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Current Molecular Pharmacology

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

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Research Article

H19/miR-675-5p Targeting SFN Enhances the Invasion and Metastasis of Nasalpharyngeal Cancer Cells

Author(s): Ting Zhang, Fanghong Lei, Tao Jiang, Lisha Xie, Pin Huang, Pei Li, Yun Huang, Xia Tang, Jie Gong, Yunpeng Lin, Ailan Cheng* and Weiguo Huang*

Volume 12, Issue 4, 2019

Page: [324 - 333] Pages: 10

DOI: 10.2174/1874467212666190719120446

Price: $65

Abstract

Aims: The aim is to study the role of miR-675-5p coded by long non-coding RNA H19 in the development of Nasopharyngeal Cancer (NPC) and whether miR-675-5p regulates the invasion and metastasis of NPC through targeting SFN (14-3-3σ). The study further validated the relationship between H19, miR-675-5p and SFN in NPC and their relationship with the invasion and metastasis of NPC.

Methods: Western blot was used to detect the expression of 14-3-3σ protein in immortalized normal nasopharyngeal epithelial cells NP69 and different metastatic potential NPC cells, 6-10B and 5-8F. At the same time, to find out the relationship between 14-3-3σ protein and the expression of H19 and miR-675-5p, the expression of H19 and miR-675-5p in normal nasopharynx epithelial cells NP69 and varied nasopharyngeal carcinoma cells 6-10B and 5-8F were quantified by real-time PCR. MiR-675-5p mimic and inhibitor were transfected into NPC 6-10B to over-express and down-express miR-675-5p; miR-675-5p mimic negative control and inhibitor negative control were transfected into NPC 6-10B as control groups. The effect of over-expression and down-expression by miR-675-5p on the expression of 14-3-3σ protein was detected by Western blotting. The 3’-UTR segments of SFN, containing miR-675-5p binding sites were amplified by PCR and the luciferase activity in the transfected cells was assayed to detect whether SFN is the direct target of miR-675-5p. Transwell and scratch assays were used to verify the changes in NPC invasion and metastasis ability of mimics and inhibitors transfected with miR-675-5p.

Results: The expression of 14-3-3σ protein in normal nasopharynx epithelial cells NP69 is significantly higher than in varied nasopharyngeal carcinoma cells, 6-10B and 5-8F (P<0.05), and the 14-3-3σ protein levels in low-metastatic nasopharyngeal carcinoma cell 6-10B is higher than in high-metastatic nasopharyngeal carcinoma cell 5-8F. The expression of H19 and miR-675-5p are significantly higher in NPC cells than in NP69 cell (P<0.05). The expression of H19 and miR-675-5p in high-Metastatic nasopharyngeal carcinoma cell 5-8F was higher than in low-Metastatic nasopharyngeal carcinoma cell 6-10B. The expression of 14-3-3σ protein in miR-675-5p mimic cells was significantly lower than in mimic NC (negative control) group and blank control group. However, compared with the blank control group, mimic NC showed no significant difference in 14-3-3σ protein between the two groups. The miR-675-5p inhibitor group was significantly higher than the inhibitor NC group and the blank control group (p<0.05), but there was no significant difference in the expression of 14-3-3σ protein in the inhibitor NC group and the blank control group (p>0.05). Dual-luciferase reporter assay system shows the 3’-UTR segments of SFN containing miR-675-5p binding sites. SFN was the target gene of miR-675-5p.

Conclusion: 14-3-3σ is downregulated in NPC and is involved in the development of NPC. H19 and miR- 675-5p are upregulated in NPC, which is related to the development of NPC. The over-expression of miR- 675-5p inhibits the expression of 14-3-3σ protein. SFN is the target gene of miR-675-5p. MiR-675-5p targets SFN, downregulates its protein expression and promotes the invasion and metastasis of NPC.

Keywords: NPC, miR-675-5p, 14-3-3σ, invasion, metastasis, nasalpharyngeal, cancer cells.

Graphical Abstract

[1]
Zong, Y. Pathological study of NPC. Chinese Journal of Pathology, 2003, 32(1), 65-68.
[2]
Zou, X.; Wang, S.L.; Liu, Y.P.; Liu, Y.L.; Zou, R.H.; Zhang, Y.N.; You, R.; Yang, Q.; Xie, Y.L.; Lin, M.; Huang, P.Y.; Jiang, R.; Zhang, M.X.; Qian, C.N.; Mai, H.Q.; Guo, L.; Hong, M.H.; Chen, M.Y. A curative-intent endoscopic surgery for postradiation nasopharyngeal necrosis in patients with nasopharyngeal carcinoma. Cancer Commun (Lond), 2018, 38(1), 74.
[http://dx.doi.org/10.1186/s40880-018-0338-4] [PMID: 30577735]
[3]
Colaco, R.J.; Betts, G.; Donne, A.; Swindell, R.; Yap, B.K.; Sykes, A.J.; Slevin, N.J.; Homer, J.J.; Lee, L.W. Nasopharyngeal carcinoma: a retrospective review of demographics, treatment and patient outcome in a single centre. Clin. Oncol. (R. Coll. Radiol.), 2013, 25(3), 171-177.
[http://dx.doi.org/10.1016/j.clon.2012.10.006] [PMID: 23337060]
[4]
Tran, N.; Abhyankar, V.; Nguyen, K.; Weidanz, J.; Gao, J. MicroRNA dysregulational synergistic network: discovering microRNA dysregulatory modules across subtypes in non-small cell lung cancers. BMC Bioinformatics, 2018, 19(Suppl. 20), 504.
[http://dx.doi.org/10.1186/s12859-018-2536-0] [PMID: 30577741]
[5]
Wan, Y.; Qu, K.; Zhang, Q.C.; Flynn, R.A.; Manor, O.; Ouyang, Z.; Zhang, J.; Spitale, R.C.; Snyder, M.P.; Segal, E.; Chang, H.Y. Landscape and variation of RNA secondary structure across the human transcriptome. Nature, 2014, 505(7485), 706-709.
[http://dx.doi.org/10.1038/nature12946] [PMID: 24476892]
[6]
Okumura, H.; Kita, Y.; Yokomakura, N.; Uchikado, Y.; Setoyama, T.; Sakurai, H.; Omoto, I.; Matsumoto, M.; Owaki, T.; Ishigami, S.; Natsugoe, S. Nuclear expression of 14-3-3 σ is related to prognosis in patients with esophageal squamous cell carcinoma. Anticancer Res., 2010, 30(12), 5175-5179.
[PMID: 21187508]
[7]
Li, Y.L.; Liu, L.; Xiao, Y.; Zeng, T.; Zeng, C. 14-3-3σ is an independent prognostic biomarker for gastric cancer and is associated with apoptosis and proliferation in gastric cancer. Oncol. Lett., 2015, 9(1), 290-294.
[http://dx.doi.org/10.3892/ol.2014.2676] [PMID: 25435977]
[8]
Meng, L.; Hsu, J.K.; Tsai, R.Y. GNL3L depletion destabilizes MDM2 and induces p53-dependent G2/M arrest. Oncogene, 2011, 30(14), 1716-1726.
[http://dx.doi.org/10.1038/onc.2010.550] [PMID: 21132010]
[9]
Huang, W.G.; Cheng, A.L.; Chen, Z.C.; Peng, F.; Zhang, P.F.; Li, M.Y.; Li, F.; Li, J.L.; Li, C.; Yi, H.; Li, X.H.; Yi, B.; Xiao, Z.Q. Targeted proteomic analysis of 14-3-3σ in nasopharyngeal carcinoma. Int. J. Biochem. Cell Biol., 2010, 42(1), 137-147.
[http://dx.doi.org/10.1016/j.biocel.2009.10.001] [PMID: 19828132]
[10]
Cheng, A.L.; Huang, W.G.; Chen, Z.C.; Peng, F.; Zhang, P.F.; Li, M.Y.; Li, F.; Li, J.L.; Li, C.; Yi, H.; Yi, B.; Xiao, Z.Q. Identification of novel nasopharyngeal carcinoma biomarkers by laser capture microdissection and proteomic analysis. Clin. Cancer Res., 2008, 14(2), 435-445.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-1215] [PMID: 18223218]
[11]
Yi, B.; Tan, S.X.; Tang, C.E.; Huang, W.G.; Cheng, A.L.; Li, C.; Zhang, P.F.; Li, M.Y.; Li, J.L.; Yi, H.; Peng, F.; Chen, Z.C.; Xiao, Z.Q. Inactivation of 14-3-3 σ by promoter methylation correlates with metastasis in nasopharyngeal carcinoma. J. Cell. Biochem., 2009, 106(5), 858-866.
[http://dx.doi.org/10.1002/jcb.22051] [PMID: 19160382]
[12]
Raveh, E.; Matouk, I.J.; Gilon, M.; Hochberg, A. The H19 Long non-coding RNA in cancer initiation, progression and metastasis - a proposed unifying theory. Mol. Cancer, 2015, 14(1), 184.
[http://dx.doi.org/10.1186/s12943-015-0458-2] [PMID: 26536864]
[13]
Liang, W.C.; Fu, W.M.; Wong, C.W.; Wang, Y.; Wang, W.M.; Hu, G.X.; Zhang, L.; Xiao, L.J.; Wan, D.C.; Zhang, J.F.; Waye, M.M. The lncRNA H19 promotes epithelial to mesenchymal transition by functioning as miRNA sponges in colorectal cancer. Oncotarget, 2015, 6(26), 22513-22525.
[http://dx.doi.org/10.18632/oncotarget.4154] [PMID: 26068968]
[14]
Yan, J.; Zhang, Y.; She, Q.; Li, X.; Peng, L.; Wang, X.; Liu, S.; Shen, X.; Zhang, W.; Dong, Y.; Lu, J.; Zhang, G. Long Noncoding RNA H19/miR-675 Axis Promotes Gastric Cancer via FADD/Caspase 8/Caspase 3 Signaling Pathway. Cell. Physiol. Biochem., 2017, 42(6), 2364-2376.
[http://dx.doi.org/10.1159/000480028] [PMID: 28848149]
[15]
Qian, B.; Wang, D.M.; Gu, X.S.; Zhou, K.; Wu, J.; Zhang, C.Y.; He, X.Y. LncRNA H19 serves as a ceRNA and participates in non-small cell lung cancer development by regulating microRNA-107. Eur. Rev. Med. Pharmacol. Sci., 2018, 22(18), 5946-5953.
[PMID: 30280776]
[16]
Ren, J.; Fu, J.; Ma, T.; Yan, B.; Gao, R.; An, Z.; Wang, D. LncRNA H19-elevated LIN28B promotes lung cancer progression through sequestering miR-196b. Cell Cycle, 2018, 17(11), 1372-1380.
[http://dx.doi.org/10.1080/15384101.2018.1482137] [PMID: 29950144]
[17]
Li, J.; Huang, Y.; Deng, X.; Luo, M.; Wang, X.; Hu, H.; Liu, C.; Zhong, M. Long noncoding RNA H19 promotes transforming growth factor-β-induced epithelial-mesenchymal transition by acting as a competing endogenous RNA of miR-370-3p in ovarian cancer cells. OncoTargets Ther., 2018, 11, 427-440.
[http://dx.doi.org/10.2147/OTT.S149908] [PMID: 29403287]
[18]
Sun, Y.; Zhu, Q.; Yang, W.; Shan, Y.; Yu, Z.; Zhang, Q.; Wu, H. LncRNA H19/miR-194/PFTK1 axis modulates the cell proliferation and migration of pancreatic cancer. J. Cell. Biochem., 2019, 120(3), 3874-3886.
[http://dx.doi.org/10.1002/jcb.27669] [PMID: 30474270]
[19]
Huang, C.; Cao, L.; Qiu, L.; Dai, X.; Ma, L.; Zhou, Y.; Li, H.; Gao, M.; Li, W.; Zhang, Q.; Han, K.; Lv, H. Upregulation of H19 promotes invasion and induces epithelial-to-mesenchymal transition in esophageal cancer. Oncol. Lett., 2015, 10(1), 291-296.
[http://dx.doi.org/10.3892/ol.2015.3165] [PMID: 26171017]
[20]
Kallen, A.N.; Zhou, X.B.; Xu, J.; Qiao, C.; Ma, J.; Yan, L.; Lu, L.; Liu, C.; Yi, J.S.; Zhang, H.; Min, W.; Bennett, A.M.; Gregory, R.I.; Ding, Y.; Huang, Y. The imprinted H19 lncRNA antagonizes let-7 microRNAs. Mol. Cell, 2013, 52(1), 101-112.
[http://dx.doi.org/10.1016/j.molcel.2013.08.027] [PMID: 24055342]
[21]
Matouk, I.; Raveh, E.; Ohana, P.; Lail, R.A.; Gershtain, E.; Gilon, M.; De Groot, N.; Czerniak, A.; Hochberg, A. The increasing complexity of the oncofetal h19 gene locus: functional dissection and therapeutic intervention. Int. J. Mol. Sci., 2013, 14(2), 4298-4316.
[http://dx.doi.org/10.3390/ijms14024298] [PMID: 23429271]
[22]
Cai, X.; Cullen, B.R. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA, 2007, 13(3), 313-316.
[http://dx.doi.org/10.1261/rna.351707] [PMID: 17237358]
[23]
Ma, L.; Tian, X.; Guo, H.; Zhang, Z.; Du, C.; Wang, F.; Xie, X.; Gao, H.; Zhuang, Y.; Kornmann, M.; Gao, H.; Yang, Y. Long noncoding RNA H19 derived miR-675 regulates cell proliferation by down-regulating E2F-1 in human pancreatic ductal adenocarcinoma. J. Cancer, 2018, 9(2), 389-399.
[http://dx.doi.org/10.7150/jca.21347] [PMID: 29344285]
[24]
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]
[25]
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]
[26]
Qu, R.; Sun, Y.; Li, Y.; Hu, C.; Shi, G.; Tang, Y.; Guo, D. MicroRNA-130a-3p suppresses cell viability, proliferation and invasion in nasopharyngeal carcinoma by inhibiting CXCL12. Am. J. Transl. Res., 2017, 9(8), 3586-3598.
[PMID: 28861150]
[27]
Wu, M.; Ye, X.; Wang, S.; Li, Q.; Lai, Y.; Yi, Y. MicroRNA-148b suppresses proliferation, migration, and invasion of nasopharyngeal carcinoma cells by targeting metastasis-associated gene 2. OncoTargets Ther., 2017, 10, 2815-2822.
[http://dx.doi.org/10.2147/OTT.S135664] [PMID: 28652762]
[28]
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]
[29]
Wang, J.G.; Tang, W.P.; Liao, M.C.; Liu, Y.P.; Ai, X.H. MiR-99a suppresses cell invasion and metastasis in nasopharyngeal carcinoma through targeting HOXA1. OncoTargets Ther., 2017, 10, 753-761.
[http://dx.doi.org/10.2147/OTT.S126781] [PMID: 28228659]
[30]
Zhao, J.C.; Shi, Y.; Zhang, Y.; Zhang, X.; Ma, X.; Jia, Z.H.; Wu, Z.J.; Zhang, J.Q. [The expression of MiR-148a in nasopharyngeal carcinoma and its effect on tumor cell biology functions in nasopharyngeal carcinoma] Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi, 2016, 30(15), 1219-1223.
[PMID: 29798333]
[31]
Li, H.; Li, X.; Ge, X.; Jia, L.; Zhang, Z.; Fang, R.; Yang, J.; Liu, J.; Peng, S.; Zhou, M.; Xiang, J.; Zeng, Z.; Zhou, W.; Xiong, W.; Xiao, G.; Fang, L.; Li, G.Y.; Li, Z. MiR-34b-3 and miR-449a inhibit malignant progression of nasopharyngeal carcinoma by targeting lactate dehydrogenase A. Oncotarget, 2016, 7(34), 54838-54851.
[http://dx.doi.org/10.18632/oncotarget.10761] [PMID: 27458165]
[32]
He, Q.; Ren, X.; Chen, J.; Li, Y.; Tang, X.; Wen, X.; Yang, X.; Zhang, J.; Wang, Y.; Ma, J.; Liu, N. miR-16 targets fibroblast growth factor 2 to inhibit NPC cell proliferation and invasion via PI3K/AKT and MAPK signaling pathways. Oncotarget, 2016, 7(3), 3047-3058.
[http://dx.doi.org/10.18632/oncotarget.6504] [PMID: 26655091]
[33]
Lv, L.Y.; Wang, Y.Z.; Zhang, Q.; Zang, H.R.; Wang, X.J. miR-539 induces cell cycle arrest in nasopharyngeal carcinoma by targeting cyclin-dependent kinase 4. Cell Biochem. Funct., 2015, 33(8), 534-540.
[http://dx.doi.org/10.1002/cbf.3152] [PMID: 26559153]
[34]
Pan, X.; Peng, G.; Liu, S.; Sun, Z.; Zou, Z.; Wu, G. MicroRNA-4649-3p inhibits cell proliferation by targeting protein tyrosine phosphatase SHP-1 in nasopharyngeal carcinoma cells. Int. J. Mol. Med., 2015, 36(2), 559-564.
[http://dx.doi.org/10.3892/ijmm.2015.2245] [PMID: 26081980]
[35]
Yang, W.; Lan, X.; Li, D.; Li, T.; Lu, S. MiR-223 targeting MAFB suppresses proliferation and migration of nasopharyngeal carcinoma cells. BMC Cancer, 2015, 15, 461.
[http://dx.doi.org/10.1186/s12885-015-1464-x] [PMID: 26055874]
[36]
Huang, S.; Li, X.; Zhu, H. MicroRNA-152 Targets Phosphatase and Tensin Homolog to Inhibit Apoptosis and Promote Cell Migration of Nasopharyngeal Carcinoma Cells. Med. Sci. Monit., 2016, 22, 4330-4337.
[http://dx.doi.org/10.12659/MSM.898110] [PMID: 27840403]
[37]
Chen, C.; Lu, Z.; Yang, J.; Hao, W.; Qin, Y.; Wang, H.; Xie, C.; Xie, R. MiR-17-5p promotes cancer cell proliferation and tumorigenesis in nasopharyngeal carcinoma by targeting p21. Cancer Med., 2016, 5(12), 3489-3499.
[http://dx.doi.org/10.1002/cam4.863] [PMID: 27774777]
[38]
Yan, H.L.; Li, L.; Li, S.J.; Zhang, H.S.; Xu, W. miR-346 promotes migration and invasion of nasopharyngeal carcinoma cells via targeting BRMS1. J. Biochem. Mol. Toxicol., 2016, 30(12), 602-607.
[http://dx.doi.org/10.1002/jbt.21827] [PMID: 27501413]
[39]
Liu, Y.; Zhao, R.; Wang, H.; Luo, Y.; Wang, X.; Niu, W.; Zhou, Y.; Wen, Q.; Fan, S.; Li, X.; Xiong, W.; Ma, J.; Li, X.; Tan, M.; Li, G.; Zhou, M. miR-141 is involved in BRD7-mediated cell proliferation and tumor formation through suppression of the PTEN/AKT pathway in nasopharyngeal carcinoma. Cell Death Dis., 2016, 7e2156.
[http://dx.doi.org/10.1038/cddis.2016.64] [PMID: 27010857]
[40]
Sun, L.; Meckes, D.G. Jr Methodological Approaches to Study Extracellular Vesicle miRNAs in Epstein(-)Barr Virus-Associated Cancers. Int. J. Mol. Sci., 2018, 19(9)
[http://dx.doi.org/10.3390/ijms19092810]
[41]
Gao, W.; Wong, T.S.; Lv, K.X. Detection of Epstein-Barr virus (EBV)-encoded microRNAs in plasma of patients with nasopharyngeal carcinoma. Head Neck, 2018.
[http://dx.doi.org/10.1002/hed.25544] [PMID: 30548946]
[42]
Matouk, I.J.; Halle, D.; Raveh, E. The role of the oncofetal H19 lncRNA in tumor metastasis: orchestrating the EMT-MET decision. Oncotarget, 2015, 6387.
[PMID: 26623562]
[43]
Zheng, Y.; Lu, X.; Xu, L.; Chen, Z.; Li, Q.; Yuan, J. MicroRNA-675 promotes glioma cell proliferation and motility by negatively regulating retinoblastoma 1. Hum. Pathol., 2017, 69, 63-71.
[http://dx.doi.org/10.1016/j.humpath.2017.09.006] [PMID: 28970140]
[44]
Vennin, C.; Spruyt, N.; Dahmani, F.; Julien, S.; Bertucci, F.; Finetti, P.; Chassat, T.; Bourette, R.P.; Le Bourhis, X.; Adriaenssens, E. H19 non coding RNA-derived miR-675 enhances tumorigenesis and metastasis of breast cancer cells by downregulating c-Cbl and Cbl-b. Oncotarget, 2015, 6(30), 29209-29223.
[http://dx.doi.org/10.18632/oncotarget.4976] [PMID: 26353930]
[45]
Zhai, L.L.; Wang, P.; Zhou, L.Y.; Yin, J.Y.; Tang, Q.; Zhang, T.J.; Wang, Y.X.; Yang, D.Q.; Lin, J.; Deng, Z.Q. Over-expression of miR-675 in formalin-fixed paraffin-embedded (FFPE) tissues of breast cancer patients. Int. J. Clin. Exp. Med., 2015, 8(7), 11195-11201.
[PMID: 26379923]
[46]
Zhuang, M.; Gao, W.; Xu, J.; Wang, P.; Shu, Y. The long non-coding RNA H19-derived miR-675 modulates human gastric cancer cell proliferation by targeting tumor suppressor RUNX1. Biochem. Biophys. Res. Commun., 2014, 448(3), 315-322.
[http://dx.doi.org/10.1016/j.bbrc.2013.12.126] [PMID: 24388988]
[47]
Yang, Y.; Meng, Q.; Wang, C.; Li, X.; Lu, Y.; Xin, X.; Zheng, Q.; Lu, D. MicroRNA 675 cooperates PKM2 to aggravate progression of human liver cancer stem cells induced from embryonic stem cells. J. Mol. Med. (Berl.), 2018, 96(10), 1119-1130.
[http://dx.doi.org/10.1007/s00109-018-1687-9] [PMID: 30140938]
[48]
He, D.; Wang, J.; Zhang, C.; Shan, B.; Deng, X.; Li, B.; Zhou, Y.; Chen, W.; Hong, J.; Gao, Y.; Chen, Z.; Duan, C. Down-regulation of miR-675-5p contributes to tumor progression and development by targeting pro-tumorigenic GPR55 in non-small cell lung cancer. Mol. Cancer, 2015, 14, 73.
[http://dx.doi.org/10.1186/s12943-015-0342-0] [PMID: 25889562]
[49]
Huang, Y.; Zheng, Y.; Jia, L.; Li, W. Long Noncoding RNA H19 Promotes Osteoblast Differentiation Via TGF-β1/Smad3/HDAC Signaling Pathway by Deriving miR-675. Stem Cells, 2015, 33(12), 3481-3492.
[http://dx.doi.org/10.1002/stem.2225] [PMID: 26417995]
[50]
Zhu, M.; Chen, Q.; Liu, X.; Sun, Q.; Zhao, X.; Deng, R.; Wang, Y.; Huang, J.; Xu, M.; Yan, J.; Yu, J. lncRNA H19/miR-675 axis represses prostate cancer metastasis by targeting TGFBI. FEBS J., 2014, 281(16), 3766-3775.
[http://dx.doi.org/10.1111/febs.12902] [PMID: 24988946]

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