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Current Molecular Pharmacology

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ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

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Mini-Review Article

Advances in Research on microRNAs Related to the Invasion and Metastasis of Nasopharyngeal Carcinoma

Author(s): ShanShan Zhang, BaiQi Wang, LuLu Zheng, ZhuQiong Fu, YiTing Fu, WeiGuo Huang and AiLan Cheng*

Volume 15, Issue 3, 2022

Published on: 11 January, 2022

Article ID: e140621194070 Pages: 12

DOI: 10.2174/1874467214666210614150720

Price: $65

Abstract

Nasopharyngeal Carcinoma (NPC), which is associated with latent Epstein-Barr virus infection in most cases, is a unique epithelial malignancy arising from the nasopharyngeal mucosal lining. Accumulating evidence is providing insights into the genetic and molecular aberrations that likely drive nasopharyngeal tumor development and progression. We review recent analyses of microRNAs (miRNAs), including Epstein-Barr virus-encoded miRNAs (EBV-encoded miRNAs) and dysregulated cellular miRNAs, that may be related to the metastasis of nasopharyngeal carcinoma. The studies summarized herein have greatly expanded our knowledge of the molecular biology of NPC involving miRNAs, and they may provide new biological targets for clinical diagnosis and reveal the potential of microRNA therapeutics. However, much remains to be uncovered.

Keywords: Nasopharyngeal carcinoma, miRNAs, EBV-encoded miRNAs, invasion, metastasis, NPC.

Graphical Abstract

[1]
Bruce, J.P.; Yip, K.; Bratman, S.V.; Ito, E.; Liu, F.F. Nasopharyngeal cancer: Molecular landscape. J. Clin. Oncol., 2015, 33(29), 3346-3355.
[http://dx.doi.org/10.1200/JCO.2015.60.7846] [PMID: 26351340]
[2]
Chen, Y-P.; Chan, A.T.C.; Le, Q-T.; Blanchard, P.; Sun, Y.; Ma, J. Nasopharyngeal carcinoma. Lancet, 2019, 394(10192), 64-80.
[http://dx.doi.org/10.1016/S0140-6736(19)30956-0] [PMID: 31178151]
[3]
Cai, L.M.; Lyu, X.M.; Luo, W.R.; Cui, X.F.; Ye, Y.F.; Yuan, C.C.; Peng, Q.X.; Wu, D.H.; Liu, T.F.; Wang, E.; Marincola, F.M.; Yao, K.T.; Fang, W.Y.; Cai, H.B.; Li, X. EBV-miR-BART7-3p promotes the EMT and metastasis of nasopharyngeal carcinoma cells by suppressing the tumor suppressor PTEN. Oncogene, 2015, 34(17), 2156-2166.
[http://dx.doi.org/10.1038/onc.2014.341] [PMID: 25347742]
[4]
Lee, H.M.; Okuda, K.S.; González, F.E.; Patel, V. Current perspectives on nasopharyngeal carcinoma. Adv. Exp. Med. Biol., 2019, 1164, 11-34.
[http://dx.doi.org/10.1007/978-3-030-22254-3_2] [PMID: 31576537]
[5]
Agulnik, M.; Epstein, J.B. Nasopharyngeal carcinoma: current management, future directions and dental implications. Oral Oncol., 2008, 44(7), 617-627.
[http://dx.doi.org/10.1016/j.oraloncology.2007.08.003] [PMID: 18061518]
[6]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[7]
Guo, R.; Mao, Y-P.; Tang, L-L.; Chen, L.; Sun, Y.; Ma, J. The evolution of nasopharyngeal carcinoma staging. Br. J. Radiol., 2019, 92(1102), 20190244.
[http://dx.doi.org/10.1259/bjr.20190244] [PMID: 31298937]
[8]
Wang, L.; Guo, Y.; Xu, J.; Chen, Z.; Jiang, X.; Zhang, L.; Huang, S.; He, X.; Zhang, Y. Clinical analysis of recurrence patterns in patients with nasopharyngeal carcinoma treated With intensity-modulated radiotherapy. Ann. Otol. Rhinol. Laryngol., 2017, 126(12), 789-797.
[http://dx.doi.org/10.1177/0003489417734229] [PMID: 29025277]
[9]
Lo, K.W.; Chung, G.T.; To, K.F. Deciphering the molecular genetic basis of NPC through molecular, cytogenetic, and epigenetic approaches. Semin. Cancer Biol., 2012, 22(2), 79-86.
[http://dx.doi.org/10.1016/j.semcancer.2011.12.011] [PMID: 22245473]
[10]
Xu, F-H.; Xiong, D.; Xu, Y-F.; Cao, S-M.; Xue, W-Q.; Qin, H-D.; Liu, W-S.; Cao, J-Y.; Zhang, Y.; Feng, Q-S.; Chen, L-Z.; Li, M-Z.; Liu, Z-W.; Liu, Q.; Hong, M-H.; Shugart, Y.Y.; Zeng, Y.X.; Zeng, M.S.; Jia, W.H. An epidemiological and molecular study of the relationship between smoking, risk of nasopharyngeal carcinoma, and Epstein-Barr virus activation. J. Natl. Cancer Inst., 2012, 104(18), 1396-1410.
[http://dx.doi.org/10.1093/jnci/djs320] [PMID: 22972969]
[11]
Paul, P.; Deka, H.; Malakar, A.K.; Halder, B.; Chakraborty, S. Nasopharyngeal carcinoma: understanding its molecular biology at a fine scale. Eur. J. Cancer Prev., 2018, 27(1), 33-41.
[http://dx.doi.org/10.1097/CEJ.0000000000000314] [PMID: 27748661]
[12]
Esquela-Kerscher, A.; Slack, F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer, 2006, 6(4), 259-269.
[http://dx.doi.org/10.1038/nrc1840] [PMID: 16557279]
[13]
Calin, G.A.; Croce, C.M. MicroRNA signatures in human cancers. Nat. Rev. Cancer, 2006, 6(11), 857-866.
[http://dx.doi.org/10.1038/nrc1997] [PMID: 17060945]
[14]
Mo, M-H.; Chen, L.; Fu, Y.; Wang, W.; Fu, S.W. Cell-free Circulating miRNA Biomarkers in Cancer. J. Cancer, 2012, 3, 432-448.
[http://dx.doi.org/10.7150/jca.4919] [PMID: 23074383]
[15]
Johannes, H. Matse, Janice Yoshizawa, Xiaoyan Wang, David Elashoff, Jan G M Bolscher, Enno C I Veerman, Elisabeth Bloemena, David T W Wong. Discovery and prevalidation of salivary extracellular microRNA biomarkers panel for the noninvasive detection of benign and malignant parotid gland tumors. Clin. Cancer Res., 2013, 19, 3032-3038.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-3505]
[16]
Wang, Y.; Guo, Z.; Shu, Y.; Zhou, H.; Wang, H.; Zhang, W. BART miRNAs: an unimaginable force in the development of nasopharyngeal carcinoma. Eur. J. Cancer Prev., 2017, 26(2), 144-150.
[http://dx.doi.org/10.1097/CEJ.0000000000000221] [PMID: 26909566]
[17]
Zhuo, X.; Zhou, W.; Ye, H.; Li, D.; Chang, A.; Wu, Y.; Zhou, Q. Screening of key miRNAs and evaluation of their diagnostic and prognostic values in nasopharyngeal carcinoma. Oncol. Lett., 2019, 17(6), 5803-5810.
[http://dx.doi.org/10.3892/ol.2019.10231] [PMID: 31186807]
[18]
Barth, S.; Meister, G.; Grässer, F.A. EBV-encoded miRNAs. Biochim. Biophys. Acta, 2011, 1809(11-12), 631-640.
[http://dx.doi.org/10.1016/j.bbagrm.2011.05.010] [PMID: 21640213]
[19]
Kim, D.N.; Lee, S.K. Biogenesis of Epstein-Barr virus microRNAs. Mol. Cell. Biochem., 2012, 365(1-2), 203-210.
[http://dx.doi.org/10.1007/s11010-012-1261-7] [PMID: 22350759]
[20]
Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2), 281-297.
[http://dx.doi.org/10.1016/S0092-8674(04)00045-5] [PMID: 14744438]
[21]
Pfeffer, S.; Zavolan, M.; Grässer, F.A.; Chien, M.; Russo, J.J.; Ju, J.; John, B.; Enright, A.J.; Marks, D.; Sander, C.; Tuschl, T. Identification of virus-encoded microRNAs. Science, 2004, 304(5671), 734-736.
[http://dx.doi.org/10.1126/science.1096781] [PMID: 15118162]
[22]
Cai, X.; Schäfer, A.; Lu, S.; Bilello, J.P.; Desrosiers, R.C.; Edwards, R.; Raab-Traub, N.; Cullen, B.R. Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog., 2006, 2(3), e23.
[http://dx.doi.org/10.1371/journal.ppat.0020023] [PMID: 16557291]
[23]
Tsao, S.W.; Tsang, C.M.; To, K.F.; Lo, K.W. The role of Epstein-Barr virus in epithelial malignancies. J. Pathol., 2015, 235(2), 323-333.
[http://dx.doi.org/10.1002/path.4448] [PMID: 25251730]
[24]
Raab-Traub, N. Epstein-Barr virus in the pathogenesis of NPC. Semin. Cancer Biol., 2002, 12(6), 431-441.
[http://dx.doi.org/10.1016/S1044579X0200086X] [PMID: 12450729]
[25]
Raab-Traub, N. Nasopharyngeal Carcinoma: An Evolving Role for the Epstein-Barr Virus. Curr. Top. Microbiol. Immunol., 2015, 390(Pt 1), 339-363.
[http://dx.doi.org/10.1007/978-3-319-22822-8_14] [PMID: 26424653]
[26]
Le, Q-T.; Zhang, Q.; Cao, H.; Cheng, A.-J.; Pinsky, B.A.; Hong, R.L.; Chang, J.T.; Wang, C.-W.; Le, T.; Tsao, K.-C.; Lo, Y.D.; Lee, N.; Ang, K.K.; Chan, A.T.C.; Chan, K.C.A. An international collaboration to har- monize the quantitative plasma Epstein-Barr virus DNA assay for future biomarker-guided trials in nasopharyngeal carcinoma. Clin. Cancer Res., 2013, 19(8), 2208-2215.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-3702] [PMID: 23459720]
[27]
Choy, E.Y.-W.; Siu, K.-L.; Kok, K.-H.; Lung, R.W.-M; Tsang, C.M.; To, K.-F.; Kwong, D.L.-W.; Tsao, S.W; Jin, D.-Y. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J. Exp. Med., 2008, 205, 2551-2560.
[28]
Cai, L.; Ye, Y.; Jiang, Q.; Chen, Y.; Lyu, X.; Li, J.; Wang, S.; Liu, T.; Cai, H.; Yao, K.; Li, J.L.; Li, X. Epstein-Barr virus-encoded microRNA BART1 induces tumour metastasis by regulating PTEN-dependent pathways in nasopharyngeal carcinoma. Nat. Commun., 2015, 6, 7353.
[http://dx.doi.org/10.1038/ncomms8353] [PMID: 26135619]
[29]
Ye, Y.; Zhou, Y.; Zhang, L.; Chen, Y.; Lyu, X.; Cai, L.; Lu, Y.; Deng, Y.; Wang, J.; Yao, K.; Fang, W.; Cai, H.; Li, X. EBV-miR-BART1 is involved in regulating metabolism-associated genes in nasopharyngeal carcinoma. Biochem. Biophys. Res. Commun., 2013, 436(1), 19-24.
[http://dx.doi.org/10.1016/j.bbrc.2013.05.008] [PMID: 23685147]
[30]
Jiang, C.; Li, L.; Xiang, Y.Q.; Lung, M.L.; Zeng, T.; Lu, J.; Tsao, S.W.; Zeng, M.S.; Yun, J.P.; Kwong, D.L.W.; Guan, X.Y. Epstein-barr virus miRNA BART2-5p promotes metastasis of nasopharyngeal carcinoma by suppressing RND3. Cancer Res., 2020, 80(10), 1957-1969.
[http://dx.doi.org/10.1158/0008-5472.CAN-19-0334] [PMID: 32060148]
[31]
Lu, T.; Guo, Q.; Lin, K.; Chen, H.; Chen, Y.; Xu, Y.; Lin, C.; Su, Y.; Chen, Y.; Chen, M.; Zheng, Y.; Ye, Y.; Lin, S.; Zong, J.; Pan, J. Circulating Epstein-Barr virus microRNAs BART7-3p and BART13-3p as novel biomarkers in nasopharyngeal carcinoma. Cancer Sci., 2020, 111(5), 1711-1723.
[http://dx.doi.org/10.1111/cas.14381] [PMID: 32155300]
[32]
Zhang, G.; Zong, J.; Lin, S.; Verhoeven, R.J.A.; Tong, S.; Chen, Y.; Ji, M.; Cheng, W.; Tsao, S-W.; Lung, M.; Pan, J.; Chen, H. Circulating Epstein-Barr virus microRNAs miR-BART7 and miR-BART13 as biomarkers for nasopharyngeal carcinoma diagnosis and treatment. Int. J. Cancer, 2015, 136(5), E301-E312.
[http://dx.doi.org/10.1002/ijc.29206] [PMID: 25213622]
[33]
Cai, L.; Long, Y.; Chong, T.; Cai, W.; Tsang, C.M.; Zhou, X.; Lin, Y.; Ding, T.; Zhou, W.; Zhao, H.; Chen, Y.; Wang, J.; Lyu, X.; Cho, W.C.; Li, X. EBV-miR-BART7-3p imposes stemness in nasopharyngeal carcinoma cells by suppressing SMAD7. Front. Genet., 2019, 10, 939.
[http://dx.doi.org/10.3389/fgene.2019.00939] [PMID: 31681406]
[34]
Lin, C.; Zong, J.; Lin, W.; Wang, M.; Xu, Y.; Zhou, R.; Lin, S.; Guo, Q.; Chen, H.; Ye, Y.; Zhang, B.; Pan, J. EBV-miR-BART8-3p induces epithelial-mesenchymal transition and promotes metastasis of nasopharyngeal carcinoma cells through activating NF-κB and Erk1/2 pathways. J. Exp. Clin. Cancer Res., 2018, 37(1), 283.
[http://dx.doi.org/10.1186/s13046-018-0953-6] [PMID: 30477559]
[35]
Zhou, X.; Zheng, J.; Tang, Y.; Lin, Y.; Wang, L.; Li, Y.; Liu, C.; Wu, D.; Cai, L.J.B.r. EBV encoded miRNA BART8-3p promotes radioresistance in nasopharyngeal carcinoma by regulating ATM/ATR signaling pathway. 2019, 39
[36]
Hsu, C.Y.; Yi, Y.H.; Chang, K.P.; Chang, Y.S.; Chen, S.J.; Chen, H.C. The Epstein-Barr virus-encoded microRNA MiR-BART9 promotes tumor metastasis by targeting E-cadherin in nasopharyngeal carcinoma. PLoS Pathog., 2014, 10(2), e1003974.
[http://dx.doi.org/10.1371/journal.ppat.1003974] [PMID: 24586173]
[37]
Yan, Q.; Zeng, Z.; Gong, Z.; Zhang, W.; Li, X.; He, B.; Song, Y.; Li, Q.; Zeng, Y.; Liao, Q.; Chen, P.; Shi, L.; Fan, S.; Xiang, B.; Ma, J.; Zhou, M.; Li, X.; Yang, J.; Xiong, W.; Li, G. EBV-miR-BART10-3p facilitates epithelial-mesenchymal transition and promotes metastasis of nasopharyngeal carcinoma by targeting BTRC. Oncotarget, 2015, 6(39), 41766-41782.
[http://dx.doi.org/10.18632/oncotarget.6155] [PMID: 26497204]
[38]
Xu, Y-J.; Zhou, R.; Zong, J-F.; Lin, W-S.; Tong, S.; Guo, Q-J.; Lin, C.; Lin, S-J.; Chen, Y-X.; Chen, M-R.; Chen, H-L.; Ye, Y-B.; Pan, J-J. Epstein-Barr virus-coded miR-BART13 promotes nasopharyngeal carcinoma cell growth and metastasis via targeting of the NKIRAS2/NF-κB pathway. Cancer Lett., 2019, 447, 33-40.
[http://dx.doi.org/10.1016/j.canlet.2019.01.022] [PMID: 30684592]
[39]
Huang, J.; Qin, Y.; Yang, C.; Wan, C.; Dai, X.; Sun, Y.; Meng, J.; Lu, Y.; Li, Y.; Zhang, Z.; Wu, B.; Xu, S.; Jin, H.; Yang, K. Downregulation of ABI2 expression by EBV-miR-BART13-3p induces epithelial-mesenchymal transition of nasopharyngeal carcinoma cells through upregulation of c-JUN/SLUG signaling. Aging (Albany NY), 2020, 12(1), 340-358.
[http://dx.doi.org/10.18632/aging.102618] [PMID: 31907338]
[40]
Chen, R.; Zhang, M.; Li, Q.; Xiong, H.; Liu, S.; Fang, W.; Zhang, Q.; Liu, Z.; Xu, X.; Jiang, Q. The Epstein-Barr Virus-encoded miR-BART22 targets MAP3K5 to promote host cell proliferative and invasive abilities in nasopharyngeal carcinoma. J. Cancer, 2017, 8(2), 305-313.
[http://dx.doi.org/10.7150/jca.15753] [PMID: 28243335]
[41]
Jiang, Q.P.; Liu, S.Y.; He, X.F.; Peng, J.; Xiong, H.Z.; Xiong, Z.T.; Yang, Y.X. [Relationship between MAP3K5 and Epstein-Barr virus-encoded miR-BART22 expression in nasopharyngeal carcinoma]. Nan Fang Yi Ke Da Xue Xue Bao, 2011, 31(7), 1146-1149.
[PMID: 21764682]
[42]
Liu, Y.; Jiang, Q.; Liu, X.; Lin, X.; Tang, Z.; Liu, C.; Zhou, J.; Zhao, M.; Li, X.; Cheng, Z.; Li, L.; Xie, Y.; Liu, Z.; Fang, W. Cinobufotalin powerfully reversed EBV-miR-BART22-induced cisplatin resistance via stimulating MAP2K4 to antagonize non-muscle myosin heavy chain IIA/glycogen synthase 3β/β-catenin signaling pathway. EBioMedicine, 2019, 48, 386-404.
[http://dx.doi.org/10.1016/j.ebiom.2019.08.040] [PMID: 31594754]
[43]
He, B.; Li, W.; Wu, Y.; Wei, F.; Gong, Z.; Bo, H.; Wang, Y.; Li, X.; Xiang, B.; Guo, C.; Liao, Q.; Chen, P.; Zu, X.; Zhou, M.; Ma, J.; Li, X.; Li, Y.; Li, G.; Xiong, W.; Zeng, Z. Epstein-Barr virus-encoded miR-BART6-3p inhibits cancer cell metastasis and invasion by targeting long non-coding RNA LOC553103. Cell Death Dis., 2016, 7(9), e2353.
[http://dx.doi.org/10.1038/cddis.2016.253] [PMID: 27584792]
[44]
Ambros, V. The functions of animal microRNAs. Nature, 2004, 431(7006), 350-355.
[http://dx.doi.org/10.1038/nature02871] [PMID: 15372042]
[45]
Lytle, J.R.; Yario, T.A.; Steitz, J.A. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc. Natl. Acad. Sci. USA, 2007, 104(23), 9667-9672.
[http://dx.doi.org/10.1073/pnas.0703820104] [PMID: 17535905]
[46]
Correia de Sousa, M.; Gjorgjieva, M.; Dolicka, D.; Sobolewski, C.; Foti, M. Deciphering miRNAs’ Action through miRNA Editing. Int. J. Mol. Sci., 2019, 20(24), 20.
[http://dx.doi.org/10.3390/ijms20246249] [PMID: 31835747]
[47]
Mishra, S.; Yadav, T.; Rani, V. Exploring miRNA based approaches in cancer diagnostics and therapeutics. Crit. Rev. Oncol. Hematol., 2016, 98, 12-23.
[http://dx.doi.org/10.1016/j.critrevonc.2015.10.003] [PMID: 26481951]
[48]
Zhao, C-X.; Zhu, W.; Ba, Z-Q.; Xu, H-J.; Liu, W-D.; Zhu, B.; Wang, L.; Song, Y-J.; Yuan, S.; Ren, C-P. The regulatory network of nasopharyngeal carcinoma metastasis with a focus on EBV, lncRNAs and miRNAs. Am. J. Cancer Res., 2018, 8(11), 2185-2209.
[PMID: 30555738]
[49]
Lee, K.T.; Tan, J.K.; Lam, A.K.; Gan, S.Y. MicroRNAs serving as potential biomarkers and therapeutic targets in nasopharyngeal carcinoma: A critical review. Crit. Rev. Oncol. Hematol., 2016, 103, 1-9.
[http://dx.doi.org/10.1016/j.critrevonc.2016.04.006] [PMID: 27179594]
[50]
Yang, Y.; Li, Q.; Guo, L. MicroRNA-122 acts as tumor suppressor by targeting TRIM29 and blocking the activity of PI3K/AKT signaling in nasopharyngeal carcinoma in vitro. Mol. Med. Rep., 2018, 17(6), 8244-8252.
[http://dx.doi.org/10.3892/mmr.2018.8894] [PMID: 29693120]
[51]
Lin, C.H.; Chiang, M.C.; Chen, Y.J. MicroRNA-328 inhibits migration and epithelial-mesenchymal transition by targeting CD44 in nasopharyngeal carcinoma cells. OncoTargets Ther., 2018, 11, 2375-2385.
[http://dx.doi.org/10.2147/OTT.S151665] [PMID: 29740213]
[52]
Zhu, X.; Li, W.; Zhang, R.; Liu, Y. MicroRNA-342 inhibits cell proliferation and invasion in nasopharyngeal carcinoma by directly targeting ZEB1. Oncol. Lett., 2018, 16(1), 1298-1304.
[http://dx.doi.org/10.3892/ol.2018.8788] [PMID: 30061949]
[53]
Wang, F.; Jiang, C.; Sun, Q.; Yan, F.; Wang, L.; Fu, Z.; Liu, T.; Hu, F. Downregulation of miR-429 and inhibition of cell migration and invasion in nasopharyngeal carcinoma. Mol. Med. Rep., 2016, 13(4), 3236-3242.
[http://dx.doi.org/10.3892/mmr.2016.4940] [PMID: 26936585]
[54]
Liang, T.S.; Zheng, Y.J.; Wang, J.; Zhao, J.Y.; Yang, D.K.; Liu, Z.S. MicroRNA-506 inhibits tumor growth and metastasis in nasopharyngeal carcinoma through the inactivation of the Wnt/β- catenin signaling pathway by down-regulating LHX2. J. Exp. Clin. Cancer Res., 2019, 38(1), 97.
[http://dx.doi.org/10.1186/s13046-019-1023-4] [PMID: 30791932]
[55]
Yang, X.; Ni, W.; Lei, K. miR-200b suppresses cell growth, migration and invasion by targeting Notch1 in nasopharyngeal carcinoma. Cell. Physiol. Biochem., 2013, 32(5), 1288-1298.
[http://dx.doi.org/10.1159/000354527] [PMID: 24281414]
[56]
Chen, X.; Li, J.; Zhang, S.; Xu, W.; Shi, D.; Zhuo, M.; Liang, S.; Lei, W.; Xie, C. MicroRNA‑30a regulates cell proliferation, migration, invasion and apoptosis in human nasopharyngeal carcinoma via targeted regulation of ZEB2. Mol. Med. Rep., 2019, 20(2), 1672-1682.
[http://dx.doi.org/10.3892/mmr.2019.10387] [PMID: 31257481]
[57]
Piskareva, O.; Harvey, H.; Nolan, J.; Conlon, R.; Alcock, L.; Buckley, P.; Dowling, P.; Henry, M.; O’Sullivan, F.; Bray, I.; Stallings, R.L. The development of cisplatin resistance in neuroblastoma is accompanied by epithelial to mesenchymal transition in vitro. Cancer Lett., 2015, 364(2), 142-155.
[http://dx.doi.org/10.1016/j.canlet.2015.05.004] [PMID: 25960282]
[58]
Shao, Q.; Zhang, P.; Ma, Y.; Lu, Z.; Meng, J.; Li, H.; Wang, X.; Chen, D.; Zhang, M.; Han, Y.; Liu, H.; Ma, S. MicroRNA-139-5p affects cisplatin sensitivity in human nasopharyngeal carcinoma cells by regulating the epithelial-to-mesenchymal transition. Gene, 2018, 652, 48-58.
[http://dx.doi.org/10.1016/j.gene.2018.02.003] [PMID: 29427737]
[59]
Ji, Y.; Wang, M.; Li, X.; Cui, F. The long noncoding RNA NEAT1 targets miR-34a-5p and drives nasopharyngeal carcinoma progression via Wnt/β-catenin signaling. Yonsei Med. J., 2019, 60(4), 336-345.
[http://dx.doi.org/10.3349/ymj.2019.60.4.336] [PMID: 30900419]
[60]
Zhu, H-M.; Jiang, X-S.; Li, H-Z.; Qian, L-X.; Du, M-Y.; Lu, Z-W.; Wu, J.; Tian, X-K.; Fei, Q.; He, X.; Yin, L. miR-184 inhibits tumor invasion, migration and metastasis in nasopharyngeal carcinoma by targeting notch2. Cell. Physiol. Biochem., 2018, 49(4), 1564-1576.
[http://dx.doi.org/10.1159/000493459] [PMID: 30223264]
[61]
Duan, H.F.; Li, X.Q.; Hu, H.Y.; Li, Y.C.; Cai, Z.; Mei, X.S.; Yu, P.; Nie, L.P.; Zhang, W.; Yu, Z.D.; Nie, G.H. Functional elucidation of miR-494 in the tumorigenesis of nasopharyngeal carcinoma. Tumour Biol., 2015, 36(9), 6679-6689.
[http://dx.doi.org/10.1007/s13277-015-3356-8] [PMID: 25809707]
[62]
Xu, S.; Zhao, N.; Hui, L.; Song, M.; Miao, Z-W.; Jiang, X-J. MicroRNA-124-3p inhibits the growth and metastasis of nasopharyngeal carcinoma cells by targeting STAT3. Oncol. Rep., 2016, 35(3), 1385-1394.
[http://dx.doi.org/10.3892/or.2015.4524] [PMID: 26707908]
[63]
Chen, J.H.; Yang, R.; Zhang, W.; Wang, Y.P. Functions of microRNA-143 in the apoptosis, invasion and migration of nasopharyngeal carcinoma. Exp. Ther. Med., 2016, 12(6), 3749-3755.
[http://dx.doi.org/10.3892/etm.2016.3847] [PMID: 28101165]
[64]
Li, Y.; Min, D.; Wang, K.; Yin, S.; Zheng, H.; Liu, L. MicroRNA‑152 inhibits cell proliferation, migration and invasion by directly targeting MAFB in nasopharyngeal carcinoma. Mol. Med. Rep., 2017, 15(2), 948-956.
[http://dx.doi.org/10.3892/mmr.2016.6059] [PMID: 28000885]
[65]
Jiang, C.; Wang, H.; Zhou, L.; Jiang, T.; Xu, Y.; Xia, L. MicroRNA-212 inhibits the metastasis of nasopharyngeal carcinoma by targeting SOX4. Oncol. Rep., 2017, 38(1), 82-88.
[http://dx.doi.org/10.3892/or.2017.5641] [PMID: 28504814]
[66]
Zhu, W.; Ma, Y.; Zhuang, X.; Jin, X. MicroRNA-425 is downregulated in nasopharyngeal carcinoma and regulates tumor cell viability and invasion by targeting hepatoma-derived growth factor. Oncol. Lett., 2018, 15(5), 6345-6351.
[http://dx.doi.org/10.3892/ol.2018.8128] [PMID: 29616111]
[67]
Wang, T.; Du, M.; Zhang, W.; Bai, H.; Yin, L.; Chen, W.; He, X.; Chen, Q. MicroRNA-432 suppresses invasion and migration via E2F3 in nasopharyngeal carcinoma. OncoTargets Ther., 2019, 12, 11271-11280.
[http://dx.doi.org/10.2147/OTT.S233435] [PMID: 31908492]
[68]
Yin, W.; Shi, L.; Mao, Y. MicroRNA-449b-5p suppresses cell proliferation, migration and invasion by targeting TPD52 in nasopharyngeal carcinoma. J. Biochem., 2019, 166(5), 433-440.
[http://dx.doi.org/10.1093/jb/mvz057] [PMID: 31350893]
[69]
Chen, X.; Shi, J.; Zhong, J.; Huang, Z.; Luo, X.; Huang, Y.; Feng, S.; Shao, J.; Liu, D. miR-1, regulated by LMP1, suppresses tumour growth and metastasis by targeting K-ras in nasopharyngeal carcinoma. Int. J. Exp. Pathol., 2015, 96(6), 427-432.
[http://dx.doi.org/10.1111/iep.12162] [PMID: 26852690]
[70]
Ma, Y-X.; Zhang, H.; Li, X-H.; Liu, Y-H. MiR-30e-5p inhibits proliferation and metastasis of nasopharyngeal carcinoma cells by target-ing USP22. Eur. Rev. Med. Pharmacol. Sci., 2018, 22(19), 6342-6349.
[PMID: 30338802]
[71]
Sun, X.; Liu, X.; Wang, Y.; Yang, S.; Chen, Y.; Yuan, T. miR-100 inhibits the migration and invasion of nasopharyngeal carcinoma by targeting IGF1R. Oncol. Lett., 2018, 15(6), 8333-8338.
[http://dx.doi.org/10.3892/ol.2018.8420] [PMID: 29805566]
[72]
Liu, Y-H.; Liu, J-L.; Wang, Z.; Zhu, X-H.; Chen, X-B.; Wang, M-Q. MiR-122-5p suppresses cell proliferation, migration and invasion by targeting SATB1 in nasopharyngeal carcinoma. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(2), 622-629.
[PMID: 30720170]
[73]
Liu, C.; Li, G.; Ren, S.; Su, Z.; Wang, Y.; Tian, Y.; Liu, Y.; Qiu, Y. miR-185-3p regulates the invasion and metastasis of nasopharyngeal carcinoma by targeting WNT2B in vitro. Oncol. Lett., 2017, 13(4), 2631-2636.
[http://dx.doi.org/10.3892/ol.2017.5778] [PMID: 28454443]
[74]
Li, G.; Wang, Y.; Liu, Y.; Su, Z.; Liu, C.; Ren, S.; Deng, T.; Huang, D.; Tian, Y.; Qiu, Y. miR-185-3p regulates nasopharyngeal carcinoma radioresistance by targeting WNT2B in vitro. Cancer Sci., 2014, 105(12), 1560-1568.
[http://dx.doi.org/10.1111/cas.12555] [PMID: 25297925]
[75]
Jiang, N.; Jiang, X.; Chen, Z.; Song, X.; Wu, L.; Zong, D.; Song, D.; Yin, L.; Wang, D.; Chen, C.; Bian, X.; He, X. MiR-203a-3p suppresses cell proliferation and metastasis through inhibiting LASP1 in nasopharyngeal carcinoma. J. Exp. Clin. Cancer Res., 2017, 36(1), 138.
[http://dx.doi.org/10.1186/s13046-017-0604-3] [PMID: 28982387]
[76]
Huang, Z.; Zhang, S.; Wang, J.; Sun, H.; Zhang, Y.; Li, X.; Song, X. miR-373 inhibits nasopharyngeal carcinoma cell migration and invasion by targeting MARCH5. Int. J. Clin. Exp. Pathol., 2019, 12(7), 2646-2652.
[PMID: 31934093]
[77]
Liu, N.; Jiang, N.; Guo, R.; Jiang, W.; He, Q-M.; Xu, Y-F.; Li, Y-Q.; Tang, L-L.; Mao, Y-P.; Sun, Y.; Ma, J. MiR-451 inhibits cell growth and invasion by targeting MIF and is associated with survival in nasopharyngeal carcinoma. Mol. Cancer, 2013, 12(1), 123.
[http://dx.doi.org/10.1186/1476-4598-12-123] [PMID: 24138931]
[78]
Zhang, T.; Sun, Q.; Liu, T.; Chen, J.; Du, S.; Ren, C.; Liao, G.; Yuan, Y. MiR-451 increases radiosensitivity of nasopharyngeal carcinoma cells by targeting ras-related protein 14 (RAB14). Tumour Biol., 2014, 35(12), 12593-12599.
[http://dx.doi.org/10.1007/s13277-014-2581-x] [PMID: 25201065]
[79]
Liu, B.; Tan, Z.; Jiang, Y.; Chen, Y.; Chen, Y.; Ling, K. Correlation between the expression of miR150 and FOXO4 and the local recurrence and metastasis of nasopharyngeal carcinoma after intensive radiotherapy. J. BUON, 2018, 23(6), 1671-1678.
[PMID: 30610793]
[80]
Lai-Sheung, Chan; On-Ying, Man; Hoi-Hin, Kwok The Wnt modulator ICG-001 mediates the inhibition of nasopharyngeal carcinoma cell migration in vitro via the miR-150/CD44 axis. Int. J. Oncol., 2019, 54, 1010-1020.
[81]
Chan, L-S.; Lung, H-L.; Ngan, R.K-C.; Lee, A.W-M.; Tsao, S.W.; Lo, K-W.; Kahn, M.; Lung, M.L.; Wieser, R.; Mak, N-K. Role of miR-96/EVI1/miR-449a axis in the nasopharyngeal carcinoma cell migration and tumor sphere formation. Int. J. Mol. Sci., 2020, 21(15), 5495.
[http://dx.doi.org/10.3390/ijms21155495] [PMID: 32752071]
[82]
Kang, M.; Xiao, J.; Wang, J.; Zhou, P.; Wei, T.; Zhao, T.; Wang, R. MiR-24 enhances radiosensitivity in nasopharyngeal carcinoma by targeting SP1. Cancer Med., 2016, 5(6), 1163-1173.
[http://dx.doi.org/10.1002/cam4.660] [PMID: 26922862]
[83]
Xu, M.; Tian, G-L.; Hao, C-C.; Shi, M.; Zha, D-J.; Liang, K. MicroRNA-29 targets FGF2 and inhibits the proliferation, migration and invasion of nasopharyngeal carcinoma cells via PI3K/AKT signaling pathway. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(12), 5215-5222.
[PMID: 31298371]
[84]
Yu, D.; Han, G.H.; Zhao, X.; Liu, X.; Xue, K.; Wang, D.; Xu, C.B. MicroRNA-129-5p suppresses nasopharyngeal carcinoma lymphangiogenesis and lymph node metastasis by targeting ZIC2. Cell Oncol. (Dordr.), 2020, 43(2), 249-261.
[http://dx.doi.org/10.1007/s13402-019-00485-5] [PMID: 31884576]
[85]
Bao, L.; You, B.; Shi, S.; Shan, Y.; Zhang, Q.; Yue, H.; Zhang, J.; Zhang, W.; Shi, Y.; Liu, Y.; Wang, X.; Liu, D.; You, Y. Metastasis-associated miR-23a from nasopharyngeal carcinoma-derived exosomes mediates angiogenesis by repressing a novel target gene TSGA10. Oncogene, 2018, 37(21), 2873-2889.
[http://dx.doi.org/10.1038/s41388-018-0183-6] [PMID: 29520105]
[86]
Yan, L.; Cai, K.; Liang, J.; Liu, H.; Liu, Y.; Gui, J. Interaction between miR-572 and PPP2R2C, and their effects on the proliferation, migration, and invasion of nasopharyngeal carcinoma (NPC) cells. Biochem. Cell Biol., 2017, 95(5), 578-584.
[http://dx.doi.org/10.1139/bcb-2016-0237] [PMID: 28525724]
[87]
Xu, Y.F.; Mao, Y.P.; Li, Y.Q.; Ren, X.Y.; He, Q.M.; Tang, X.R.; Sun, Y.; Liu, N.; Ma, J. MicroRNA-93 promotes cell growth and invasion in nasopharyngeal carcinoma by targeting disabled homolog-2. Cancer Lett., 2015, 363(2), 146-155.
[http://dx.doi.org/10.1016/j.canlet.2015.04.006] [PMID: 25892549]
[88]
Cao, W.; Sun, J. MicroRNA-200c promotes tumor cell proliferation and migration by directly targeting dachshund family transcription factor 1 by the Wnt/β-catenin signaling pathway in nasopharyngeal carcinoma. Anticancer Drugs, 2019, 30(3), 218-224.
[http://dx.doi.org/10.1097/CAD.0000000000000713] [PMID: 30431444]
[89]
He, H.; Liao, X.; Yang, Q.; Liu, Y.; Peng, Y.; Zhong, H.; Yang, J.; Zhang, H.; Yu, Z.; Zuo, Y.; Guan, C.; Xu, Z. MicroRNA-494-3p promotes cell growth, migration, and invasion of nasopharyngeal carcinoma by targeting Sox7. Technol. Cancer Res. Treat., 2018, 17, 1533033818809993.
[http://dx.doi.org/10.1177/1533033818809993] [PMID: 30381030]
[90]
Wang, M.; Jia, M.; Yuan, K. MicroRNA-663b promotes cell proliferation and epithelial mesenchymal transition by directly targeting SMAD7 in nasopharyngeal carcinoma. Exp. Ther. Med., 2018, 16(4), 3129-3134.
[http://dx.doi.org/10.3892/etm.2018.6576] [PMID: 30250517]
[91]
Fang, Y.; Zhu, X.; Wang, J.; Li, N.; Li, D.; Sakib, N.; Sha, Z.; Song, W. MiR-744 functions as a proto-oncogene in nasopharyngeal carcinoma progression and metastasis via transcriptional control of ARHGAP5. Oncotarget, 2015, 6(15), 13164-13175.
[http://dx.doi.org/10.18632/oncotarget.3754] [PMID: 25961434]
[92]
Zheng, Y-Q.; Bai, Y-F.; Yang, S.; Cui, Y-R.; Wang, Y-P.; Hu, W-L. MircoRNA-629 promotes proliferation, invasion and migration of nasopharyngeal carcinoma through targeting PDCD4. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(1), 207-216.
[PMID: 30657562]
[93]
Palamarchuk, A.; Efanov, A.; Maximov, V.; Aqeilan, R.I.; Croce, C.M.; Pekarsky, Y. Akt phosphorylates and regulates Pdcd4 tumor suppressor protein. Cancer Res., 2005, 65(24), 11282-11286.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-3469] [PMID: 16357133]

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