Research Article

The Computational Analysis of Single Nucleotide Associated with MicroRNA Affecting Hepatitis B Infection

Author(s): Mirza Ali Nazarnezhad, Mahdi Barazesh*, Soudabeh Kavousipour*, Shiva Mohammadi, Ebrahim Eftekhar and Sajad Jalili

Volume 11, Issue 2, 2022

Published on: 04 August, 2022

Page: [139 - 162] Pages: 24

DOI: 10.2174/2211536611666220509103724

Price: $65

Abstract

Background: MicroRNAs (miRNAs) have a pivotal role in Hepatitis B Virus (HBV) infection and its complications by targeting the cellular transcription factors required for gene expression or directly binding to HBV transcripts. Single Nucleotide Polymorphisms (SNPs) in miRNA genes affect their expression and the regulation of target genes, clinical course, diagnosis, and therapeutic interventions of HBV infection.

Methods: Computational assessment and cataloging of miRNA gene polymorphisms targeting mRNA transcripts straightly or indirectly through the regulation of hepatitis B infection by annotating the functional impact of SNPs on mRNA-miRNA and miRNA-RBS (miRNA binding sites) interaction were screened by applying various universally available datasets such as the miRNA SNP3.0 software.

Results: 2987 SNPs were detected in 139 miRNAs affecting hepatitis B infection. Among them, 313 SNPs were predicted to have a significant role in the progression of hepatitis B infection. The computational analysis also revealed that 45 out of the 313 SNPs were located in the seed region and were more important than others. Has-miR-139-3p had the largest number of SNPs in the seed region (n=6). On the other hand, proteoglycans in cancer, adherens junction, lysine degradation, NFkappa B signaling cascade, ECM-receptor binding, viral carcinogenesis, fatty acid metabolism, TGF-beta signaling pathway, p53 signaling pathway, immune evasion related pathways, and fatty acid biosynthesis were the most important pathways affected by these 139 miRNAs.

Conclusion: The results revealed 45 SNPs in the seed region of 25 miRNAs as the catalog in miRNA genes that regulated the hepatitis B infection. The results also showed the most important pathways regulated by these miRNAs that can be targeted for therapeutic purposes.

Keywords: Hepatitis B, hepatocellular carcinoma, single nucleotide polymorphisms, microRNA, cellular transcription, biosynthesis.

Graphical Abstract

[1]
Liu, C.; Yu, S.; Lavker, R.M.; Cai, L.; Liu, W. MicroRNA-21 acts as an oncomir through multiple targets in human hepatocellular carcinoma. J. Hepatol., 2010, 53, 98-107.
[2]
Lamontagne, J.; Steel, L.F.; Bouchard, M.J. Hepatitis B virus and microRNAs: Complex interactions affecting hepatitis B virus replication and hepatitis B virus-associated diseases. World J. Gastroenterol., 2015, 21(24), 7375-7399.
[http://dx.doi.org/10.3748/wjg.v21.i24.7375] [PMID: 26139985]
[3]
Liu, W.H.; Yeh, S.H.; Chen, P.J. Role of microRNAs in hepatitis B virus replication and pathogenesis. Biochim Biophys Acta (BBA) -. Gene Regulatory Mechanisms, 2011, 1809(11), 678-685.
[http://dx.doi.org/10.1016/j.bbagrm.2011.04.008]
[4]
Sartorius, K.; Makarova, J.; Sartorius, B. The regulatory role of microRNA in hepatitis-B virus-associated hepatocellular carcinoma (HBV-HCC) pathogenesis. Cells, 2019, 8(12), E1504.
[http://dx.doi.org/10.3390/cells8121504] [PMID: 31771261]
[5]
Wang, X.W.; Heegaard, N.H.; Orum, H. MicroRNAs in liver disease. Gastroenterology, 2012, 142(7), 1431-1443.
[http://dx.doi.org/10.1053/j.gastro.2012.04.007] [PMID: 22504185]
[6]
Fu, X.; Wen, H.; Jing, L. MicroRNA-155-5p promotes hepatocellular carcinoma progression by suppressing PTEN through the PI3K/Akt pathway. Cancer Sci., 2017, 108(4), 620-631.
[http://dx.doi.org/10.1111/cas.13177] [PMID: 28132399]
[7]
Yu, G.; Chen, X.; Chen, S.; Ye, W.; Hou, K.; Liang, M. MiR-19a, miR-122 and miR-223 are differentially regulated by hepatitis B virus X protein and involve in cell proliferation in hepatoma cells. J. Transl. Med., 2016, 14(1), 122.
[http://dx.doi.org/10.1186/s12967-016-0888-7] [PMID: 27150195]
[8]
Ivashchenko, A.; Berillo, O.; Pyrkova, A.; Niyazova, R. Binding sites of miR-1273 family on the mRNA of target genes. BioMed Res. Int., 2014, 2014, 620530.
[http://dx.doi.org/10.1155/2014/620530] [PMID: 25243165]
[9]
Al-Qahtani, A.A.; Al-Anazi, M.R.; Nazir, N. Association of single nucleotide polymorphisms in microRNAs with susceptibility to hepatitis B virus infection and HBV-related liver complications: A study in a Saudi Arabian population. J. Viral Hepat., 2017, 24(12), 1132-1142.
[http://dx.doi.org/10.1111/jvh.12749] [PMID: 28685993]
[10]
Liu, Y.; Xie, K.; Wen, J.; Deng, M.; Li, J.; Hu, Z. A genetic variant in microRNA-122 regulatory region confers risk for chronic hepatitis B virus infection and hepatocellular carcinoma in Han Chinese. J. Med. Virol., 2014, 86(10), 1669-1674.
[http://dx.doi.org/10.1002/jmv.23996] [PMID: 24995424]
[11]
Bei, C.; Liu, S.; Yu, X. Single nucleotide polymorphisms in mir-122 are associated with the risk of hepatocellular carcinoma in a southern Chinese population. BioMed Res. Int., 2018, 2018, 1540201.
[12]
Ellwanger, J.H.; Zambra, F.M.B.; Guimarães, R.L.; Chies, J.A.B. MicroRNA-related polymorphisms in infectious diseases-tiny changes with a huge impact on viral infections and potential clinical applications. Front. Immunol., 2018, 9, 1316.
[http://dx.doi.org/10.3389/fimmu.2018.01316] [PMID: 29963045]
[13]
Farokhizadeh, Z.; Dehbidi, S.; Geramizadeh, B. Association of MicroRNA polymorphisms with hepatocellular carcinoma in an Iranian population. Ann. Lab. Med., 2019, 39(1), 58-66.
[http://dx.doi.org/10.3343/alm.2019.39.1.58]
[14]
Xing, T.J.; Jiang, D.F.; Huang, J.X.; Xu, Z.L. Expression and clinical significance of miR-122 and miR-29 in hepatitis B virus-related liver disease. Genet. Mol. Res., 2014, 13(3), 7912-7918.
[http://dx.doi.org/10.4238/2014.September.29.4] [PMID: 25299106]
[15]
Burchard, J.; Zhang, C.; Liu, A.M. microRNA-122 as a regulator of mitochondrial metabolic gene network in hepatocellular carcinoma. Mol. Syst. Biol., 2010, 6(1), 402.
[http://dx.doi.org/10.1038/msb.2010.58] [PMID: 20739924]
[16]
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]
[17]
Loureiro, D.; Tout, I.; Narguet, S.; Benazzouz, S.M.; Mansouri, A.; Asselah, T. miRNAs as potential biomarkers for viral hepatitis B and C. Viruses, 2020, 12(12), E1440.
[http://dx.doi.org/10.3390/v12121440] [PMID: 33327640]
[18]
Moosavy, S.H.; Nejatizadeh, A.; Davoodian, P.; Eftekhar, E.; Zare, S.; Nazarnezhad, M.A. MicroRNAs biomarkers profiling in diagnosis and therapeutic management of hepatitis B virus Infection. J. Biochem. Technol., 2018, 9(2), 117-127.
[19]
Zhu, X.; Wu, L.; Yao, J. MicroRNA let-7c inhibits cell proliferation and induces cell cycle arrest by targeting CDC25A in human hepatocellular carcinoma. PLoS One, 2015, 10(4), e0124266.
[http://dx.doi.org/10.1371/journal.pone.0124266] [PMID: 25909324]
[20]
Ding, Y.; Yan, J.L.; Fang, A.N.; Zhou, W.F.; Huang, L. Circulating miRNAs as novel diagnostic biomarkers in hepatocellular carcinoma detection: A meta-analysis based on 24 articles. Oncotarget, 2017, 8(39), 66402-66413.
[http://dx.doi.org/10.18632/oncotarget.18949] [PMID: 29029522]
[21]
He, R.Q.; Wu, P.R.; Xiang, X.L. Downregulated miR-23b-3p expression acts as a predictor of hepatocellular carcinoma progression: A study based on public data and RT-qPCR verification. Int. J. Mol. Med., 2018, 41(5), 2813-2831.
[http://dx.doi.org/10.3892/ijmm.2018.3513] [PMID: 29484429]
[22]
Wu, N.; Liu, X.; Xu, X. MicroRNA-373, a new regulator of protein phosphatase 6, functions as an oncogene in hepatocellular carcinoma. FEBS J., 2011, 278(12), 2044-2054.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08120.x] [PMID: 21481188]
[23]
Li, T.; Xie, J.; Shen, C. MiR-150-5p inhibits hepatoma cell migration and invasion by targeting MMP14. PLoS One, 2014, 9(12), e115577.
[http://dx.doi.org/10.1371/journal.pone.0115577] [PMID: 25549355]
[24]
Xu, X.; Tao, Y.; Niu, Y. MiR-125a-5p inhibits tumorigenesis in hepatocellular carcinoma. Aging (Albany NY), 2019, 11(18), 7639-7662.
[http://dx.doi.org/10.18632/aging.102276] [PMID: 31527306]
[25]
Iacob, D.G.; Rosca, A.; Ruta, S.M. Circulating microRNAs as non-invasive biomarkers for hepatitis B virus liver fibrosis. World J. Gastroenterol., 2020, 26(11), 1113-1127.
[http://dx.doi.org/10.3748/wjg.v26.i11.1113] [PMID: 32231417]
[26]
Dundar, H.Z.; Aksoy, F.; Aksoy, S.A. Overexpression of miR-21 is associated with recurrence in patients with Hepatitis B virus-mediated hepatocellular carcinoma undergoing liver transplantation. Transplant. Proc., 2019, 51(4), 1157-1161.
[http://dx.doi.org/10.1016/j.transproceed.2019.01.089] [PMID: 31101191]
[27]
Tai, D.I.; Tai, J. The role of genetic factors in HBV-related HCC: Perspectives from local genetic backgrounds and clinical epidemiology. Hepatoma Res., 2020, 6, 74.
[http://dx.doi.org/10.20517/2394-5079.2020.54]
[28]
Yang, Y.F.; Wang, F.; Xiao, J.J. MiR-222 overexpression promotes proliferation of human hepatocellular carcinoma HepG2 cells by downregulating p27. Int. J. Clin. Exp. Med., 2014, 7(4), 893-902.
[PMID: 24955159]
[29]
Xiao, F.; Zhang, W.; Zhou, L. MicroRNA-200a is an independent prognostic factor of hepatocellular carcinoma and induces cell cycle arrest by targeting CDK6. Oncol. Rep., 2013, 30(5), 2203-2210.
[http://dx.doi.org/10.3892/or.2013.2715] [PMID: 24009066]
[30]
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), 209-214.
[http://dx.doi.org/10.3233/CBM-161671] [PMID: 27983537]
[31]
Wong, Q.W.; Lung, R.W.; Law, P.T. MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology, 2008, 135(1), 257-269.
[http://dx.doi.org/10.1053/j.gastro.2008.04.003] [PMID: 18555017]
[32]
Visalli, M.; Bartolotta, M.; Polito, F. MiRNA expression profiling regulates necroptotic cell death in hepatocellular carcinoma. Int. J. Oncol., 2018, 53(2), 771-780.
[http://dx.doi.org/10.3892/ijo.2018.4410] [PMID: 29845207]
[33]
El-Serag, H.B.; Rudolph, K.L. Hepatocellular carcinoma: Epidemiology and molecular carcinogenesis. Gastroenterology, 2007, 132(7), 2557-2576.
[http://dx.doi.org/10.1053/j.gastro.2007.04.061] [PMID: 17570226]
[34]
Xu, J.; An, P.; Winkler, C.A.; Yu, Y. Dysregulated microRNAs in hepatitis B virus-related hepatocellular carcinoma: Potential as biomarkers and therapeutic targets. Front. Oncol., 2020, 10, 1271.
[http://dx.doi.org/10.3389/fonc.2020.01271] [PMID: 32850386]
[35]
Gao, P.; Wong, C.C.; Tung, E.K.; Lee, J.M.; Wong, C.M.; Ng, I.O. Deregulation of microRNA expression occurs early and accumulates in early stages of HBV-associated multistep hepatocarcinogenesis. J. Hepatol., 2011, 54(6), 1177-1184.
[http://dx.doi.org/10.1016/j.jhep.2010.09.023] [PMID: 21145831]
[36]
An, P.; Xu, J.; Yu, Y.; Winkler, C.A. Host and viral genetic variation in HBV-related hepatocellular carcinoma. Front. Genet., 2018, 9, 261.
[http://dx.doi.org/10.3389/fgene.2018.00261] [PMID: 30073017]
[37]
Soriano, V.; Young, B.; Reau, N. Report from the international conference on viral hepatitis-2017. AIDS Rev., 2018, 20(1), 58-70.
[http://dx.doi.org/10.24875/AIDSRev.M17000012] [PMID: 29369303]
[38]
Lou, W.; Liu, J.; Gao, Y. MicroRNA regulation of liver cancer stem cells. Am. J. Cancer Res., 2018, 8(7), 1126-1141.
[PMID: 30094089]
[39]
Giovannetti, E.; Erozenci, A.; Smit, J.; Danesi, R.; Peters, G.J. Molecular mechanisms underlying the role of microRNAs (miRNAs) in anticancer drug resistance and implications for clinical practice. Crit. Rev. Oncol. Hematol., 2012, 81(2), 103-122.
[http://dx.doi.org/10.1016/j.critrevonc.2011.03.010] [PMID: 21546262]
[40]
Ji, J.; Shi, J.; Budhu, A. MicroRNA expression, survival, and response to interferon in liver cancer. N. Engl. J. Med., 2009, 361(15), 1437-1447.
[41]
Fan, H.X.T.H. Complex interactions between microRNAs and hepatitis B/C viruses. World journal of gastroenterology, 2014, 20(37), 13477-13492.
[42]
Budhu, A.; Jia, H.L.; Forgues, M. Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology, 2008, 47(3), 897-907.
[http://dx.doi.org/10.1002/hep.22160] [PMID: 18176954]
[43]
Li, L.M.; Hu, Z.B.; Zhou, Z.X. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res., 2010, 70(23), 9798-9807.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1001] [PMID: 21098710]
[44]
Kitab, B.; Alj, H.S.; Ezzikouri, S.; Benjelloun, S. MicroRNAs as important players in host-hepatitis B virus interactions. J. Clin. Transl. Hepatol., 2015, 3(2), 149-161.
[PMID: 26357642]
[45]
Huang, D.P.; Zeng, Y.H.; Yuan, W.Q. Bioinformatics analyses of potential miRNA-mRNA regulatory Axis in HBV-related hepatocellular carcinoma. Int. J. Med. Sci., 2021, 18(2), 335-346.
[http://dx.doi.org/10.7150/ijms.50126] [PMID: 33390802]
[46]
Barbu, M.G.; Condrat, C.E.; Thompson, D.C. MicroRNA involvement in signaling pathways during viral infection. Front. Cell Dev. Biol., 2020, 8(143), 143.
[http://dx.doi.org/10.3389/fcell.2020.00143] [PMID: 32211411]
[47]
Wu, H.J.; Zhuo, Y.; Zhou, Y.C. MiR-29a promotes hepatitis B virus replication and expression by targeting SMARCE1 in hepatoma carcinoma. World J. Gastroenterol., 2017, 23(25), 4569-4578.
[http://dx.doi.org/10.3748/wjg.v23.i25.4569] [PMID: 28740345]
[48]
Huang, Y.H.; Yang, Y.L.; Wang, F.S. The role of miR-29a in the regulation, function, and signaling of liver fibrosis. Int. J. Mol. Sci., 2018, 19(7), E1889.
[http://dx.doi.org/10.3390/ijms19071889] [PMID: 29954104]
[49]
Jiang, X.M.; Yu, X.N.; Liu, T.T. MicroRNA-19a-3p promotes tumor metastasis and chemoresistance through the PTEN/Akt pathway in hepatocellular carcinoma. Biomed. Pharmacother., 2018, 105, 1147-1154.
[http://dx.doi.org/10.1016/j.biopha.2018.06.097] [PMID: 30021351]
[50]
Wu, J.; Zhang, T.; Chen, Y.; Ha, S. MiR-139-5p influences hepatocellular carcinoma cell invasion and proliferation capacities via decreasing SLITRK4 expression. Biosci. Rep., 2020, 40(5), BSR20193295.
[http://dx.doi.org/10.1042/BSR20193295] [PMID: 32285917]
[51]
Su, C.; Hou, Z.; Zhang, C.; Tian, Z.; Zhang, J. Ectopic expression of microRNA-155 enhances innate antiviral immunity against HBV infection in human hepatoma cells. Virol. J., 2011, 8(1), 354.
[http://dx.doi.org/10.1186/1743-422X-8-354] [PMID: 21762537]
[52]
Ji, W.B.; Liu, X.; Luo, Y.; Zhang, W.Z. High expression of miR-15b predicts poor prognosis for hepatocellular carcinoma after curative hepatectomy. Oncol. Rep., 2016, 36(4), 1901-1908.
[http://dx.doi.org/10.3892/or.2016.4982] [PMID: 27499071]
[53]
Niu, Y.; Tang, G. miR-185-5p targets ROCK2 and inhibits cell migration and invasion of hepatocellular carcinoma. Oncol. Lett., 2019, 17(6), 5087-5093.
[http://dx.doi.org/10.3892/ol.2019.10144] [PMID: 31105794]
[54]
Du, C.; Weng, X.; Hu, W. Hypoxia-inducible MiR-182 promotes angiogenesis by targeting RASA1 in hepatocellular carcinoma. J. Exp. Clin. Cancer Res., 2015, 34(1), 67.
[http://dx.doi.org/10.1186/s13046-015-0182-1] [PMID: 26126858]
[55]
Cao, G.; Dong, W.; Meng, X.; Liu, H.; Liao, H.; Liu, S. MiR-511 inhibits growth and metastasis of human hepatocellular carcinoma cells by targeting PIK3R3. Tumour Biol., 2015, 36(6), 4453-4459.
[http://dx.doi.org/10.1007/s13277-015-3085-z] [PMID: 25608840]
[56]
Li, C.; Wang, X.; Song, Q. MicroRNA 885-5p inhibits hepatocellular carcinoma metastasis by repressing AEG1. OncoTargets Ther., 2020, 13, 981-988.
[http://dx.doi.org/10.2147/OTT.S228576] [PMID: 32099401]
[57]
He, J.; Mu, M.; Luo, Y. MicroRNA-20b promotes proliferation of H22 hepatocellular carcinoma cells by targeting PTEN. Oncol. Lett., 2019, 17(3), 2931-2936.
[http://dx.doi.org/10.3892/ol.2019.9925] [PMID: 30854070]
[58]
Wang, Y.; Yang, L.; Chen, T. A novel lncRNA MCM3AP-AS1 promotes the growth of hepatocellular carcinoma by targeting miR-194-5p/FOXA1 axis. Mol. Cancer, 2019, 18(1), 28.
[http://dx.doi.org/10.1186/s12943-019-0957-7] [PMID: 30782188]
[59]
Hou, Z.; Zhang, J.; Han, Q. Hepatitis B virus inhibits intrinsic RIG-I and RIG-G immune signaling via inducing miR146a. Sci. Rep., 2016, 6(1), 26150.
[http://dx.doi.org/10.1038/srep26150] [PMID: 27210312]
[60]
Chavalit, T.; Nimsamer, P.; Sirivassanametha, K. Hepatitis B virus-encoded microRNA (HBV-miR-3) regulates host gene PPM1A related to hepatocellular carcinoma. MicroRNA, 2020, 9(3), 232-239.
[http://dx.doi.org/10.2174/2211536608666191104105334] [PMID: 31686644]
[61]
Brunetto, M.R.; Cavallone, D.; Oliveri, F. A serum microRNA signature is associated with the immune control of chronic hepatitis B virus infection. PLoS One, 2014, 9(10), e110782.
[http://dx.doi.org/10.1371/journal.pone.0110782] [PMID: 25350115]
[62]
Wang, Y.; Cao, J.; Zhang, S. MicroRNA-802 induces hepatitis B virus replication and replication through regulating SMARCE1 expression in hepatocellular carcinoma. Cell Death Dis., 2019, 10(10), 783.
[http://dx.doi.org/10.1038/s41419-019-1999-x] [PMID: 31611549]
[63]
Fiorino, S.; Bacchi-Reggiani, M.L.; Visani, M. MicroRNAs as possible biomarkers for diagnosis and prognosis of hepatitis B- and C-related-hepatocellular-carcinoma. World J. Gastroenterol., 2016, 22(15), 3907-3936.
[http://dx.doi.org/10.3748/wjg.v22.i15.3907] [PMID: 27099435]
[64]
Murakami, Y.; Tamori, A.; Itami, S. 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]
[65]
Xing, T.; Zhu, J.; Xian, J. MiRNA-548ah promotes the replication and expression of hepatitis B virus by targeting histone deacetylase 4. Life Sci., 2019, 219, 199-208.
[http://dx.doi.org/10.1016/j.lfs.2018.12.057] [PMID: 30615846]
[66]
Li, J.H.; Liu, S.; Zhou, H.; Qu, L.H.; Yang, J.H. starBase v2.0: Decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res., 2014, 42(Database issue), D92-D97.
[http://dx.doi.org/10.1093/nar/gkt1248] [PMID: 24297251]
[67]
Nagy, Á.; Lánczky, A.; Menyhárt, O. Győrffy B. Validation of miRNA prognostic power in hepatocellular carcinoma using expression data of independent datasets. Sci. Rep., 2018, 8(1), 9227.
[http://dx.doi.org/10.1038/s41598-018-27521-y] [PMID: 29907753]
[68]
Li, Y.; Jiang, M.; Li, M. Compound Phyllanthus urinaria L. Inhibits HBV-related HCC through HBx-SHH pathway axis inactivation. Evid. Based Complement. Alternat. Med., 2019, 2019, 1635837.
[http://dx.doi.org/10.1155/2019/1635837] [PMID: 31019539]
[69]
Wang, X.; Gao, J.; Zhou, B.; Xie, J.; Zhou, G.; Chen, Y. Identification of prognostic markers for hepatocellular carcinoma based on miRNA expression profiles. Life Sci., 2019, 232, 116596.
[http://dx.doi.org/10.1016/j.lfs.2019.116596] [PMID: 31233760]
[70]
Jiang, C.; Yu, M.; Xie, X. miR-217 targeting DKK1 promotes cancer stem cell properties via activation of the Wnt signaling pathway in hepatocellular carcinoma. Oncol. Rep., 2017, 38(4), 2351-2359.
[http://dx.doi.org/10.3892/or.2017.5924] [PMID: 28849121]
[71]
Li, P.; Xiao, Z.; Luo, J.; Zhang, Y.; Lin, L. MiR-139-5p, miR-940 and miR-193a-5p inhibit the growth of hepatocellular carcinoma by targeting SPOCK1. J. Cell. Mol. Med., 2019, 23(4), 2475-2488.
[http://dx.doi.org/10.1111/jcmm.14121] [PMID: 30710422]
[72]
Wu, P.; Xiao, Y.; Guo, T. Identifying miRNA-mRNA pairs and novel miRNAs from hepatocelluar carcinoma miRNomes and TCGA database. J. Cancer, 2019, 10(11), 2552-2559.
[http://dx.doi.org/10.7150/jca.28167] [PMID: 31258761]
[73]
Huang, B.; Huang, M.; Li, Q. MiR-137 suppresses migration and invasion by targeting EZH2-STAT3 signaling in human hepatocellular carcinoma. Pathol. Res. Pract., 2018, 214(12), 1980-1986.
[http://dx.doi.org/10.1016/j.prp.2018.08.005] [PMID: 30274685]
[74]
Sherr, C.J. Cancer cell cycles. Science, 1996, 274(5293), 1672-1677.
[http://dx.doi.org/10.1126/science.274.5293.1672] [PMID: 8939849]
[75]
Cammaerts, S.; Strazisar, M.; De Rijk, P.; Del Favero, J. Genetic variants in microRNA genes: Impact on microRNA expression, function, and disease. Front. Genet., 2015, 6(186), 186.
[http://dx.doi.org/10.3389/fgene.2015.00186] [PMID: 26052338]
[76]
Zheng, B.Y.; Gao, W.Y.; Huang, X.Y. HBx promotes the proliferative ability of HL 7702 cells via the COX 2/Wnt/β catenin pathway. Mol. Med. Rep., 2018, 17(6), 8432-8438.
[http://dx.doi.org/10.3892/mmr.2018.8906] [PMID: 29693167]
[77]
Xia, Y.; Cheng, X.; Li, Y. Hepatitis B virus deregulates the cell cycle to promote viral replication and a premalignant phenotype. J. Virol., 2018, 92(19), 92.
[http://dx.doi.org/10.1128/JVI.00722-18] [PMID: 30021897]
[78]
Mei, Y.; You, Y.; Xia, J.; Gong, J.P.; Wang, Y.B. Identifying differentially expressed micrornas between cirrhotic and non-cirrhotic hepatocellular carcinoma and exploring their functions using bioinformatic analysis. Cell. Physiol. Biochem., 2018, 48(4), 1443-1456.
[http://dx.doi.org/10.1159/000492254] [PMID: 30064138]
[79]
Yang, L.; Ma, Z.; Wang, D.; Zhao, W.; Chen, L.; Wang, G. MicroRNA-602 regulating tumor suppressive gene RASSF1A is overexpressed in hepatitis B virus-infected liver and hepatocellular carcinoma. Cancer Biol. Ther., 2010, 9(10), 803-808.
[http://dx.doi.org/10.4161/cbt.9.10.11440] [PMID: 20364114]
[80]
Jin, J.; Liu, H.; Jin, M.; Li, W.; Xu, H.; Wei, F. Silencing of hsa_circ_0101145 reverses the epithelial-mesenchymal transition in hepatocellular carcinoma via regulation of the miR-548c-3p/LAMC2 axis. Aging (Albany NY), 2020, 12(12), 11623-11635.
[http://dx.doi.org/10.18632/aging.103324] [PMID: 32554866]
[81]
Timofeev, O.; Cizmecioglu, O.; Settele, F.; Kempf, T.; Hoffmann, I. Cdc25 phosphatases are required for timely assembly of CDK1-cyclin B at the G2/M transition. J. Biol. Chem., 2010, 285(22), 16978-16990.
[http://dx.doi.org/10.1074/jbc.M109.096552] [PMID: 20360007]
[82]
Shen, D.Y.; Fang, Z.X.; You, P. Clinical significance and expression of cyclin kinase subunits 1 and 2 in hepatocellular carcinoma. Liver Int., 2010, 30, 119-125.
[http://dx.doi.org/10.1111/j.1478-3231.2009.02106.x]
[83]
Fang, Y.; Yu, H.; Liang, X.; Xu, J.; Cai, X. Chk1-induced CCNB1 overexpression promotes cell proliferation and tumor growth in human colorectal cancer. Cancer Biol. Ther., 2014, 15(9), 1268-1279.
[http://dx.doi.org/10.4161/cbt.29691] [PMID: 24971465]
[84]
Luo, Q.; Li, X.; Li, J. MiR-15a is underexpressed and inhibits the cell cycle by targeting CCNE1 in breast cancer. Int. J. Oncol., 2013, 43(4), 1212-1218.
[http://dx.doi.org/10.3892/ijo.2013.2034] [PMID: 23900351]
[85]
Cheng, P.; Li, Y.; Yang, L. Hepatitis B virus X protein (HBx) induces G2/M arrest and apoptosis through sustained activation of cyclin B1-CDK1 kinase. Oncol. Rep., 2009, 22(5), 1101-1107.
[PMID: 19787227]
[86]
Chin, R.; Earnest-Silveira, L.; Koeberlein, B. Modulation of MAPK pathways and cell cycle by replicating hepatitis B virus: Factors contributing to hepatocarcinogenesis. J. Hepatol., 2007, 47(3), 325-337.
[http://dx.doi.org/10.1016/j.jhep.2007.03.025] [PMID: 17512084]
[87]
Sung, W.K.; Zheng, H.; Li, S. Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat. Genet., 2012, 44(7), 765-769.
[http://dx.doi.org/10.1038/ng.2295] [PMID: 22634754]
[88]
Sohn, W.; Kim, J.; Kang, S.H. Serum exosomal microRNAs as novel biomarkers for hepatocellular carcinoma. Exp. Mol. Med., 2015, 47(9), e184.
[http://dx.doi.org/10.1038/emm.2015.68] [PMID: 26380927]
[89]
Yang, X.; Li, H.; Sun, H. Hepatitis B virus-encoded microRNA controls viral replication. J. Virol., 2017, 91(10), e01919-e16.
[http://dx.doi.org/10.1128/JVI.01919-16] [PMID: 28148795]
[90]
Furuta, M.; Kozaki, K.; Tanimoto, K. The tumor-suppressive miR-497-195 cluster targets multiple cell-cycle regulators in hepatocellular carcinoma. PLoS One, 2013, 8(3), e60155.
[http://dx.doi.org/10.1371/journal.pone.0060155] [PMID: 23544130]
[91]
Li, J.; Huang, L.; Yan, J.; Qiu, M.; Yan, Y. Liver resection for hepatocellular carcinoma: Personal experiences in a series of 1330 consecutive cases in China. ANZ J. Surg., 2018, 88(10), E713-E717.
[http://dx.doi.org/10.1111/ans.14381] [PMID: 29363237]
[92]
Iorio, M.V.; Croce, C.M. MicroRNA dysregulation in cancer: Diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med., 2012, 4(3), 143-159.
[http://dx.doi.org/10.1002/emmm.201100209] [PMID: 22351564]
[93]
Croce, C.M.; Calin, G.A. MiRNAs, cancer, and stem cell division. Cell, 2005, 122(1), 6-7.
[http://dx.doi.org/10.1016/j.cell.2005.06.036] [PMID: 16009126]
[94]
Hung, C.H.; Hu, T.H.; Lu, S.N. Circulating microRNAs as biomarkers for diagnosis of early hepatocellular carcinoma associated with hepatitis B virus. Int. J. Cancer, 2016, 138(3), 714-720.
[http://dx.doi.org/10.1002/ijc.29802] [PMID: 26264553]
[95]
Ge, W.; Yu, D.C.; Li, Q.G.; Chen, X.; Zhang, C.Y.; Ding, Y.T. Expression of serum miR-16, let-7f, and miR-21 in patients with hepatocellular carcinoma and their clinical significances. Clin. Lab., 2014, 60(3), 427-434.
[http://dx.doi.org/10.7754/Clin.Lab.2013.130133] [PMID: 24697119]
[96]
Thurnherr, T.; Mah, W.C.; Lei, Z.; Jin, Y.; Rozen, S.G.; Lee, C.G. Differentially expressed miRNAs in hepatocellular carcinoma target genes in the genetic information processing and metabolism pathways. Sci. Rep., 2016, 6(1), 20065.
[http://dx.doi.org/10.1038/srep20065] [PMID: 26817861]
[97]
Giray, B.G.; Emekdas, G.; Tezcan, S. Profiles of serum microRNAs; miR-125b-5p and miR223-3p serve as novel biomarkers for HBV-positive hepatocellular carcinoma. Mol. Biol. Rep., 2014, 41(7), 4513-4519.
[http://dx.doi.org/10.1007/s11033-014-3322-3] [PMID: 24595450]
[98]
Hou, J.; Lin, L.; Zhou, W. 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), 232-243.
[http://dx.doi.org/10.1016/j.ccr.2011.01.001] [PMID: 21316602]
[99]
Lou, W.; Liu, J.; Ding, B. Identification of potential miRNA-mRNA regulatory network contributing to pathogenesis of HBV-related HCC. J. Transl. Med., 2019, 17(1), 7.
[http://dx.doi.org/10.1186/s12967-018-1761-7] [PMID: 30602391]
[100]
Yang, Y.; Chen, L.; Gu, J. Recurrently deregulated lncRNAs in hepatocellular carcinoma. Nat. Commun., 2017, 8(1), 14421.
[http://dx.doi.org/10.1038/ncomms14421] [PMID: 28194035]
[101]
Sagnelli, E.; Potenza, N.; Onorato, L.; Sagnelli, C.; Coppola, N.; Russo, A. Micro-RNAs in hepatitis B virus-related chronic liver diseases and hepatocellular carcinoma. World J. Hepatol., 2018, 10(9), 558-570.
[http://dx.doi.org/10.4254/wjh.v10.i9.558] [PMID: 30310534]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy