Knockdown of LncRNA PVT1 Inhibits Glioma Progression by Regulating MiR-424 Expression

Overview

Journal Oncol Res

Specialty Oncology

Date 2019 Mar 6

PMID 30832754

Citations 19

Authors

Yanjie Han

Xinxin Li

Fei He

Jiliang Yan

Chunyan Ma

Xiaoli Zheng

Jinli Zhang

Donghui Zhang

Cuiping Meng

Zhen Zhang

Xinying Ji

Affiliations

Soon will be listed here.

Abstract

Plasmacytoma variability translocation 1 (PVT1), an oncogene, has been reported to be highly expressed in many tumors, including human glioma, gastric cancer, and non-small cell lung cancer. Functionally, it could also regulate the development of tumor cells. However, its specific roles and pathogenesis in human gliomas are still not clear. This study investigated the function and mechanism of PVT1 knockdown in the proliferation and malignant transformation of human gliomas. We first examined the expression levels of PVT1 and miR-424 in human glioma tissues and cell lines. We also used gene manipulation techniques to explore the effects of PVT1 knockdown on cell viability, migration, invasion, and miR-424. We found that PVT1 knockdown effectively inhibited cell viability, migration, and invasion of human glioma cells and increased miR-424 expression. Based on the negative correlation between PVT1 and miR-424, we then confirmed the direct interaction between PVT1 and miR-424 using RNA immunoprecipitation (RIP) and luciferase reporter assays. Further, we established a xenograft nude mouse model to determine the role and mechanism of PVT1 on tumor growth in vivo. In addition, PVT1 knockdown was shown to promote miR-424 in vivo. In summary, the present study demonstrated that PVT1 knockdown could negatively regulate miR-424 to inhibit human glioma cell activity, migration, and invasiveness. PVT1 knockdown could negatively regulate miR-424 to inhibit cellular activity, migration, and invasiveness in human gliomas, which explained the oncogenic mechanism of PVT1 in human gliomas. It also suggested that PVT1 might be a novel therapeutic target for human gliomas.

Citing Articles

LncRNA MIR600HG inhibits laryngeal cancer development by mediating the miR-424-5p/BTG2 axis.

Zhu X, Zhong M, Wang Q, Zhang M Cancer Sci. 2024; 116(2):544-558.

PMID: 39618050 PMC: 11786319. DOI: 10.1111/cas.16404.

New sights on long non-coding RNAs in glioblastoma: A review of molecular mechanism.

Bagheri-Mohammadi S, Karamivandishi A, Mahdavi S, Siahposht-Khachaki A Heliyon. 2024; 10(21):e39744.

PMID: 39553554 PMC: 11564028. DOI: 10.1016/j.heliyon.2024.e39744.

Roles of LncRNAs in the Pathogenesis of Pulmonary Hypertension.

Liu T, Xu S, Yang J, Xing X Rev Cardiovasc Med. 2024; 25(6):217.

PMID: 39076325 PMC: 11270120. DOI: 10.31083/j.rcm2506217.

LncRNA INHEG promotes glioma stem cell maintenance and tumorigenicity through regulating rRNA 2'-O-methylation.

Liu L, Liu Z, Liu Q, Wu W, Lin P, Liu X Nat Commun. 2023; 14(1):7526.

PMID: 37980347 PMC: 10657414. DOI: 10.1038/s41467-023-43113-5.

Unraveling the role of disulfidptosis-related LncRNAs in colon cancer: a prognostic indicator for immunotherapy response, chemotherapy sensitivity, and insights into cell death mechanisms.

Chi H, Huang J, Yan Y, Jiang C, Zhang S, Chen H Front Mol Biosci. 2023; 10:1254232.

PMID: 37916187 PMC: 10617599. DOI: 10.3389/fmolb.2023.1254232.

References

Cai H, Liu X, Zheng J, Xue Y, Ma J, Xi Z . Long non-coding RNA taurine upregulated 1 enhances tumor-induced angiogenesis through inhibiting microRNA-299 in human glioblastoma. Oncogene. 2016; 36(3):318-331. DOI: 10.1038/onc.2016.212. View

Chen C, Tseng Y, Wu J, Chen G, Lin K, Hwang S . Suppression of hepatocellular carcinoma by baculovirus-mediated expression of long non-coding RNA PTENP1 and MicroRNA regulation. Biomaterials. 2015; 44:71-81. DOI: 10.1016/j.biomaterials.2014.12.023. View

Ho T, Huang J, Zhou N, Zhang Z, Koirala P, Zhou X . Regulation of PCGEM1 by p54/nrb in prostate cancer. Sci Rep. 2016; 6:34529. PMC: 5041109. DOI: 10.1038/srep34529. View

Ding C, Yang Z, Lv Z, Du C, Xiao H, Peng C . Long non-coding RNA PVT1 is associated with tumor progression and predicts recurrence in hepatocellular carcinoma patients. Oncol Lett. 2015; 9(2):955-963. PMC: 4301564. DOI: 10.3892/ol.2014.2730. View

Osada H, Takahashi T . Genetic alterations of multiple tumor suppressors and oncogenes in the carcinogenesis and progression of lung cancer. Oncogene. 2002; 21(48):7421-34. DOI: 10.1038/sj.onc.1205802. View

Guo D, Wang Y, Ren K, Han X . Knockdown of LncRNA PVT1 inhibits tumorigenesis in non-small-cell lung cancer by regulating miR-497 expression. Exp Cell Res. 2017; 362(1):172-179. DOI: 10.1016/j.yexcr.2017.11.014. View

Wheeler D, Wang L . From human genome to cancer genome: the first decade. Genome Res. 2013; 23(7):1054-62. PMC: 3698498. DOI: 10.1101/gr.157602.113. View

Verduci L, Ferraiuolo M, Sacconi A, Ganci F, Vitale J, Colombo T . The oncogenic role of circPVT1 in head and neck squamous cell carcinoma is mediated through the mutant p53/YAP/TEAD transcription-competent complex. Genome Biol. 2017; 18(1):237. PMC: 5738800. DOI: 10.1186/s13059-017-1368-y. View

Santoro F, Mayer D, Klement R, Warczok K, Stukalov A, Barlow D . Imprinted Igf2r silencing depends on continuous Airn lncRNA expression and is not restricted to a developmental window. Development. 2013; 140(6):1184-95. DOI: 10.1242/dev.088849. View

10.

Wang Q, Zhang J, Liu Y, Zhang W, Zhou J, Duan R . A novel cell cycle-associated lncRNA, HOXA11-AS, is transcribed from the 5-prime end of the HOXA transcript and is a biomarker of progression in glioma. Cancer Lett. 2016; 373(2):251-9. DOI: 10.1016/j.canlet.2016.01.039. View

11.

Osborne C, Wilson P, Tripathy D . Oncogenes and tumor suppressor genes in breast cancer: potential diagnostic and therapeutic applications. Oncologist. 2004; 9(4):361-77. DOI: 10.1634/theoncologist.9-4-361. View

12.

Yu Y, Nangia-Makker P, Farhana L, Majumdar A . A novel mechanism of lncRNA and miRNA interaction: CCAT2 regulates miR-145 expression by suppressing its maturation process in colon cancer cells. Mol Cancer. 2017; 16(1):155. PMC: 5622467. DOI: 10.1186/s12943-017-0725-5. View

13.

Yang A, Wang H, Yang X . Long non-coding RNA PVT1 indicates a poor prognosis of glioma and promotes cell proliferation and invasion via target EZH2. Biosci Rep. 2017; 37(6). PMC: 6435466. DOI: 10.1042/BSR20170871. View

14.

Tassone P, Tagliaferri P, Rossi M, Gaspari M, Terracciano R, Venuta S . Genetics and molecular profiling of multiple myeloma: novel tools for clinical management?. Eur J Cancer. 2006; 42(11):1530-8. DOI: 10.1016/j.ejca.2006.04.005. View

15.

Xia T, Liao Q, Jiang X, Shao Y, Xiao B, Xi Y . Long noncoding RNA associated-competing endogenous RNAs in gastric cancer. Sci Rep. 2014; 4:6088. PMC: 4133709. DOI: 10.1038/srep06088. View

16.

Kurtz A, Aigner A, Cabal-Manzano R, Butler R, Hood D, Sessions R . Differential regulation of a fibroblast growth factor-binding protein during skin carcinogenesis and wound healing. Neoplasia. 2004; 6(5):595-602. PMC: 1531664. DOI: 10.1593/neo.04214. View

17.

Zou H, Wu L, Yang Y, Li S, Mei Y, Liu Y . lncRNAs PVT1 and HAR1A are prognosis biomarkers and indicate therapy outcome for diffuse glioma patients. Oncotarget. 2017; 8(45):78767-78780. PMC: 5667997. DOI: 10.18632/oncotarget.20226. View

18.

Jin C, Li M, Ouyang Y, Tan Z, Jiang Y . MiR-424 functions as a tumor suppressor in glioma cells and is down-regulated by DNA methylation. J Neurooncol. 2017; 133(2):247-255. DOI: 10.1007/s11060-017-2438-4. View

19.

Liu C, Chang C, Hsueh K, Su H, Chiou T, Lin S . Migration/Invasion of Malignant Gliomas and Implications for Therapeutic Treatment. Int J Mol Sci. 2018; 19(4). PMC: 5979613. DOI: 10.3390/ijms19041115. View

20.

Shen C, Cheng Y, Wang C . LncRNA PVT1 epigenetically silences miR-195 and modulates EMT and chemoresistance in cervical cancer cells. J Drug Target. 2017; 25(7):637-644. DOI: 10.1080/1061186X.2017.1307379. View