MicorRNA-195 Links Long Non-coding RNA SEMA3B Antisense RNA 1 (head to Head) and Cyclin D1 to Regulate the Proliferation of Glioblastoma Cells

Overview

Journal Bioengineered

Date 2022 Mar 15

PMID 35287551

Authors

Kaijun Liu

Yan Deng

Yongxia Yang

Hui Wang

Ping Zhou

Affiliations

Soon will be listed here.

Abstract

Long non-coding RNA (lncRNA) SEMA3B antisense RNA 1 (head to head) (SEMA3B-AS1) is a recently identified tumor suppressor in gastric cancer. However, its role in glioblastoma (GBM) is unclear. This study was conducted to explore the role of SEMA3B-AS1 in GBM. In this study, the expression of SEMA3B-AS1, cyclin D1 and miR-195 were determined by RT-qPCR. Gene interactions were evaluated by dual-luciferase assay and overexpression experiments. BrdU assay was performed to monitor cell proliferation. We observed downregulation of SEMA3B-AS1 in GBM. The expression of SEMA3B-AS1 was inversely correlated with the expression of cyclin D1 but positively correlated with the expression of miR-195. In GBM cells, overexpression of SEMA3B-AS1 and miR-195 caused reduced expression levels of cyclin D1. MiR-195 inhibitor reduced the effects of overexpression of SEMA3B-AS1 on the expression of cyclin D1. Moreover, overexpression of SEMA3B-AS1 increased the expression levels of miR-195. Cell proliferation data showed that, SEMA3B-AS1 and miR-195 decreased cell proliferation, while overexpression of cyclin D1 increased GBM cell proliferation. In addition, miR-195 inhibitor inhibited the role of overexpression of SEMA3B-AS1 in cancer cell proliferation. Moreover, miR-195 interacted with cyclin D1, but not SEMA3B-AS1. Furthermore, SEMA3B-AS1 decreased the methylation of the promoter region of miR-195. Therefore, we concluded that miR-195 links lncRNA SEMA3B-AS1 and cyclin D1 to regulate the proliferation of GBM cells.

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References

Prensner J, Chinnaiyan A . The emergence of lncRNAs in cancer biology. Cancer Discov. 2011; 1(5):391-407. PMC: 3215093. DOI: 10.1158/2159-8290.CD-11-0209. View

Brandes A, Vastola F, Basso U, Berti F, Pinna G, Rotilio A . A prospective study on glioblastoma in the elderly. Cancer. 2003; 97(3):657-62. DOI: 10.1002/cncr.11097. View

Rock K, McArdle O, Forde P, Dunne M, Fitzpatrick D, ONeill B . A clinical review of treatment outcomes in glioblastoma multiforme--the validation in a non-trial population of the results of a randomised Phase III clinical trial: has a more radical approach improved survival?. Br J Radiol. 2012; 85(1017):e729-33. PMC: 3487092. DOI: 10.1259/bjr/83796755. View

Aldape K, Zadeh G, Mansouri S, Reifenberger G, von Deimling A . Glioblastoma: pathology, molecular mechanisms and markers. Acta Neuropathol. 2015; 129(6):829-48. DOI: 10.1007/s00401-015-1432-1. View

Qi P, Zhou X, Du X . Circulating long non-coding RNAs in cancer: current status and future perspectives. Mol Cancer. 2016; 15(1):39. PMC: 4869386. DOI: 10.1186/s12943-016-0524-4. View

Liu Y, Wang L, Chen S, Zong Z, Guan X, Zhao Y . LncRNA ABHD11-AS1 promotes the development of endometrial carcinoma by targeting cyclin D1. J Cell Mol Med. 2018; 22(8):3955-3964. PMC: 6050509. DOI: 10.1111/jcmm.13675. View

Thomson D, Dinger M . Endogenous microRNA sponges: evidence and controversy. Nat Rev Genet. 2016; 17(5):272-83. DOI: 10.1038/nrg.2016.20. View

McNabb D, Reed R, Marciniak R . Dual luciferase assay system for rapid assessment of gene expression in Saccharomyces cerevisiae. Eukaryot Cell. 2005; 4(9):1539-49. PMC: 1214206. DOI: 10.1128/EC.4.9.1539-1549.2005. View

Shan Y, Hsu H, Lai M, Hung Y, Wang C, Yen M . Cyclin D1 overexpression correlates with poor tumor differentiation and prognosis in gastric cancer. Oncol Lett. 2017; 14(4):4517-4526. PMC: 5594254. DOI: 10.3892/ol.2017.6736. View

10.

Paraskevopoulou M, Hatzigeorgiou A . Analyzing MiRNA-LncRNA Interactions. Methods Mol Biol. 2016; 1402:271-286. DOI: 10.1007/978-1-4939-3378-5_21. View

11.

Bhan A, Mandal S . LncRNA HOTAIR: A master regulator of chromatin dynamics and cancer. Biochim Biophys Acta. 2015; 1856(1):151-64. PMC: 4544839. DOI: 10.1016/j.bbcan.2015.07.001. View

12.

Evans J, Feng F, Chinnaiyan A . The bright side of dark matter: lncRNAs in cancer. J Clin Invest. 2016; 126(8):2775-82. PMC: 4966302. DOI: 10.1172/JCI84421. View

13.

Han L, Zhang K, Shi Z, Zhang J, Zhu J, Zhu S . LncRNA proﬁle of glioblastoma reveals the potential role of lncRNAs in contributing to glioblastoma pathogenesis. Int J Oncol. 2012; 40(6):2004-12. DOI: 10.3892/ijo.2012.1413. View

14.

Li X, Gong X, Chen J, Zhang J, Sun J, Guo M . miR-340 inhibits glioblastoma cell proliferation by suppressing CDK6, cyclin-D1 and cyclin-D2. Biochem Biophys Res Commun. 2015; 460(3):670-7. DOI: 10.1016/j.bbrc.2015.03.088. View

15.

Kato J, Sherr C . Inhibition of granulocyte differentiation by G1 cyclins D2 and D3 but not D1. Proc Natl Acad Sci U S A. 1993; 90(24):11513-7. PMC: 48014. DOI: 10.1073/pnas.90.24.11513. View

16.

Wu Z . MiR-195 connects lncRNA RUNX1-IT1 and cyclin D1 to regulate the proliferation of glioblastoma cells. Int J Neurosci. 2021; 133(1):13-18. DOI: 10.1080/00207454.2021.1881090. View

17.

Guo W, Liang X, Liu L, Guo Y, Shen S, Liang J . MiR-6872 host gene SEMA3B and its antisense lncRNA SEMA3B-AS1 function synergistically to suppress gastric cardia adenocarcinoma progression. Gastric Cancer. 2019; 22(4):705-722. DOI: 10.1007/s10120-019-00924-0. View

18.

Muskhelishvili L, Latendresse J, Kodell R, Henderson E . Evaluation of cell proliferation in rat tissues with BrdU, PCNA, Ki-67(MIB-5) immunohistochemistry and in situ hybridization for histone mRNA. J Histochem Cytochem. 2003; 51(12):1681-8. DOI: 10.1177/002215540305101212. View

19.

Louis D, Ohgaki H, Wiestler O, Cavenee W, Burger P, Jouvet A . The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114(2):97-109. PMC: 1929165. DOI: 10.1007/s00401-007-0243-4. View

20.

Liu A, Hou C, Chen H, Zong X, Zong P . Genetics and Epigenetics of Glioblastoma: Applications and Overall Incidence of IDH1 Mutation. Front Oncol. 2016; 6:16. PMC: 4731485. DOI: 10.3389/fonc.2016.00016. View