Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

Hsa_circ_0001687 Function as a ceRNA to Facilitate Hepatocellular Carcinoma Progression via miR-140- 3p/FOXQ1 Axis

Author(s): Song You, Niangmei Cheng, Fei Wang, Xiaoyuan Zheng, Yingchao Wang, Bixing Zhao* and Jingfeng Liu*

Volume 30, Issue 11, 2023

Published on: 20 October, 2023

Page: [930 - 940] Pages: 11

DOI: 10.2174/0109298665238824231012072118

Price: $65

Abstract

Background: Increasingly convincing evidence has revealed that circular RNAs (circRNAs) are critical regulatory components of hepatocellular carcinoma (HCC) genesis. However, the expression of circRNAs in HCC and the relevance of circRNAs to HCC progression remain largely unexplained.

Methods: qRT-PCR or western blotting was utilized to confirm circ_0001687, miR-140-3p, and Forkhead Box q1 (FOXQ1) levels in HCC tissues or cells. Cell proliferation ability was evaluated via CCK-8 and colony formation assay. The correlation of circ_0001687 or FOXQ1 and miR-140- 3p was determined using dual luciferase reporter assay. Nude mice xenograft tumor model was constructed to verify the effect of circ_0001687 on tumor growth.

Results: Circ_0001687 was elevated in HCC. Function assays and the nude mice xenograft tumor model indicated that circ_0001687 acts as a promoting gene in HCC to regulate the proliferation of the tumor cell and foster tumor growth. Further mechanistic exploration revealed that the tumor growth-promoting mechanism of circ_0001687 relied on blocking the inhibitory effect of miR-140- 3p on FOXQ1 and activating FOXQ1 expression.

Conclusion: This research indicated the role of circ_0001687/miR-140-3p/FOXQ1 network in regulating HCC development. These may provide new insights into the treatment of HCC.

Graphical Abstract

[1]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[2]
Li, S.; Yang, F.; Ren, X. Immunotherapy for hepatocellular carcinoma. Drug Discov. Ther., 2015, 9(5), 363-371.
[http://dx.doi.org/10.5582/ddt.2015.01054] [PMID: 26632545]
[3]
Huang, A.; Yang, X.R.; Chung, W.Y.; Dennison, A.R.; Zhou, J. Targeted therapy for hepatocellular carcinoma. Signal Transduct. Target. Ther., 2020, 5(1), 146.
[http://dx.doi.org/10.1038/s41392-020-00264-x] [PMID: 32782275]
[4]
Giraud, J.; Chalopin, D.; Blanc, J.F.; Saleh, M. Hepatocellular carcinoma immune landscape and the potential of immunotherapies. Front. Immunol., 2021, 12, 655697.
[http://dx.doi.org/10.3389/fimmu.2021.655697] [PMID: 33815418]
[5]
Villanueva, A. Hepatocellular carcinoma. N. Engl. J. Med., 2019, 380(15), 1450-1462.
[http://dx.doi.org/10.1056/NEJMra1713263] [PMID: 30970190]
[6]
Chen, L.L. The biogenesis and emerging roles of circular RNAs. Nat. Rev. Mol. Cell Biol., 2016, 17(4), 205-211.
[http://dx.doi.org/10.1038/nrm.2015.32] [PMID: 26908011]
[7]
Li, S.; Han, L. Circular RNAs as promising biomarkers in cancer: Detection, function, and beyond. Genome Med., 2019, 11(1), 15.
[http://dx.doi.org/10.1186/s13073-019-0629-7] [PMID: 30894216]
[8]
Yu, C.Y.; Li, T.C.; Wu, Y.Y.; Yeh, C.H.; Chiang, W.; Chuang, C.Y.; Kuo, H.C. The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency. Nat. Commun., 2017, 8(1), 1149.
[http://dx.doi.org/10.1038/s41467-017-01216-w] [PMID: 29074849]
[9]
Jin, C.; Zhao, J.; Zhang, Z.P.; Wu, M.; Li, J.; Liu, B.; Bin, Liao X. Liao, Y.X.; Liu, J.P. CircRNA EPHB4 modulates stem properties and proliferation of gliomas via sponging miR-637 and up-regulating SOX10. Mol. Oncol., 2021, 15(2), 596-622.
[http://dx.doi.org/10.1002/1878-0261.12830] [PMID: 33085838]
[10]
Li, L.; Guo, L.; Yin, G.; Yu, G.; Zhao, Y.; Pan, Y. Upregulation of circular RNA circ_0001721 predicts unfavorable prognosis in osteosarcoma and facilitates cell progression via sponging miR-569 and miR-599. Biomed. Pharmacother., 2019, 109, 226-232.
[http://dx.doi.org/10.1016/j.biopha.2018.10.072] [PMID: 30396080]
[11]
Ding, L.; Wang, R.; Zheng, Q.; Shen, D.; Wang, H.; Lu, Z.; Luo, W.; Xie, H.; Ren, L.; Jiang, M.; Yu, C.; Zhou, Z.; Lin, Y.; Lu, H.; Xue, D.; Su, W.; Xia, L.; Neuhaus, J.; Cheng, S.; Li, G. circPDE5A regulates prostate cancer metastasis via controlling WTAP-dependent N6-methyladenisine methylation of EIF3C mRNA. J. Exp. Clin. Cancer Res., 2022, 41(1), 187.
[http://dx.doi.org/10.1186/s13046-022-02391-5] [PMID: 35650605]
[12]
Wang, Z.; Ma, K.; Pitts, S.; Cheng, Y.; Liu, X.; Ke, X.; Kovaka, S.; Ashktorab, H.; Smoot, D.T.; Schatz, M.; Wang, Z.; Meltzer, S.J. Novel circular RNA circNF1 acts as a molecular sponge, promoting gastric cancer by absorbing miR-16. Endocr. Relat. Cancer, 2019, 26(3), 265-277.
[http://dx.doi.org/10.1530/ERC-18-0478] [PMID: 30576282]
[13]
Chen, T.; Yang, Z.; Liu, C.; Wang, L.; Yang, J.; Chen, L.; Li, W. Circ_0078767 suppresses non‐small‐cell lung cancer by protecting RASSF1A expression via sponging miR‐330‐3p. Cell Prolif., 2019, 52(2), e12548.
[http://dx.doi.org/10.1111/cpr.12548] [PMID: 30507050]
[14]
Zhao, W.; Cui, Y.; Liu, L.; Qi, X.; Liu, J.; Ma, S.; Hu, X.; Zhang, Z.; Wang, Y.; Li, H.; Wang, Z.; Liu, Z.; Wu, J. Splicing factor derived circular RNA circUHRF1 accelerates oral squamous cell carcinoma tumorigenesis via feedback loop. Cell Death Differ., 2020, 27(3), 919-933.
[http://dx.doi.org/10.1038/s41418-019-0423-5] [PMID: 31570856]
[15]
Huang, X.Y.; Zhang, P.F.; Wei, C.Y.; Peng, R.; Lu, J.C.; Gao, C.; Cai, J.B.; Yang, X.; Fan, J.; Ke, A.W.; Zhou, J.; Shi, G.M. Circular RNA circMET drives immunosuppression and anti-PD1 therapy resistance in hepatocellular carcinoma via the miR-30-5p/snail/DPP4 axis. Mol. Cancer, 2020, 19(1), 92.
[http://dx.doi.org/10.1186/s12943-020-01213-6] [PMID: 32430013]
[16]
Xu, J.Z.; Shao, C.C.; Wang, X.J.; Zhao, X.; Chen, J.Q.; Ouyang, Y.X.; Feng, J.; Zhang, F.; Huang, W.H.; Ying, Q.; Chen, C.F.; Wei, X.L.; Dong, H.Y.; Zhang, G.J.; Chen, M. circTADA2As suppress breast cancer progression and metastasis via targeting miR-203a-3p/SOCS3 axis. Cell Death Dis., 2019, 10(3), 175.
[http://dx.doi.org/10.1038/s41419-019-1382-y] [PMID: 30787278]
[17]
Hansen, T.B.; Jensen, T.I.; Clausen, B.H.; Bramsen, J.B.; Finsen, B.; Damgaard, C.K.; Kjems, J. Natural RNA circles function as efficient microRNA sponges. Nature, 2013, 495(7441), 384-388.
[http://dx.doi.org/10.1038/nature11993] [PMID: 23446346]
[18]
Yu, J.; Xu, Q.; Wang, Z.; Yang, Y.; Zhang, L.; Ma, J.; Sun, S.; Yang, F.; Zhou, W. Circular RNA cSMARCA5 inhibits growth and metastasis in hepatocellular carcinoma. J. Hepatol., 2018, 68(6), 1214-1227.
[http://dx.doi.org/10.1016/j.jhep.2018.01.012] [PMID: 29378234]
[19]
Gao, C.; Wen, Y.; Jiang, F.; Gu, X.; Zhu, X. Circular RNA circ_0008274 upregulates granulin to promote the progression of hepatocellular carcinoma via sponging microRNA -140-3p. Bioengineered, 2021, 12(1), 1890-1901.
[http://dx.doi.org/10.1080/21655979.2021.1926195] [PMID: 34002672]
[20]
Yang, J.; Qi, M.; Fei, X.; Wang, X.; Wang, K. Hsa_circRNA_0088036 acts as a ceRNA to promote bladder cancer progression by sponging miR-140-3p. Cell Death Dis., 2022, 13(4), 322.
[http://dx.doi.org/10.1038/s41419-022-04732-w] [PMID: 35396504]
[21]
Han, S.; Shi, Y.; Sun, L.; Liu, Z.; Song, T.; Liu, Q. MiR-4319 induced an inhibition of epithelial-mesenchymal transition and prevented cancer stemness of HCC through targeting FOXQ1. Int. J. Biol. Sci., 2019, 15(13), 2936-2947.
[http://dx.doi.org/10.7150/ijbs.38000] [PMID: 31853229]
[22]
Yang, F.; Fang, E.; Mei, H.; Chen, Y.; Li, H.; Li, D.; Song, H.; Wang, J.; Hong, M.; Xiao, W.; Wang, X.; Huang, K.; Zheng, L.; Tong, Q. Cis -Acting circ-CTNNB1 Promotes β-Catenin Signaling and Cancer Progression via DDX3-Mediated Transactivation of YY1. Cancer Res., 2019, 79(3), 557-571.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-1559] [PMID: 30563889]
[23]
Li, Y.; Zheng, F.; Xiao, X.; Xie, F.; Tao, D.; Huang, C.; Liu, D.; Wang, M.; Wang, L.; Zeng, F.; Jiang, G. Circ HIPK 3 sponges miR-558 to suppress heparanase expression in bladder cancer cells. EMBO Rep., 2017, 18(9), 1646-1659.
[http://dx.doi.org/10.15252/embr.201643581] [PMID: 28794202]
[24]
Song, T.; Xu, A.; Zhang, Z.; Gao, F.; Zhao, L.; Chen, X.; Gao, J.; Kong, X. CircRNA hsa_circRNA_101996 increases cervical cancer proliferation and invasion through activating TPX2 expression by restraining miR-8075. J. Cell. Physiol., 2019, 234(8), 14296-14305.
[http://dx.doi.org/10.1002/jcp.28128] [PMID: 30633364]
[25]
Yu, M.C.; Ding, G.Y.; Ma, P.; Chen, Y.D.; Zhu, X.D.; Cai, J.B.; Shen, Y.H.; Zhou, J.; Fan, J.; Sun, H.C.; Kuang, M.; Huang, C. CircRNA UBAP2 serves as a sponge of miR-1294 to increase tumorigenesis in hepatocellular carcinoma through regulating c-Myc expression. Carcinogenesis, 2021, 42(10), 1293-1303.
[http://dx.doi.org/10.1093/carcin/bgab068] [PMID: 34314478]
[26]
Cheng, Z.; Yu, C.; Cui, S.; Wang, H.; Jin, H.; Wang, C.; Li, B.; Qin, M.; Yang, C.; He, J.; Zuo, Q.; Wang, S.; Liu, J.; Ye, W.; Lv, Y.; Zhao, F.; Yao, M.; Jiang, L.; Qin, W. circTP63 functions as a ceRNA to promote lung squamous cell carcinoma progression by upregulating FOXM1. Nat. Commun., 2019, 10(1), 3200.
[http://dx.doi.org/10.1038/s41467-019-11162-4] [PMID: 31324812]
[27]
Huang, H.; Wang, Y.; Li, Q.; Fei, X.; Ma, H.; Hu, R. miR-140-3p functions as a tumor suppressor in squamous cell lung cancer by regulating BRD9. Cancer Lett., 2019, 446, 81-89.
[http://dx.doi.org/10.1016/j.canlet.2019.01.007] [PMID: 30660651]
[28]
Wang, Z.; Chen, K.; Li, D.; Chen, M.; Li, A.; Wang, J. miR-140-3p is involved in the occurrence and metastasis of gastric cancer by regulating the stability of FAM83B. Cancer Cell Int., 2021, 21(1), 537.
[http://dx.doi.org/10.1186/s12935-021-02245-8] [PMID: 34656115]
[29]
Zhou, Y.; Wang, B.; Wang, Y.; Chen, G.; Lian, Q.; Wang, H. miR 140 3p inhibits breast cancer proliferation and migration by directly regulating the expression of tripartite motif 28. Oncol. Lett., 2019, 17(4), 3835-3841.
[http://dx.doi.org/10.3892/ol.2019.10038] [PMID: 30881504]
[30]
Zhang, H.; Meng, F.; Liu, G.; Zhang, B.; Zhu, J.; Wu, F.; Ethier, S.P.; Miller, F.; Wu, G. Forkhead transcription factor foxq1 promotes epithelial-mesenchymal transition and breast cancer metastasis. Cancer Res., 2011, 71(4), 1292-1301.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-2825] [PMID: 21285253]
[31]
Yang, M.; Liu, Q.; Dai, M.; Peng, R.; Li, X.; Zuo, W.; Gou, J.; Zhou, F.; Yu, S.; Liu, H.; Huang, M. FOXQ1-mediated SIRT1 upregulation enhances stemness and radio-resistance of colorectal cancer cells and restores intestinal microbiota function by promoting β-catenin nuclear translocation. J. Exp. Clin. Cancer Res., 2022, 41(1), 70.
[http://dx.doi.org/10.1186/s13046-021-02239-4] [PMID: 35183223]
[32]
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]
[33]
Bartel, D.P. MicroRNAs: Target recognition and regulatory functions. Cell, 2009, 136(2), 215-233.
[http://dx.doi.org/10.1016/j.cell.2009.01.002] [PMID: 19167326]
[34]
Wang, Y.; Chen, J.; Wang, X.; Wang, K. miR-140-3p inhibits bladder cancer cell proliferation and invasion by targeting FOXQ1. Aging, 2020, 12(20), 20366-20379.
[http://dx.doi.org/10.18632/aging.103828] [PMID: 33098639]

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