Long non-coding RNA urothelial carcinoma associated 1 induces cell replication by inhibiting BRG1 in 5637 cells

Wang,Xiujuan; Gong,Yanbing; Jin,Bo; Wu,Chenglin; Yang,Jianming; Wang,Le; Zhang,Zheng; Mao,Zebin

doi:10.3892/or.2014.3309

Long non-coding RNA urothelial carcinoma associated 1 induces cell replication by inhibiting BRG1 in 5637 cells

Authors:
- Xiujuan Wang
- Yanbing Gong
- Bo Jin
- Chenglin Wu
- Jianming Yang
- Le Wang
- Zheng Zhang
- Zebin Mao
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Affiliations: Department of Biochemistry and Molecular Biology, Health Science Center, Peking University, Beijing 100191, P.R. China, Department of Urology, Peking University First Hospital, Institute of Urology, Peking University, National Urological Cancer Center, Beijing 100034, P.R. China
Published online on: July 3, 2014 https://doi.org/10.3892/or.2014.3309
Pages: 1281-1290

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Abstract

Long non-coding RNA urothelial carcinoma associated 1 (UCA1) was first identified in bladder cancer tissues. High expression of UCA1 in bladder cancer has suggested it may serve as a potential diagnostic molecular marker for bladder cancer. Subsequent research in bladder cancer cell lines showed that UCA1 can promote cell proliferation, but the underlying mechanism remains unknown. In the present study, we identified BRG1 as a UCA1 binding partner using an in vitro RNA pull-down assay, and RNA-binding protein immunoprecipitation assay confirmed UCA1-BRG binding in bladder cancer cells in vivo. BRG1 is a chromatin remodeling factor with reported tumor suppressor activities that directly upregulates levels of the p21 cell cycle inhibitor by binding sequences in the p21 promoter. Depletion of UCA1 by RNAi resulted in upregulated p21 levels and inhibition of cell replication, while overexpressed UCA1 reduced p21 protein and promoted cell growth. Notably, UCA1 downregulation of p21 and induction of cell proliferation antagonized the function of BRG1. UCA1 highly expressed tissue samples are often with BRG1 high expression. Furthermore, we found that UCA1 impairs both binding of BRG1 to the p21 promoter and chromatin remodeling activity of BRG1. Collectively, these results demonstrate that UCA1 promotes bladder cancer cell proliferation by inhibiting BRG1.

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1	ENCODE Project Consortium. Birney E, Stamatoyannopoulos JA, et al: Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 447:799–816. 2007.
2	Khachane AN and Harrison PM: Mining mammalian transcript data for functional long non-coding RNAs. PLoS One. 5:e103162010. View Article : Google Scholar : PubMed/NCBI
3	Tsang WP, Wong TW, Cheung AH, Co CN and Kwok TT: Induction of drug resistance and transformation in human cancer cells by the noncoding RNA CUDR. RNA. 13:890–898. 2007. View Article : Google Scholar : PubMed/NCBI
4	Wilusz JE, Sunwoo H and Spector DL: Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 23:1494–1504. 2009. View Article : Google Scholar : PubMed/NCBI
5	Wang KC and Chang HY: Molecular mechanisms of long noncoding RNAs. Mol Cell. 43:904–914. 2011. View Article : Google Scholar
6	Mercer TR, Dinger ME and Mattick JS: Long non-coding RNAs: insights into functions. Nat Rev Genet. 10:155–159. 2009. View Article : Google Scholar : PubMed/NCBI
7	Costa FF: Non-coding RNAs, epigenetics and complexity. Gene. 410:9–17. 2008. View Article : Google Scholar : PubMed/NCBI
8	Faghihi MA and Wahlestedt C: Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol. 10:637–643. 2009. View Article : Google Scholar : PubMed/NCBI
9	Ponting CP, Oliver PL and Reik W: Evolution and functions of long noncoding RNAs. Cell. 136:629–641. 2009. View Article : Google Scholar : PubMed/NCBI
10	Gibb EA, Brown CJ and Lam WL: The functional role of long non-coding RNA in human carcinomas. Mol Cancer. 10:382011. View Article : Google Scholar : PubMed/NCBI
11	Wapinski O and Chang HY: Long noncoding RNAs and human disease. Trends Cell Biol. 21:354–361. 2011. View Article : Google Scholar : PubMed/NCBI
12	Wang XS, Zhang Z, Wang HC, et al: Rapid identification of UCA1 as a very sensitive and specific unique marker for human bladder carcinoma. Clin Cancer Res. 12:4851–4858. 2006. View Article : Google Scholar : PubMed/NCBI
13	Xie XJ, Li X, Wang F and Chen W: Cellular localization and tissue expression pattern of UCA1, a non-coding RNA. Nan Fang Yi Ke Da Xue Xue Bao. 30:57–60. 2010.(In Chinese).
14	Wang F, Li X, Xie X, Zhao L and Chen W: UCA1, a non-protein-coding RNA up-regulated in bladder carcinoma and embryo, influencing cell growth and promoting invasion. FEBS Lett. 582:1919–1927. 2008. View Article : Google Scholar
15	Peifer M and Polakis P: Wnt signaling in oncogenesis and embryogenesis - a look outside the nucleus. Science. 287:1606–1609. 2000. View Article : Google Scholar : PubMed/NCBI
16	Shimada T and Fujii-Kuriyama Y: Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci. 95:1–6. 2004. View Article : Google Scholar : PubMed/NCBI
17	Katayama H, Brinkley WR and Sen S: The Aurora kinases: role in cell transformation and tumorigenesis. Cancer Metastasis Rev. 22:451–464. 2003. View Article : Google Scholar : PubMed/NCBI
18	Wilson BG and Roberts CW: SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer. 11:481–492. 2011. View Article : Google Scholar : PubMed/NCBI
19	Kidder BL, Palmer S and Knott JG: SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells. 27:317–328. 2009. View Article : Google Scholar : PubMed/NCBI
20	Tu Z, Zhuang X, Yao YG and Zhang R: BRG1 is required for formation of senescence-associated heterochromatin foci induced by oncogenic RAS or BRCA1 loss. Mol Cell Biol. 33:1819–1829. 2013. View Article : Google Scholar : PubMed/NCBI
21	Kang H, Cui K and Zhao K: BRG1 controls the activity of the retinoblastoma protein via regulation of p21^{CIP1/WAF1/SDI}. Mol Cell Biol. 24:1188–1199. 2004. View Article : Google Scholar : PubMed/NCBI
22	Xu Y, Zhang J and Chen X: The activity of p53 is differentially regulated by Brm- and Brg1-containing SWI/SNF chromatin remodeling complexes. J Biol Chem. 282:37429–37435. 2007. View Article : Google Scholar : PubMed/NCBI
23	Tsai MC, Manor O, Wan Y, et al: Long noncoding RNA as modular scaffold of histone modification complexes. Science. 329:689–693. 2010. View Article : Google Scholar : PubMed/NCBI
24	Bochar DA, Savard J, Wang W, et al: A family of chromatin remodeling factors related to Williams syndrome transcription factor. Proc Natl Acad Sci USA. 97:1038–1043. 2000. View Article : Google Scholar : PubMed/NCBI
25	Yang C, Li X, Wang Y, Zhao L and Chen W: Long non-coding RNA UCA1 regulated cell cycle distribution via CREB through PI3-K dependent pathway in bladder carcinoma cells. Gene. 496:8–16. 2012. View Article : Google Scholar : PubMed/NCBI
26	Barker N, Hurlstone A, Musisi H, Miles A, Bienz M and Clevers H: The chromatin remodelling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J. 20:4935–4943. 2001.
27	DiRenzo J, Shang YF, Phelan M, et al: BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation. Mol Cell Biol. 20:7541–7549. 2000. View Article : Google Scholar : PubMed/NCBI
28	Alessio N, Squillaro T, Cipollaro M, Bagella L, Giordano A and Galderisi U: The BRG1 ATPase of chromatin remodeling complexes is involved in modulation of mesenchymal stem cell senescence through RB-P53 pathways. Oncogene. 29:5452–5463. 2010. View Article : Google Scholar : PubMed/NCBI
29	Aravinthan A, Mells G, Allison M, et al: Gene polymorphisms of cellular senescence marker p21 and disease progression in non-alcohol-related fatty liver disease. Cell Cycle. 13:1489–1494. 2014. View Article : Google Scholar : PubMed/NCBI
30	Bai J, Chen J, Ma M, et al: Inhibiting enhancer of zeste homolog 2 promotes cellular senescence in gastric cancer cells SGC-7901 by activation of p21 and p16. DNA Cell Biol. 33:337–344. 2014. View Article : Google Scholar : PubMed/NCBI