MicroRNAs as Potential Diagnostic and Prognostic Biomarkers in Hepatocellular Carcinoma

Author(s): Seyed Mostafa Parizadeh , Reza Jafarzadeh-Esfehani , Maryam Ghandehari , Fatemeh Goldani , Seyed Mohammad Reza Parizadeh , Seyed Mahdi Hassanian , Majid Ghayour-Mobarhan , Gordon A. Ferns , Amir Avan* .

Journal Name: Current Drug Targets

Volume 20 , Issue 11 , 2019

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Abstract:

Hepatocellular carcinoma (HCC) is a common cancer, and the second most common cause of cancer-associated death globally. One of the major reasons for this high rate of mortality is a failure to make an early diagnosis. The average survival in untreated HCC patients is estimated to be approximately three months. The 5-year overall survival rate after radical resection is about 15-40% and within two years, more than two third of patients experience a relapse. To date, the most common biomarker which has been used for the diagnosis of HCC is serum alpha-fetoprotein (AFP). However, there is a lack of sensitive and specific tumor biomarkers for the early diagnosis of HCC. MicroRNAs are a class of short endogenous RNA with crucial role in many biological activities and cellular pathways and can be found in various tissues and body fluids. The aim of this review was to summarize the results of recent studies investigating miRNAs as novel biomarkers for the early diagnosis and prognostic risk stratification of patients with this type of liver cancer.

Keywords: microRNA, hepatocellular carcinoma, liver cancer, diagnosis, prognosis, tumor biomarkers.

[1]
Li S, Li T, Li X, et al. MicroRNA-32 regulates development and progression of hepatocellular carcinoma by targeting adamts9 and affects its prognosis. Med Sci Monit Basic Res 2018; 24: 177-87.
[http://dx.doi.org/10.12659/MSMBR.910522] [PMID: 30393368]
[2]
Ding W, Tan H, Li X, et al. MicroRNA-493 suppresses cell proliferation and invasion by targeting ZFX in human hepatocellular carcinoma. Cancer Biomark 2018; 22(3): 427-34.
[http://dx.doi.org/10.3233/CBM-171036] [PMID: 29758928]
[3]
Xie RT, Cong XL, Zhong XM, et al. MicroRNA-33a downregulation is associated with tumorigenesis and poor prognosis in patients with hepatocellular carcinoma. Oncol Lett 2018; 15(4): 4571-7.
[http://dx.doi.org/10.3892/ol.2018.7892] [PMID: 29541227]
[4]
Tao J, Liu Z, Wang Y, et al. MicroRNA-645 represses hepatocellular carcinoma progression by inhibiting SOX30-mediated p53 transcriptional activation. Int J Biol Macromol 2019; 121: 214-22.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.10.032] [PMID: 30312695]
[5]
Kulik L, El-Serag HB. Epidemiology and Management of Hepatocellular Carcinoma. Gastroenterology 2019; 156(2): 477-491.e1.
[http://dx.doi.org/10.1053/j.gastro.2018.08.065] [PMID: 30367835]
[6]
An Y, Gao S, Zhao W-C, et al. Novel serum microRNAs panel on the diagnostic and prognostic implications of hepatocellular carcinoma. World J Gastroenterol 2018; 24(24): 2596-604.
[http://dx.doi.org/10.3748/wjg.v24.i24.2596] [PMID: 29962816]
[7]
Wang F, Dai M, Chen H, et al. Prognostic value of hsa-mir-299 and hsa-mir-7706 in hepatocellular carcinoma. Oncol Lett 2018; 16(1): 815-20.
[http://dx.doi.org/10.3892/ol.2018.8710] [PMID: 29963149]
[8]
Wu X-M, Xi Z-F, Liao P, et al. Diagnostic and prognostic potential of serum microRNA-4651 for patients with hepatocellular carcinoma related to aflatoxin B1. Oncotarget 2017; 8(46): 81235-49.
[http://dx.doi.org/10.18632/oncotarget.16027] [PMID: 29113383]
[9]
Parizadeh SM, Ghandehari M, Heydari-Majd M, et al. Toll-like receptors signaling pathways as a potential therapeutic target in cardiovascular disease. Curr Pharm Des 2018; 24(17): 1887-98.
[http://dx.doi.org/10.2174/1381612824666180614090224] [PMID: 29898648]
[10]
Baffy G. MicroRNAs in nonalcoholic fatty liver disease. J Clin Med 2015; 4(12): 1977-88.
[http://dx.doi.org/10.3390/jcm4121953] [PMID: 26690233]
[11]
Wong C-M, Tsang FH-C, Ng IO-L. Non-coding RNAs in hepatocellular carcinoma: Molecular functions and pathological implications. Nat Rev Gastroenterol Hepatol 2018; 15(3): 137-51.
[http://dx.doi.org/10.1038/nrgastro.2017.169] [PMID: 29317776]
[12]
Parizadeh SM, Ferns GA, Ghandehari M, et al. The diagnostic and prognostic value of circulating microRNAs in coronary artery disease: A novel approach to disease diagnosis of stable CAD and acute coronary syndrome. J Cell Physiol 2018; 233(9): 6418-24.
[http://dx.doi.org/10.1002/jcp.26324] [PMID: 29215707]
[13]
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]
[14]
Wang F, Wang J, Ju L, Chen L, Cai W, Yang J. Diagnostic and prognostic potential of serum miR-132/212 cluster in patients with hepatocellular carcinoma. Ann Clin Biochem 2018; 55(5): 576-82.
[http://dx.doi.org/10.1177/0004563218755815] [PMID: 29357677]
[15]
Ji J, Yamashita T, Budhu A, Forgues M, Jia HL, Li C, et al. Identification of microRNA‐181 by genome‐wide screening as a critical player in EpCAM-positive hepatic cancer stem cells 50(2): 472-80.
[http://dx.doi.org/10.1002/hep.22989]
[16]
Mohamed AA, Ali-Eldin ZA, Elbedewy TA, El-Serafy M, Ali-Eldin FA. AbdelAziz HJWjoh MicroRNAs and clinical implications in hepatocellular carcinoma. 2017; 9: p. (23)101.
[17]
Motawi TK, Shaker OG, El-Maraghy SA. Senousy MAJPo Serum microRNAs as potential biomarkers for early diagnosis of hepatitis C virus-related hepatocellular carcinoma in Egyptian patients. 2015; 10: p. (9)e0137706.
[18]
Elemeery MN, Badr AN, Mohamed MA. Ghareeb DAJWjog Validation of a serum microRNA panel as biomarkers for early diagnosis of hepatocellular carcinoma post-hepatitis C infection in Egyptian patients. 2017; 23: p. (21)3864.
[19]
Totoki Y, Tatsuno K, Yamamoto S, Arai Y, Hosoda F, Ishikawa S, et al. High-resolution characterization of a hepatocellular carcinoma genome 2011; 43: p. (5)464
[http://dx.doi.org/10.1038/ng.804]
[20]
Moinzadeh P, Breuhahn K, Stützer H. Schirmacher PJBjoc Chromosome alterations in human hepatocellular carcinomas correlate with aetiology and histological grade-results of an explorative CGH meta-analysis . 2005; 92: p. (5)935.
[21]
Chang J, Guo J-T, Jiang D, Guo H, Taylor JM. Liver-specific microRNA miR-122 enhances the replication of hepatitis C virus in nonhepatic cells. 2008; 82: pp. (16)8215.-23.
[22]
Lu Y-L, Yao J-G, Huang X-Y, Wang C, Wu X-M, Xia Q, et al. Prognostic significance of miR-1268a expression and its beneficial effects for post-operative adjuvant transarterial chemoembolization in hepatocellular carcinoma 2016; 82: p. (6)36104
[http://dx.doi.org/10.1038/srep36104]
[23]
Braconi C, Henry JC, Kogure T, Schmittgen T, Patel T, Eds. The role of microRNAs in human liver cancers Seminars in oncology. Elsevier 2011.
[24]
Negrini M, Gramantieri L, Sabbioni S. M Croce CJA-CAiMC. microRNA involvement in hepatocellular carcinoma, 2011; 11(6): 500-21.
[25]
Long X-R, Zhang Y-J, Zhang M-Y, Chen K, Zheng XS, Wang H-YJA. Identification of an 88-microRNA signature in whole blood for diagnosis of hepatocellular carcinoma and other chronic liver diseases. 2017; 9: p. (6)1565.
[26]
Wu L, Yang F, Lin B, et al. MicroRNA-424 expression predicts tumor recurrence in patients with hepatocellular carcinoma following liver transplantation. Oncol Lett 2018; 15(6): 9126-32.
[http://dx.doi.org/10.3892/ol.2018.8539] [PMID: 29805644]
[27]
Luo J, Chen M, Huang H, Yuan T, Zhang M, Zhang K, et al. Circulating microRNA-122a as a diagnostic marker for hepatocellular carcinoma 2013; 6(577)
[28]
Yu F, Lu Z, Chen B, Dong P. Zheng JJDp. microRNA-150: A promising novel biomarker for hepatitis B virus-related hepatocellular carcinoma 2015; 10(1): 129.
[29]
Liao Q, Han P, Huang Y, Wu Z, Chen Q, Li S, et al. Potential role of circulating microRNA-21 for hepatocellular carcinoma diagnosis: A meta-analysis 2015 10: p (6)e0130677
[http://dx.doi.org/10.1371/journal.pone.0130677]
[30]
Zhou J, Yu L, Gao X, Hu J, Wang J, Dai Z, et al. Plasma microRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma 2011 29(36): 4781-8
[http://dx.doi.org/10.1177/0004563218755815]
[31]
Wu X-M, Xi Z-F, Liao P, Huang H-D, Huang X-Y, Wang C, et al. Diagnostic and prognostic potential of serum microRNA-4651 for patients with hepatocellular carcinoma related to aflatoxin B1 2017; 8(46): 81235
[http://dx.doi.org/10.18632/oncotarget.16027]
[32]
Chen L, Chu F, Cao Y, Shao J, Wang FJTB. Serum miR-182 and miR-331-3p as diagnostic and prognostic markers in patients with hepatocellular carcinoma 2015; 36(10): 7439-47
[http://dx.doi.org/10.1007/s13277-015-3430-2]
[33]
Zhang Z-q, Meng H, Wang N, et al. Serum microRNA 143 and microRNA 215 as potential biomarkers for the diagnosis of chronic hepatitis and hepatocellular carcinoma 2014; 9(1): 135
[http://dx.doi.org/10.1186/1746-1596-9-135]
[34]
Xiao C-Z, Wei W, Guo Z-X, Zhang M-Y, Zhang Y-F, Wang J-H, et al. MicroRNA-34c-3p promotes cell proliferation and invasion in hepatocellular carcinoma by regulation of NCKAP1 expression 2017; 143(2): 262-73
[35]
Zhang Y, Wei C, Guo C-C, Bi R-X, Xie J, Guan D-H, et al. Prognostic value of microRNAs in hepatocellular carcinoma: A meta-analysis 2017; 8(63): 107237
[http://dx.doi.org/10.18632/oncotarget.20883]
[36]
Mohamed AA, Ali-Eldin ZA, Elbedewy TA, El-Serafy M, Ali-Eldin FA, AbdelAziz H. MicroRNAs and clinical implications in hepatocellular carcinoma. World J Hepatol 2017; 9(23): 1001-7.
[http://dx.doi.org/10.4254/wjh.v9.i23.1001] [PMID: 28878865]
[37]
Motawi TK, Shaker OG, El-Maraghy SA, Senousy MA. Serum microRNAs as potential biomarkers for early diagnosis of hepatitis C virus-related hepatocellular carcinoma in Egyptian patients. PLoS One 2015; 10(9)e0137706
[http://dx.doi.org/10.1371/journal.pone.0137706] [PMID: 26352740]
[38]
Liao Q, Han P, Huang Y, et al. Potential role of circulating microRNA-21 for hepatocellular carcinoma diagnosis: A meta-analysis. PLoS One 2015; 10(6)e0130677
[http://dx.doi.org/10.1371/journal.pone.0130677] [PMID: 26114756]
[39]
Zhu HT, Liu RB, Liang YY, et al. Serum microRNA profiles as diagnostic biomarkers for HBV-positive hepatocellular carcinoma. Liver Int 2017; 37(6): 888-96.
[http://dx.doi.org/10.1111/liv.13356] [PMID: 28061012]
[40]
Zhang Y, Li T, Qiu Y, et al. Serum microRNA panel for early diagnosis of the onset of hepatocellular carcinoma. Medicine (Baltimore) 2017; 96(2)e5642
[http://dx.doi.org/10.1097/MD.0000000000005642] [PMID: 28079796]
[41]
Chen Y, Dong X, Yu D, Wang X. Serum miR-96 is a promising biomarker for hepatocellular carcinoma in patients with chronic hepatitis B virus infection. Int J Clin Exp Med 2015; 8(10): 18462-8.
[PMID: 26770453]
[42]
Yang X, Pang YY, He RQ, et al. Diagnostic value of strand-specific miRNA-101-3p and miRNA-101-5p for hepatocellular carcinoma and a bioinformatic analysis of their possible mechanism of action. FEBS Open Bio 2017; 8(1): 64-84.
[http://dx.doi.org/10.1002/2211-5463.12349] [PMID: 29321958]
[43]
Luo J, Chen M, Huang H, et al. Circulating microRNA-122a as a diagnostic marker for hepatocellular carcinoma. OncoTargets Ther 2013; 6: 577-83.
[PMID: 23723713]
[44]
Elemeery MN, Badr AN, Mohamed MA, Ghareeb DA. Validation of a serum microRNA panel as biomarkers for early diagnosis of hepatocellular carcinoma post-hepatitis C infection in Egyptian patients. World J Gastroenterol 2017; 23(21): 3864-75.
[http://dx.doi.org/10.3748/wjg.v23.i21.3864] [PMID: 28638226]
[45]
Zhang J, Lin H, Wang X-Y, et al. Predictive value of microRNA-143 in evaluating the prognosis of patients with hepatocellular carcinoma. Cancer Biomark 2017; 19(3): 257-62.
[http://dx.doi.org/10.3233/CBM-160357] [PMID: 28436387]
[46]
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(1): 135.
[http://dx.doi.org/10.1186/1746-1596-9-135] [PMID: 24993656]
[47]
Yu F, Lu Z, Chen B, Dong P, Zheng J. microRNA-150: A promising novel biomarker for hepatitis B virus-related hepatocellular carcinoma. Diagn Pathol 2015; 10(1): 129.
[http://dx.doi.org/10.1186/s13000-015-0369-y] [PMID: 26215970]
[48]
Chen L, Chu F, Cao Y, Shao J, Wang F. Serum miR-182 and miR-331-3p as diagnostic and prognostic markers in patients with hepatocellular carcinoma. Tumour Biol 2015; 36(10): 7439-47.
[http://dx.doi.org/10.1007/s13277-015-3430-2] [PMID: 25903466]
[49]
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]
[50]
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]
[51]
Long X-R, Zhang Y-J, Zhang M-Y, Chen K, Zheng XFS, Wang H-Y. Identification of an 88-microRNA signature in whole blood for diagnosis of hepatocellular carcinoma and other chronic liver diseases. Aging (Albany NY) 2017; 9(6): 1565-84.
[http://dx.doi.org/10.18632/aging.101253] [PMID: 28657540]
[52]
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]
[53]
Murakami Y, Tamori A, Itami S, et al. The expression level of miR-18b in hepatocellular carcinoma is associated with the grade of malignancy and prognosis. BMC Cancer 2013; 13(1): 99.
[http://dx.doi.org/10.1186/1471-2407-13-99] [PMID: 23496901]
[54]
Lee YR, Kim G, Tak WY, Jang SY, Kweon YO, Park JG, et al. Circulating exosomal non‐coding RNAs as prognostic biomarkers in human hepatocellular carcinoma. Int J Cancer 2018.
[55]
Wang X, Zhang J, Zhou L, et al. Significance of serum microRNA-21 in diagnosis of hepatocellular carcinoma (HCC): Clinical analyses of patients and an HCC rat model. Int J Clin Exp Pathol 2015; 8(2): 1466-78.
[PMID: 25973032]
[56]
Cao J, Liu J, Long J, et al. microRNA-23b suppresses epithelial-mesenchymal transition (EMT) and metastasis in hepatocellular carcinoma via targeting Pyk2. Biomed Pharmacother 2017; 89: 642-50.
[http://dx.doi.org/10.1016/j.biopha.2017.02.030] [PMID: 28262617]
[57]
Yang H, Li Y, Zhong X, et al. Upregulation of microRNA-32 is associated with tumorigenesis and poor prognosis in patients with hepatocellular carcinoma. Oncol Lett 2018; 15(4): 4097-104.
[http://dx.doi.org/10.3892/ol.2018.7879] [PMID: 29541175]
[58]
Fu X, Liu M, Qu S, et al. Exosomal microRNA-32-5p induces multidrug resistance in hepatocellular carcinoma via the PI3K/Akt pathway. J Exp Clin Cancer Res 2018; 37(1): 52.
[http://dx.doi.org/10.1186/s13046-018-0677-7] [PMID: 29530052]
[59]
Xiao C-Z, Wei W, Guo Z-X, et al. MicroRNA-34c-3p promotes cell proliferation and invasion in hepatocellular carcinoma by regulation of NCKAP1 expression. J Cancer Res Clin Oncol 2017; 143(2): 263-73.
[http://dx.doi.org/10.1007/s00432-016-2280-7] [PMID: 27704267]
[60]
Ma Y-S, Wu T-M, Lv Z-W, et al. High expression of miR-105-1 positively correlates with clinical prognosis of hepatocellular carcinoma by targeting oncogene NCOA1. Oncotarget 2017; 8(7): 11896-905.
[http://dx.doi.org/10.18632/oncotarget.14435] [PMID: 28060733]
[61]
Jin Y, Wang J, Han J, Luo D, Sun Z. MiR-122 inhibits epithelial-mesenchymal transition in hepatocellular carcinoma by targeting Snail1 and Snail2 and suppressing WNT/β-cadherin signaling pathway. Exp Cell Res 2017; 360(2): 210-7.
[http://dx.doi.org/10.1016/j.yexcr.2017.09.010] [PMID: 28890291]
[62]
Cho HJ, Kim JK, Nam JS, et al. High circulating microRNA-122 expression is a poor prognostic marker in patients with hepatitis B virus-related hepatocellular carcinoma who undergo radiofrequency ablation. Clin Biochem 2015; 48(16-17): 1073-8.
[http://dx.doi.org/10.1016/j.clinbiochem.2015.06.019] [PMID: 26129878]
[63]
Long H-D, Ma Y-S, Yang H-Q, et al. Reduced hsa-miR-124-3p levels are associated with the poor survival of patients with hepatocellular carcinoma. Mol Biol Rep 2018; 45(6): 2615-23.
[http://dx.doi.org/10.1007/s11033-018-4431-1] [PMID: 30341691]
[64]
Wang X, Zeng J, Wang L, et al. Overexpression of microRNA-133b is associated with the increased survival of patients with hepatocellular carcinoma after curative hepatectomy: Involvement of the EGFR/PI3K/Akt/mTOR signaling pathway. Oncol Rep 2017; 38(1): 141-50.
[http://dx.doi.org/10.3892/or.2017.5699] [PMID: 28586051]
[65]
Chen J, Yu Y, Xue C, et al. Low microRNA-139 expression associates with poor prognosis in patients with tumors: A meta-analysis HBPD INT 2018S1499-3872(18)30206-6 [http://dx.doi.org/10.1016/j.hbpd.2018.09.016] [PMID: 30290990]
[66]
Hua S, Lei L, Deng L, et al. miR-139-5p inhibits aerobic glycolysis, cell proliferation, migration, and invasion in hepatocellular carcinoma via a reciprocal regulatory interaction with ETS1. Oncogene 2018; 37(12): 1624-36.
[http://dx.doi.org/10.1038/s41388-017-0057-3] [PMID: 29335523]
[67]
Duan F, Liu W, Fu X, et al. Evaluating the prognostic value of miR-148/152 family in cancers: Based on a systemic review of observational studies. Oncotarget 2017; 8(44): 77999-8010.
[http://dx.doi.org/10.18632/oncotarget.20830] [PMID: 29100442]
[68]
Luo G, Chao Y-L, Tang B, et al. miR-149 represses metastasis of hepatocellular carcinoma by targeting actin-regulatory proteins PPM1F. Oncotarget 2015; 6(35): 37808-23.
[http://dx.doi.org/10.18632/oncotarget.5676] [PMID: 26498692]
[69]
Cao M-Q, You A-B, Zhu X-D, et al. miR-182-5p promotes hepatocellular carcinoma progression by repressing FOXO3a. J Hematol Oncol 2018; 11(1): 12.
[http://dx.doi.org/10.1186/s13045-018-0555-y] [PMID: 29361949]
[70]
Zhang Q, Chen Y, Liu K. miR-185 inhibits cell migration and invasion of hepatocellular carcinoma through CDC42. Oncol Lett 2018; 16(3): 3101-7.
[http://dx.doi.org/10.3892/ol.2018.8971] [PMID: 30127901]
[71]
Yu S, Jing L, Yin X-R, et al. MiR-195 suppresses the metastasis and epithelial-mesenchymal transition of hepatocellular carcinoma by inhibiting YAP. Oncotarget 2017; 8(59): 99757-71.
[http://dx.doi.org/10.18632/oncotarget.20909] [PMID: 29245938]
[72]
Tsai SC, Lin CC, Shih TC, et al. The miR-200b-ZEB1 circuit regulates diverse stemness of human hepatocellular carcinoma. Mol Carcinog 2017; 56(9): 2035-47.
[http://dx.doi.org/10.1002/mc.22657] [PMID: 28383782]
[73]
Yang Y, Zhang J, Xia T, et al. MicroRNA-210 promotes cancer angiogenesis by targeting fibroblast growth factor receptor-like 1 in hepatocellular carcinoma. Oncol Rep 2016; 36(5): 2553-62.
[http://dx.doi.org/10.3892/or.2016.5129] [PMID: 27666683]
[74]
Feng Y, Duan F, Liu W, Fu X, Cui S, Yang Z. Prognostic value of the microRNA-214 in multiple human cancers: A meta-analysis of observational studies. Oncotarget 2017; 8(43): 75350-60.
[http://dx.doi.org/10.18632/oncotarget.17642] [PMID: 29088870]
[75]
Li Y, Li Y, Chen Y, et al. MicroRNA-214-3p inhibits proliferation and cell cycle progression by targeting MELK in hepatocellular carcinoma and correlates cancer prognosis. Cancer Cell Int 2017; 17(1): 102.
[http://dx.doi.org/10.1186/s12935-017-0471-1] [PMID: 29151817]
[76]
Wang L, Wang YM, Xu S, et al. MicroRNA-215 is upregulated by treatment with Adriamycin and leads to the chemoresistance of hepatocellular carcinoma cells and tissues. Mol Med Rep 2015; 12(4): 5274-80.
[http://dx.doi.org/10.3892/mmr.2015.4012] [PMID: 26135967]
[77]
Yang J, Sheng Y-Y, Wei J-W, Gao X-M, Zhu Y, Jia H-L, et al. MicroRNA-219-5p Promotes tumor growth and metastasis of hepatocellular carcinoma by regulating cadherin 1. BioMed research international, 2018; 2018
[78]
Chen F, Li X-F, Fu D-S, Huang J-G, Yang S-E. Clinical potential of miRNA-221 as a novel prognostic biomarker for hepatocellular carcinoma. Cancer Biomark 2017; 18(2): 209-14.
[http://dx.doi.org/10.3233/CBM-161671] [PMID: 27983537]
[79]
Li F, Wang F, Zhu C, Wei Q, Zhang T, Zhou YL. miR-221 suppression through nanoparticle-based miRNA delivery system for hepatocellular carcinoma therapy and its diagnosis as a potential biomarker. Int J Nanomedicine 2018; 13: 2295-307.
[http://dx.doi.org/10.2147/IJN.S157805] [PMID: 29713162]
[80]
Hu X, Feng Y, Sun L, Qu L, Sun C. Roles of microrna-330 and its target gene ing4 in the development of aggressive phenotype in hepatocellular carcinoma cells. Dig Dis Sci 2017; 62(3): 715-22.
[http://dx.doi.org/10.1007/s10620-016-4429-2] [PMID: 28050784]
[81]
Hu J, Ruan J, Liu X, Xiao C, Xiong J. MicroRNA-301a-3p suppressed the progression of hepatocellular carcinoma via targeting VGLL4. Pathol Res Pract 2018; 214(12): 2039-45.
[http://dx.doi.org/10.1016/j.prp.2018.09.008] [PMID: 30322806]
[82]
Ma Y-S, Lv Z-W, Yu F, et al. MicroRNA-302a/d inhibits the self-renewal capability and cell cycle entry of liver cancer stem cells by targeting the E2F7/AKT axis. J Exp Clin Cancer Res 2018; 37(1): 252.
[http://dx.doi.org/10.1186/s13046-018-0927-8] [PMID: 30326936]
[83]
Chen YL, Xu QP, Guo F, Guan WH. MicroRNA-302d downregulates TGFBR2 expression and promotes hepatocellular carcinoma growth and invasion. Exp Ther Med 2017; 13(2): 681-7.
[http://dx.doi.org/10.3892/etm.2016.3970] [PMID: 28352351]
[84]
Zhang H, Liu H, Bi H. MicroRNA-345 inhibits hepatocellular carcinoma metastasis by inhibiting YAP1. Oncol Rep 2017; 38(2): 843-9.
[http://dx.doi.org/10.3892/or.2017.5772] [PMID: 28677785]
[85]
Guo Z, Li J, Sun J, Sun L, Zhou Y, Yu Z. miR-346 promotes HCC progression by suppressing breast cancer metastasis suppressor 1 expression. Oncol Res 2018; 26(7): 1073-81.
[http://dx.doi.org/10.3727/096504017X15145088802439] [PMID: 29295726]
[86]
Zhang J, Fan J, Zhou C, Qi Y. miR-363-5p as potential prognostic marker for hepatocellular carcinoma indicated by weighted co-expression network analysis of miRNAs and mRNA. BMC Gastroenterol 2017; 17(1): 81.
[http://dx.doi.org/10.1186/s12876-017-0637-2] [PMID: 28637446]
[87]
Lin Y, Liu J, Huang Y, Liu D, Zhang G, Kan H. MicroRNA-489 plays an anti-metastatic role in human hepatocellular carcinoma by targeting matrix metalloproteinase-7. Transl Oncol 2017; 10(2): 211-20.
[http://dx.doi.org/10.1016/j.tranon.2017.01.010] [PMID: 28189067]
[88]
Bao L, Zhang M, Han S, et al. MicroRNA-500a promotes the progression of hepatocellular carcinoma by post-transcriptionally targeting BID. Cell Physiol Biochem 2018; 47(5): 2046-55.
[http://dx.doi.org/10.1159/000491472] [PMID: 29969781]
[89]
Guo Y, Chen L, Sun C, Yu C. MicroRNA-500a promotes migration and invasion in hepatocellular carcinoma by activating the Wnt/β-catenin signaling pathway. Biomed Pharmacother 2017; 91: 13-20.
[http://dx.doi.org/10.1016/j.biopha.2017.04.018] [PMID: 28437633]
[90]
Luo C, Yin D, Zhan H, et al. microRNA-501-3p suppresses metastasis and progression of hepatocellular carcinoma through targeting LIN7A. Cell Death Dis 2018; 9(5): 535.
[http://dx.doi.org/10.1038/s41419-018-0577-y] [PMID: 29749382]
[91]
Liu X, Yang L, Tu J, et al. microRNA-526b servers as a prognostic factor and exhibits tumor suppressive property by targeting Sirtuin 7 in hepatocellular carcinoma. Oncotarget 2017; 8(50): 87737-49.
[http://dx.doi.org/10.18632/oncotarget.21209] [PMID: 29152116]
[92]
Zhang T, Liu W, Meng W, et al. Downregulation of miR-542-3p promotes cancer metastasis through activating TGF-β/Smad signaling in hepatocellular carcinoma. OncoTargets Ther 2018; 11: 1929-39.
[http://dx.doi.org/10.2147/OTT.S154416] [PMID: 29670368]
[93]
Ge X, Gong L. MiR-590-3p suppresses hepatocellular carcinoma growth by targeting TEAD1. Tumour Biol 2017; 39(3)1010428317695947
[http://dx.doi.org/10.1177/1010428317695947] [PMID: 28349829]
[94]
Zhang D, Zhou P, Wang W, et al. MicroRNA-616 promotes the migration, invasion and epithelial-mesenchymal transition of HCC by targeting PTEN. Oncol Rep 2016; 35(1): 366-74.
[http://dx.doi.org/10.3892/or.2015.4334] [PMID: 26499912]
[95]
Song W-H, Feng X-J, Gong S-J, et al. microRNA-622 acts as a tumor suppressor in hepatocellular carcinoma. Cancer Biol Ther 2015; 16(12): 1754-63.
[http://dx.doi.org/10.1080/15384047.2015.1095402] [PMID: 26467022]
[96]
Chen WX, Zhang ZG, Ding ZY, et al. MicroRNA-630 suppresses tumor metastasis through the TGF-β- miR-630-Slug signaling pathway and correlates inversely with poor prognosis in hepatocellular carcinoma. Oncotarget 2016; 7(16): 22674-86.
[http://dx.doi.org/10.18632/oncotarget.8047] [PMID: 26993767]
[97]
Ye W, Li J, Fang G, et al. Expression of microRNA 638 and sex-determining region Y-box 2 in hepatocellular carcinoma: Association between clinicopathological features and prognosis. Oncol Lett 2018; 15(5): 7255-64.
[http://dx.doi.org/10.3892/ol.2018.8208] [PMID: 29731884]
[98]
Sun D, Lu J, Hu C, et al. Prognostic role of miR-760 in hepatocellular carcinoma. Oncol Lett 2018; 16(6): 7239-44.
[http://dx.doi.org/10.3892/ol.2018.9546] [PMID: 30546462]
[99]
Yang C, Ma X, Guan G, Liu H, Yang Y, Niu Q, et al. MicroRNA-766 promotes cancer progression by targeting NR3C2 in hepatocellular carcinoma. The FASEB Journal 2018 fj 201801151R 13(1): 1456-67.
[100]
You Y, Que K, Zhou Y, et al. MicroRNA-766-3p inhibits tumour progression by targeting Wnt3a in hepatocellular carcinoma. Mol Cells 2018; 41(9): 830-41.
[PMID: 30145863]
[101]
Lu Y-L, Yao J-G, Huang X-Y, et al. Prognostic significance of miR-1268a expression and its beneficial effects for post-operative adjuvant transarterial chemoembolization in hepatocellular carcinoma. Sci Rep 2016; 6: 36104.
[http://dx.doi.org/10.1038/srep36104] [PMID: 27796321]
[102]
Xu Q, Liu X, Liu Z, et al. MicroRNA-1296 inhibits metastasis and epithelial-mesenchymal transition of hepatocellular carcinoma by targeting SRPK1-mediated PI3K/AKT pathway. Mol Cancer 2017; 16(1): 103.
[http://dx.doi.org/10.1186/s12943-017-0675-y] [PMID: 28606154]
[103]
Hu T, Li J, Zhang C, et al. The potential value of microRNA-4463 in the prognosis evaluation in hepatocellular carcinoma. Genes Dis 2017; 4(2): 116-22.
[http://dx.doi.org/10.1016/j.gendis.2017.03.003] [PMID: 30258914]
[104]
Shi W, Zhang Z, Yang B, et al. Overexpression of microRNA let-7 correlates with disease progression and poor prognosis in hepatocellular carcinoma. Medicine (Baltimore) 2017; 96(32)e7764
[http://dx.doi.org/10.1097/MD.0000000000007764] [PMID: 28796071]
[105]
Wang X, Zeng J, Wang L, et al. Overexpression of microRNA- 133b is associated with the increased survival of patients with hepatocellular carcinoma after curative hepatectomy: Involvement of the EGFR/PI3K/Akt/mTOR signaling pathway 2017; 38(1): 140-50.
[106]
Ni H, Dai X, Leng X, et al. Higher variety and quantity of microRNA‐139‐5p isoforms confer suppressive role in hepatocellular carcinoma 2018.
[http://dx.doi.org/10.1002/jcb.26874]
[107]
Chen YL, Xu QP, Guo F, Guan WHJE. medicine t. MicroRNA- 302d downregulates TGFBR2 expression and promotes hepatocellular carcinoma growth and invasion 2017; 13(2): 681-7.
[108]
Zhang J, Fan J, Zhou C. Qi YJBg. miR-363-5p as potential prognostic marker for hepatocellular carcinoma indicated by weighted co-expression network analysis of miRNAs and mRNA, 2017; 17(1): 81.
[109]
Sun D, Lu J, Hu C, et al. Prognostic role of miR-760 in hepatocellular carcinoma 2018; 16(6): 7239-44.
[http://dx.doi.org/10.3892/ol.2018.9546]


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VOLUME: 20
ISSUE: 11
Year: 2019
Page: [1129 - 1140]
Pages: 12
DOI: 10.2174/1389450120666190307095720
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