1002/hep.24504] [PMID: 21721029]
[76]
Wang H, Hou L, Li A, Duan Y, Gao H, Song X. Expression of serum exosomal microRNA-21 in human hepatocellular carcinoma. BioMed Res Int 2014; 2014864894
[http://dx.doi.org/10.1155/2014/864894] [PMID: 24963487]
[77]
Qu Z, Wu J, Wu J, et al. Exosomal miR-665 as a novel minimally invasive biomarker for hepatocellular carcinoma diagnosis and prognosis. Oncotarget 2017; 8(46): 80666-78.
[http://dx.doi.org/10.18632/oncotarget.20881] [PMID: 29113334]
[78]
Köberle V, Kronenberger B, Pleli T, et al. Serum microRNA-1 and microRNA-122 are prognostic markers in patients with hepatocellular carcinoma. Eur J Cancer 2013; 49(16): 3442-9.
[http://dx.doi.org/10.1016/j.ejca.2013.06.002] [PMID: 23810247]
[79]
Xu Y, Bu X, Dai C, Shang C. High serum microRNA-122 level is independently associated with higher overall survival rate in hepatocellular carcinoma patients. Tumour Biol 2015; 36(6): 4773-6.
[http://dx.doi.org/10.1007/s13277-015-3128-5] [PMID: 25636448]
[80]
Li J, Wang Y, Yu W, Chen J, Luo J. Expression of serum miR-221 in human hepatocellular carcinoma and its prognostic significance. Biochem Biophys Res Commun 2011; 406(1): 70-3.
[http://dx.doi.org/10.1016/j.bbrc.2011.01.111] [PMID: 21295551]
[81]
Zhang P, Zhang M, Han R, et al. The correlation between microRNA-221/222 cluster overexpression and malignancy: an updated meta-analysis including 2693 patients. Cancer Manag Res 2018; 10: 3371-81.
[http://dx.doi.org/10.2147/CMAR.S171303] [PMID: 30237739]
[82]
Zhang Y, Wei C, Guo C-C, et al. Prognostic value of microRNAs in hepatocellular carcinoma: a meta-analysis. Oncotarget 2017; 8(63): 107237-57.
[http://dx.doi.org/10.18632/oncotarget.20883] [PMID: 29291025]
[83]
Su ZX, Zhao J, Rong ZH, Geng WM, Wu YG, Qin CK. Upregulation of microRNA-25 associates with prognosis in hepatocellular carcinoma. Diagn Pathol 2014; 9: 47.
[http://dx.doi.org/10.1186/1746-1596-9-47] [PMID: 24593846]
[84]
Wang J, Li J, Shen J, Wang C, Yang L, Zhang X. MicroRNA-182 downregulates metastasis suppressor 1 and contributes to metastasis of hepatocellular carcinoma. BMC Cancer 2012; 12: 227.
[http://dx.doi.org/10.1186/1471-2407-12-227] [PMID: 22681717]
[85]
Gu H, Guo X, Zou L, Zhu H, Zhang J. Upregulation of microRNA-372 associates with tumor progression and prognosis in hepatocellular carcinoma. Mol Cell Biochem 2013; 375(1-2): 23-30.
[http://dx.doi.org/10.1007/s11010-012-1521-6] [PMID: 23291979]
[86]
Xiong Y, Fang J-H, Yun J-P, et al. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 2010; 51(3): 836-45.
[PMID: 20041405]
[87]
Zhu H-T, Dong Q-Z, Sheng Y-Y, et al. MicroRNA-29a-5p is a novel predictor for early recurrence of hepatitis B virus-related hepatocellular carcinoma after surgical resection. PLoS One 2012; 7(12)e52393
[http://dx.doi.org/10.1371/journal.pone.0052393] [PMID: 23285022]
[88]
Zhang Y, Guo X, Xiong L, et al. MicroRNA-101 suppresses SOX9-dependent tumorigenicity and promotes favorable prognosis of human hepatocellular carcinoma. FEBS Lett 2012; 586(24): 4362-70.
[http://dx.doi.org/10.1016/j.febslet.2012.10.053] [PMID: 23178713]
[89]
Zhang Z, Zheng W, Hai J. MicroRNA-148b expression is decreased in hepatocellular carcinoma and associated with prognosis. Med Oncol 2014; 31(6): 984.
[http://dx.doi.org/10.1007/s12032-014-0984-6] [PMID: 24805877]
[90]
Luk JM, Burchard J, Zhang C, et al. DLK1-DIO3 genomic imprinted microRNA cluster at 14q32.2 defines a stem like subtype of hepatocellular carcinoma associated with poor survival. J Biol Chem 2011; 286(35): 30706-13.
[http://dx.doi.org/10.1074/jbc.M111.229831] [PMID: 21737452]
[91]
Chen H-Y, Han Z-B, Fan J-W, et al. miR-203 expression predicts outcome after liver transplantation for hepatocellular carcinoma in cirrhotic liver. Med Oncol 2012; 29(3): 1859-65.
[http://dx.doi.org/10.1007/s12032-011-0031-9] [PMID: 21786180]
[92]
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 2012; 56(2): 389-96.
[http://dx.doi.org/10.1016/j.jhep.2011.08.008] [PMID: 21888875]
[93]
Zheng F, Liao Y-J, Cai M-Y, et al. The putative tumour suppressor microRNA-124 modulates hepatocellular carcinoma cell aggressiveness by repressing ROCK2 and EZH2. Gut 2012; 61(2): 278-89.
[http://dx.doi.org/10.1136/gut.2011.239145] [PMID: 21672940]
[94]
Coulouarn C, Factor VM, Andersen JB, Durkin ME, Thorgeirsson SS. Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene 2009; 28(40): 3526-36.
[http://dx.doi.org/10.1038/onc.2009.211] [PMID: 19617899]
[95]
Wong CC-L, Wong C-M, Tung EK-K, et al. The microRNA miR-139 suppresses metastasis and progression of hepatocellular carcinoma by down-regulating Rho-kinase 2. Gastroenterology 2011; 140(1): 322-31.
[http://dx.doi.org/10.1053/j.gastro.2010.10.006] [PMID: 20951699]
[96]
Li D, Liu X, Lin L, et al. MicroRNA-99a inhibits hepatocellular carcinoma growth and correlates with prognosis of patients with hepatocellular carcinoma. J Biol Chem 2011; 286(42): 36677-85.
[http://dx.doi.org/10.1074/jbc.M111.270561] [PMID: 21878637]
[97]
Zhang J, Yang Y, Yang T, et al. microRNA-22, downregulated in hepatocellular carcinoma and correlated with prognosis, suppresses cell proliferation and tumourigenicity. Br J Cancer 2010; 103(8): 1215-20.
[http://dx.doi.org/10.1038/sj.bjc.6605895] [PMID: 20842113]
[98]
Wang C, Song B, Song W, et al. Underexpressed microRNA-199b-5p targets hypoxia-inducible factor-1α in hepatocellular carcinoma and predicts prognosis of hepatocellular carcinoma patients. J Gastroenterol Hepatol 2011; 26(11): 1630-7.
[http://dx.doi.org/10.1111/j.1440-1746.2011.06758.x] [PMID: 21557766]
[99]
Ji J, Zhao L, Budhu A, et al. Let-7g targets collagen type I alpha2 and inhibits cell migration in hepatocellular carcinoma. J Hepatol 2010; 52(5): 690-7.
[http://dx.doi.org/10.1016/j.jhep.2009.12.025] [PMID: 20338660]
[100]
Lian J, Jing Y, Dong Q, et al. miR-192, a prognostic indicator, targets the SLC39A6/SNAIL pathway to reduce tumor metastasis in human hepatocellular carcinoma. Oncotarget 2016; 7(3): 2672-83.
[http://dx.doi.org/10.18632/oncotarget.6603] [PMID: 26684241]
[101]
Huang YH, Lin KH, Chen HC, et al. Identification of postoperative prognostic microRNA predictors in hepatocellular carcinoma. PLoS One 2012; 7(5)e37188
[http://dx.doi.org/10.1371/journal.pone.0037188] [PMID: 22629365]
[102]
Zhang J, Chong CCN, Chen GG, Lai PBS. A seven-microRNA expression signature predicts survival in hepatocellular carcinoma. PLoS One 2015; 10(6)e0128628
[http://dx.doi.org/10.1371/journal.pone.0128628] [PMID: 26046780]
[103]
Han ZB, Chen HY, Fan JW, Wu JY, Tang HM, Peng ZH. Up-regulation of microRNA-155 promotes cancer cell invasion and predicts poor survival of hepatocellular carcinoma following liver transplantation. J Cancer Res Clin Oncol 2012; 138(1): 153-61.
[http://dx.doi.org/10.1007/s00432-011-1076-z] [PMID: 22071603]
[104]
Han Z-B, Zhong L, Teng M-J, et al. Identification of recurrence-related microRNAs in hepatocellular carcinoma following liver transplantation. Mol Oncol 2012; 6(4): 445-57.
[http://dx.doi.org/10.1016/j.molonc.2012.04.001] [PMID: 22552153]
[105]
Barry CT, D’Souza M, McCall M, et al. Micro RNA expression profiles as adjunctive data to assess the risk of hepatocellular carcinoma recurrence after liver transplantation. Am J Transplant 2012; 12(2): 428-37.
[http://dx.doi.org/10.1111/j.1600-6143.2011.03788.x] [PMID: 22008552]
[106]
Yoon SO, Chun S-M, Han EH, et al. Deregulated expression of microRNA-221 with the potential for prognostic biomarkers in surgically resected hepatocellular carcinoma. Hum Pathol 2011; 42(10): 1391-400.
[http://dx.doi.org/10.1016/j.humpath.2010.12.010] [PMID: 21458843]
[107]
Wang J, Li J, Wang X, Zheng C, Ma W. Downregulation of microRNA-214 and overexpression of FGFR-1 contribute to hepatocellular carcinoma metastasis. Biochem Biophys Res Commun 2013; 439(1): 47-53.
[http://dx.doi.org/10.1016/j.bbrc.2013.08.032] [PMID: 23962428]
[108]
Ura S, Honda M, Yamashita T, et al. Differential microRNA expression between hepatitis B and hepatitis C leading disease progression to hepatocellular carcinoma. Hepatology 2009; 49(4): 1098-112.
[http://dx.doi.org/10.1002/hep.22749] [PMID: 19173277]
[109]
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 2009; 275(1): 44-53.
[http://dx.doi.org/10.1016/j.canlet.2008.09.035] [PMID: 19006648]
[110]
Pan L, Huang S, He R, Rong M, Dang Y, Chen G. Decreased expression and clinical significance of miR-148a in hepatocellular carcinoma tissues. Eur J Med Res 2014; 19: 68.
[http://dx.doi.org/10.1186/s40001-014-0068-2] [PMID: 25444499]
[111]
El Tayebi HM, Omar K, Hegy S, et al. Repression of miR-17-5p with elevated expression of E2F-1 and c-MYC in non-metastatic hepatocellular carcinoma and enhancement of cell growth upon reversing this expression pattern. Biochem Biophys Res Commun 2013; 434(3): 421-7.
[http://dx.doi.org/10.1016/j.bbrc.2013.04.003] [PMID: 23583198]
[112]
Karakatsanis A, Papaconstantinou I, Gazouli M, Lyberopoulou A, Polymeneas G, Voros D. Expression of microRNAs, miR-21, miR-31, miR-122, miR-145, miR-146a, miR-200c, miR-221, miR-222, and miR-223 in patients with hepatocellular carcinoma or intrahepatic cholangiocarcinoma and its prognostic significance. Mol Carcinog 2013; 52(4): 297-303.
[http://dx.doi.org/10.1002/mc.21864] [PMID: 22213236]
[113]
Chen Q, Yin D, Zhang Y, et al. MicroRNA-29a induces loss of 5-hydroxymethylcytosine and promotes metastasis of hepatocellular carcinoma through a TET-SOCS1-MMP9 signaling axis. Cell Death Dis 2017; 8(6)e2906
[http://dx.doi.org/10.1038/cddis.2017.142] [PMID: 28661477]
[114]
Huang X-H, Wang Q, Chen J-S, et al. Bead-based microarray analysis of microRNA expression in hepatocellular carcinoma: miR-338 is downregulated. Hepatol Res 2009; 39(8): 786-94.
[http://dx.doi.org/10.1111/j.1872-034X.2009.00502.x] [PMID: 19473441]
[115]
Augello C, Vaira V, Caruso L, et al. MicroRNA profiling of hepatocarcinogenesis identifies C19MC cluster as a novel prognostic biomarker in hepatocellular carcinoma. Liver Int 2012; 32(5): 772-82.
[http://dx.doi.org/10.1111/j.1478-3231.2012.02795.x] [PMID: 22429613]
[116]
Sato F, Hatano E, Kitamura K, et al. MicroRNA profile predicts recurrence after resection in patients with hepatocellular carcinoma within the Milan Criteria. PLoS One 2011; 6(1)e16435
[http://dx.doi.org/10.1371/journal.pone.0016435] [PMID: 21298008]
[117]
Li QJ, Zhou L, Yang F, et al. MicroRNA-10b promotes migration and invasion through CADM1 in human hepatocellular carcinoma cells. Tumour Biol 2012; 33(5): 1455-65.
[http://dx.doi.org/10.1007/s13277-012-0396-1] [PMID: 22528944]
[118]
Vaira V, Roncalli M, Carnaghi C, et al. MicroRNA-425-3p predicts response to sorafenib therapy in patients with hepatocellular carcinoma. Liver Int 2015; 35(3): 1077-86.
[http://dx.doi.org/10.1111/liv.12636] [PMID: 25040368]
[119]
Krützfeldt J, Kuwajima S, Braich R, et al. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res 2007; 35(9): 2885-92.
[http://dx.doi.org/10.1093/nar/gkm024] [PMID: 17439965]
[120]
Stenvang J, Silahtaroglu AN, Lindow M, Elmen J, Kauppinen S. The utility of LNA in microRNA-based cancer diagnostics and therapeutics. Semin Cancer Biol 2008; 18(2): 89-102.
[http://dx.doi.org/10.1016/j.semcancer.2008.01.004] [PMID: 18295505]
[121]
Park JK, Kogure T, Nuovo GJ, et al. miR-221 silencing blocks hepatocellular carcinoma and promotes survival. Cancer Res 2011; 71(24): 7608-16.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-1144] [PMID: 22009537]
[122]
Callegari E, Elamin BK, Giannone F, et al. Liver tumorigenicity promoted by microRNA-221 in a mouse transgenic model. Hepatology 2012; 56(3): 1025-33.
[http://dx.doi.org/10.1002/hep.25747] [PMID: 22473819]
[123]
Toffanin S, Hoshida Y, Lachenmayer A, et al. MicroRNA-based classification of hepatocellular carcinoma and oncogenic role of miR-517a. Gastroenterology 2011; 140(5): 1618-28.e16.
[http://dx.doi.org/10.1053/j.gastro.2011.02.009] [PMID: 21324318]
[124]
Krützfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with ‘antagomirs’. Nature 2005; 438(7068): 685-9.
[http://dx.doi.org/10.1038/nature04303] [PMID: 16258535]
[125]
Lim L, Balakrishnan A, Huskey N, et al. MicroRNA-494 within an oncogenic microRNA megacluster regulates G1/S transition in liver tumorigenesis through suppression of mutated in colorectal cancer. Hepatology 2014; 59(1): 202-15.
[http://dx.doi.org/10.1002/hep.26662] [PMID: 23913442]
[126]
Ying Q, Liang L, Guo W, et al. Hypoxia-inducible microRNA-210 augments the metastatic potential of tumor cells by targeting vacuole membrane protein 1 in hepatocellular carcinoma. Hepatology 2011; 54(6): 2064-75.
[http://dx.doi.org/10.1002/hep.24614] [PMID: 22144109]
[127]
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 2010; 51(5): 1614-23.
[http://dx.doi.org/10.1002/hep.23566] [PMID: 20209605]
[128]
Xu J, Li J, Zheng T-H, Bai L, Liu Z-J. MicroRNAs in the occurrence and development of primary hepatocellular carcinoma. Adv Clin Exp Med 2016; 25(5): 971-5.
[http://dx.doi.org/10.17219/acem/36460] [PMID: 28028963]
[129]
Kota J, Chivukula RR, O’Donnell KA, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009; 137(6): 1005-17.
[http://dx.doi.org/10.1016/j.cell.2009.04.021] [PMID: 19524505]
[130]
Fornari F, Milazzo M, Chieco P, et al. MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 2010; 70(12): 5184-93.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-0145] [PMID: 20501828]
[131]
Jia XQ, Cheng HQ, Qian X, et al. Lentivirus-mediated overexpression of microRNA-199a inhibits cell proliferation of human hepatocellular carcinoma. Cell Biochem Biophys 2012; 62(1): 237-44.
[http://dx.doi.org/10.1007/s12013-011-9263-8] [PMID: 21847633]
[132]
Hsu S-H, Wang B, Kota J, et al. Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest 2012; 122(8): 2871-83.
[http://dx.doi.org/10.1172/JCI63539] [PMID: 22820288]
[133]
Lang Q, Ling C. MiR-124 suppresses cell proliferation in hepatocellular carcinoma by targeting PIK3CA. Biochem Biophys Res Commun 2012; 426(2): 247-52.
[http://dx.doi.org/10.1016/j.bbrc.2012.08.075] [PMID: 22940133]
[134]
Lou G, Song X, Yang F, et al. Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma. J Hematol Oncol 2015; 8: 122.
[http://dx.doi.org/10.1186/s13045-015-0220-7] [PMID: 26514126]
[135]
Spaniel C, Honda M, Selitsky SR, et al. microRNA-122 abundance in hepatocellular carcinoma and non-tumor liver tissue from Japanese patients with persistent HCV versus HBV infection. PLoS One 2013; 8(10)e76867
[http://dx.doi.org/10.1371/journal.pone.0076867] [PMID: 24130799]
[136]
Lanford RE, Hildebrandt-Eriksen ES, Petri A, et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010; 327(5962): 198-201.
[http://dx.doi.org/10.1126/science.1178178] [PMID: 19965718]
[137]
Hildebrandt-Eriksen ES, Aarup V, Persson R, Hansen HF, Munk ME, Ørum H. A locked nucleic acid oligonucleotide targeting microRNA 122 is well-tolerated in cynomolgus monkeys. Nucleic Acid Ther 2012; 22(3): 152-61.
[http://dx.doi.org/10.1089/nat.2011.0332] [PMID: 22545703]
[138]
Janssen HLA, Reesink HW, Lawitz EJ, et al. Treatment of HCV infection by targeting microRNA. N Engl J Med 2013; 368(18): 1685-94.
[http://dx.doi.org/10.1056/NEJMoa1209026] [PMID: 23534542]
[139]
Gebert LFR, Rebhan MAE, Crivelli SEM, Denzler R, Stoffel M, Hall J. Miravirsen (SPC3649) can inhibit the biogenesis of miR-122. Nucleic Acids Res 2014; 42(1): 609-21.
[http://dx.doi.org/10.1093/nar/gkt852] [PMID: 24068553]
[140]
Salvi A, Conde I, Abeni E, et al. Effects of miR-193a and sorafenib on hepatocellular carcinoma cells. Mol Cancer 2013; 12: 162.
[http://dx.doi.org/10.1186/1476-4598-12-162] [PMID: 24330766]
[141]
Aravalli RN. Development of microRNA therapeutics for hepatocellular carcinoma. Diagnostics (Basel) 2013; 3(1): 170-91.
[http://dx.doi.org/10.3390/diagnostics3010170] [PMID: 26835673]
[142]
Beg MS, Brenner AJ, Sachdev J, et al. Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Invest New Drugs 2017; 35(2): 180-8.
[http://dx.doi.org/10.1007/s10637-016-0407-y] [PMID: 27917453]
[143]
Heo MJ, Yun J, Kim SG. Role of non-coding RNAs in liver disease progression to hepatocellular carcinoma. Arch Pharm Res 2019; 42(1): 48-62.
[http://dx.doi.org/10.1007/s12272-018-01104-x] [PMID: 30610616]
[144]
Zhuang L, Zeng X, Yang Z, Meng Z. Effect and safety of interferon for hepatocellular carcinoma: a systematic review and meta-analysis. PLoS One 2013; 8(9)e61361
[http://dx.doi.org/10.1371/journal.pone.0061361] [PMID: 24069133]
[145]
Tomokuni A, Eguchi H, Tomimaru Y, et al. miR-146a suppresses the sensitivity to interferon-α in hepatocellular carcinoma cells. Biochem Biophys Res Commun 2011; 414(4): 675-80.
[http://dx.doi.org/10.1016/j.bbrc.2011.09.124] [PMID: 21982769]
[146]
Ji J, Shi J, Budhu A, et al. MicroRNA expression, survival, and response to interferon in liver cancer. N Engl J Med 2009; 361(15): 1437-47.
[http://dx.doi.org/10.1056/NEJMoa0901282] [PMID: 19812400]
[147]
Ji J, Yu L, Yu Z, et al. Development of a miR-26 companion diagnostic test for adjuvant interferon-alpha therapy in hepatocellular carcinoma. Int J Biol Sci 2013; 9(3): 303-12.
[http://dx.doi.org/10.7150/ijbs.6214] [PMID: 23569435]
[148]
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 2010; 103(10): 1617-26.
[http://dx.doi.org/10.1038/sj.bjc.6605958] [PMID: 20978511]
[149]
Chen Z, Ma T, Huang C, et al. MiR-27a modulates the MDR1/P-glycoprotein expression by inhibiting FZD7/β-catenin pathway in hepatocellular carcinoma cells. Cell Signal 2013; 25(12): 2693-701.
[http://dx.doi.org/10.1016/j.cellsig.2013.08.032] [PMID: 24018051]
[150]
Yin J, Tang HF, Xiang Q, et al. MiR-122 increases sensitivity of drug-resistant BEL-7402/5-FU cells to 5-fluorouracil via down-regulation of bcl-2 family proteins. Pharmazie 2011; 66(12): 975-81.
[PMID: 22312705]
[151]
Jiang J-X, Gao S, Pan Y-Z, Yu C, Sun C-Y. Overexpression of microRNA-125b sensitizes human hepatocellular carcinoma cells to 5-fluorouracil through inhibition of glycolysis by targeting hexokinase II. Mol Med Rep 2014; 10(2): 995-1002.
[http://dx.doi.org/10.3892/mmr.2014.2271] [PMID: 24865963]
[152]
Yang X, Yin J, Yu J, et al. miRNA-195 sensitizes human hepatocellular carcinoma cells to 5-FU by targeting BCL-w. Oncol Rep 2012; 27(1): 250-7.
[PMID: 21947305]
[153]
Yang X, Zang J, Pan X, et al. miR-503 inhibits proliferation making human hepatocellular carcinoma cells susceptible to 5-fluorouracil by targeting EIF4E. Oncol Rep 2017; 37(1): 563-70.
[http://dx.doi.org/10.3892/or.2016.5220] [PMID: 27840964]
[154]
He X, Li J, Guo W, et al. Targeting the microRNA-21/AP1 axis by 5-fluorouracil and pirarubicin in human hepatocellular carcinoma. Oncotarget 2015; 6(4): 2302-14.
[http://dx.doi.org/10.18632/oncotarget.2955] [PMID: 25544773]
[155]
Shi L, Wu L, Chen Z, et al. MiR-141 activates Nrf2-dependent antioxidant pathway via down-regulating the expression of keap1 conferring the resistance of hepatocellular carcinoma cells to 5-fluorouracil. Cell Physiol Biochem 2015; 35(6): 2333-48.
[http://dx.doi.org/10.1159/000374036] [PMID: 25896253]
[156]
Lee H, Kim C, Kang H, et al. microRNA-200a-3p increases 5-fluorouracil resistance by regulating dual specificity phosphatase 6 expression. Exp Mol Med 2017; 49(5)e327
[http://dx.doi.org/10.1038/emm.2017.33] [PMID: 28496200]
[157]
Shao P, Qu W-K, Wang C-Y, et al. MicroRNA-205-5p regulates the chemotherapeutic resistance of hepatocellular carcinoma cells by targeting PTEN/JNK/ANXA3 pathway. Am J Transl Res 2017; 9(9): 4300-7.
[PMID: 28979703]
[158]
Zhou C, Liu J, Li Y, et al. microRNA-1274a, a modulator of sorafenib induced a disintegrin and metalloproteinase 9 (ADAM9) down-regulation in hepatocellular carcinoma. FEBS Lett 2011; 585(12): 1828-34.
[http://dx.doi.org/10.1016/j.febslet.2011.04.040] [PMID: 21530512]
[159]
Bai S, Nasser MW, Wang B, et al. MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J Biol Chem 2009; 284(46): 32015-27.
[http://dx.doi.org/10.1074/jbc.M109.016774] [PMID: 19726678]
[160]
Xu Y, Huang J, Ma L, et al. MicroRNA-122 confers sorafenib resistance to hepatocellular carcinoma cells by targeting IGF-1R to regulate RAS/RAF/ERK signaling pathways. Cancer Lett 2016; 371(2): 171-81.
[http://dx.doi.org/10.1016/j.canlet.2015.11.034] [PMID: 26655273]
[161]
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 2010; 52(5): 698-704.
[http://dx.doi.org/10.1016/j.jhep.2009.12.024] [PMID: 20347499]
[162]
Mao K, Zhang J, He C, et al. Restoration of miR-193b sensitizes hepatitis B virus-associated hepatocellular carcinoma to sorafenib. Cancer Lett 2014; 352(2): 245-52.
[http://dx.doi.org/10.1016/j.canlet.2014.07.004] [PMID: 25034398]
[163]
Xu H, Zhao L, Fang Q, et al. MiR-338-3p inhibits hepatocarcinoma cells and sensitizes these cells to sorafenib by targeting hypoxia-induced factor 1α. PLoS One 2014; 9(12)e115565
[http://dx.doi.org/10.1371/journal.pone.0115565] [PMID: 25531114]
[164]
Yang F, Li QJ, Gong ZB, et al. MicroRNA-34a targets Bcl-2 and sensitizes human hepatocellular carcinoma cells to sorafenib treatment. Technol Cancer Res Treat 2014; 13(1): 77-86.
[http://dx.doi.org/10.7785/tcrt.2012.500364] [PMID: 23862748]
[165]
He C, Dong X, Zhai B, et al. MiR-21 mediates sorafenib resistance of hepatocellular carcinoma cells by inhibiting autophagy via the PTEN/Akt pathway. Oncotarget 2015; 6(30): 28867-81.
[http://dx.doi.org/10.18632/oncotarget.4814] [PMID: 26311740]
[166]
Liu K, Liu S, Zhang W, Ji B, Wang Y, Liu Y. miR-222 regulates sorafenib resistance and enhance tumorigenicity in hepatocellular carcinoma. Int J Oncol 2014; 45(4): 1537-46.
[http://dx.doi.org/10.3892/ijo.2014.2577] [PMID: 25096647]
[167]
Liu K, Liu S, Zhang W, et al. miR-494 promotes cell proliferation, migration and invasion, and increased sorafenib resistance in hepatocellular carcinoma by targeting PTEN. Oncol Rep 2015; 34(2): 1003-10.
[http://dx.doi.org/10.3892/or.2015.4030] [PMID: 26045065]
[168]
Kabir TD, Ganda C, Brown RM, et al. A microRNA-7/growth arrest specific 6/TYRO3 axis regulates the growth and invasiveness of sorafenib-resistant cells in human hepatocellular carcinoma. Hepatology 2018; 67(1): 216-31.
[http://dx.doi.org/10.1002/hep.29478] [PMID: 28833396]
[169]
Potenza N, Mosca N, Zappavigna S, et al. MicroRNA-125a-5p is a downstream effector of sorafenib in its antiproliferative activity toward human hepatocellular carcinoma cells. J Cell Physiol 2017; 232(7): 1907-13.
[http://dx.doi.org/10.1002/jcp.25744] [PMID: 27982429]
[170]
Lu A-Q, Lv B, Qiu F, Wang X-Y, Cao X-H. Upregulation of miR-137 reverses sorafenib resistance and cancer-initiating cell phenotypes by degrading ANT2 in hepatocellular carcinoma. Oncol Rep 2017; 37(4): 2071-8.
[http://dx.doi.org/10.3892/or.2017.5498] [PMID: 28350139]
[171]
Fornari F, Pollutri D, Patrizi C, et al. In hepatocellular carcinoma miR-221 modulates sorafenib resistance through inhibition of caspase-3-mediated apoptosis. Clin Cancer Res 2017; 23(14): 3953-65.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-1464] [PMID: 28096271]
[172]
Xu J, Lin H, Li G, et al. The miR-367-3p increases sorafenib chemotherapy efficacy to suppress hepatocellular carcinoma metastasis through altering the androgen receptor signals. EBioMedicine 2016; 12: 55-67.
[http://dx.doi.org/10.1016/j.ebiom.2016.07.013] [PMID: 27688096]
[173]
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 2009; 69(14): 5761-7.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-4797] [PMID: 19584283]
[174]
Zhao N, Wang R, Zhou L, Zhu Y, Gong J, Zhuang S-M. MicroRNA-26b suppresses the NF-κB signaling and enhances the chemosensitivity of hepatocellular carcinoma cells by targeting TAK1 and TAB3. Mol Cancer 2014; 13: 35.
[http://dx.doi.org/10.1186/1476-4598-13-35] [PMID: 24565101]
[175]
Jin F, Wang Y, Li M, et al. MiR-26 enhances chemosensitivity and promotes apoptosis of hepatocellular carcinoma cells through inhibiting autophagy. Cell Death Dis 2017; 8(1)e2540
[http://dx.doi.org/10.1038/cddis.2016.461] [PMID: 28079894]
[176]
He H, Tian W, Chen H, Deng Y. MicroRNA-101 sensitizes hepatocellular carcinoma cells to doxorubicin-induced apoptosis via targeting Mcl-1. Mol Med Rep 2016; 13(2): 1923-9.
[http://dx.doi.org/10.3892/mmr.2015.4727] [PMID: 26718267]
[177]
Xu Y, An Y, Wang Y, et al. miR-101 inhibits autophagy and enhances cisplatin-induced apoptosis in hepatocellular carcinoma cells. Oncol Rep 2013; 29(5): 2019-24.
[http://dx.doi.org/10.3892/or.2013.2338] [PMID: 23483142]
[178]
Meng W, Tai Y, Zhao H, et al. Downregulation of miR-33a-5p in hepatocellular carcinoma: a possible mechanism for chemotherapy resistance. Med Sci Monit 2017; 23: 1295-304.
[http://dx.doi.org/10.12659/MSM.902692] [PMID: 28291769]
[179]
Xu N, Zhang J, Shen C, et al. Cisplatin-induced downregulation of miR-199a-5p increases drug resistance by activating autophagy in HCC cell. Biochem Biophys Res Commun 2012; 423(4): 826-31.
[http://dx.doi.org/10.1016/j.bbrc.2012.06.048] [PMID: 22713463]
[180]
Ou Y, Zhai D, Wu N, Li X. Downregulation of miR-363 increases drug resistance in cisplatin-treated HepG2 by dysregulating Mcl-1. Gene 2015; 572(1): 116-22.
[http://dx.doi.org/10.1016/j.gene.2015.07.002] [PMID: 26143754]
[181]
Qin J, Luo M, Qian H, Chen W. Upregulated miR-182 increases drug resistance in cisplatin-treated HCC cell by regulating TP53INP1. Gene 2014; 538(2): 342-7.
[http://dx.doi.org/10.1016/j.gene.2013.12.043] [PMID: 24447717]
[182]
Yin W, Nie Y, Zhang Z, Xie L, He X. miR-193b acts as a cisplatin sensitizer via the caspase-3-dependent pathway in HCC chemotherapy. Oncol Rep 2015; 34(1): 368-74.
[http://dx.doi.org/10.3892/or.2015.3996] [PMID: 25997995]
[183]
Wang N, Zhu M, Tsao S-W, Man K, Zhang Z, Feng Y. MiR-23a-mediated inhibition of topoisomerase 1 expression potentiates cell response to etoposide in human hepatocellular carcinoma. Mol Cancer 2013; 12(1): 119.
[http://dx.doi.org/10.1186/1476-4598-12-119] [PMID: 24103454]
[184]
Chen F, Zhu H-H, Zhou L-F, Wu S-S, Wang J, Chen Z. Inhibition of c-FLIP expression by miR-512-3p contributes to taxol-induced apoptosis in hepatocellular carcinoma cells. Oncol Rep 2010; 23(5): 1457-62.
[http://dx.doi.org/10.3892/or_00000784] [PMID: 20372864]
[185]
Huang X, Qin J, Lu S. Up-regulation of miR-877 induced by paclitaxel inhibits hepatocellular carcinoma cell proliferation though targeting FOXM1. Int J Clin Exp Pathol 2015; 8(2): 1515-24.
[PMID: 25973036]
[186]
Xue F, Liang Y, Li Z, et al. MicroRNA-9 enhances sensitivity to cetuximab in epithelial phenotype hepatocellular carcinoma cells through regulation of the eukaryotic translation initiation factor 5A-2. Oncol Lett 2018; 15(1): 813-20.
[PMID: 29399149]
[187]
Liu Y, Lei P, Qiao H, et al. miR-9 enhances the chemosensitivity of AML cells to daunorubicin by targeting the EIF5A2/MCL-1 axis. Int J Biol Sci 2019; 15(3): 579-86.
[http://dx.doi.org/10.7150/ijbs.29775] [PMID: 30745844]
[188]
Borel F, Han R, Visser A, et al. Réseau centre de ressources biologiques foie (French Liver Biobanks Network), France. Adenosine triphosphate-binding cassette transporter genes up-regulation in untreated hepatocellular carcinoma is mediated by cellular microRNAs. Hepatology 2012; 55(3): 821-32.
[http://dx.doi.org/10.1002/hep.24682] [PMID: 21932399]

© 2024 Bentham Science Publishers | Privacy Policy