RBM24 Suppresses Cancer Progression by Upregulating MiR-25 to Target MALAT1 in Nasopharyngeal Carcinoma

Overview

Journal Cell Death Dis

Specialties Cell Biology
General Medicine

Date 2016 Sep 2

PMID 27584791

Citations 38

Authors

Wen-Feng Hua

Qian Zhong

Tian-Liang Xia

Qi Chen

Mei-Yin Zhang

Ai-Jun Zhou

Zi-Wei Tu

Chen Qu

Man-Zhi Li

Yun-Fei Xia

Hui-Yun Wang

Dan Xie

Francois-Xavier Claret

Er-Wei Song

Mu-Sheng Zeng

Affiliations

Soon will be listed here.

Abstract

Abnormal interaction between non-coding RNAs has been demonstrated to be a common molecular event in various human cancers, but its significance and underlying mechanisms have not been well documented. RNA-binding proteins (RBPs) are key regulators of RNA transcription and post-transcriptional processing. In this study, we found that RNA-binding protein 24 (RBM24) was frequently downregulated in nasopharyngeal carcinoma (NPC). The restoration of RBM24 expression suppressed NPC cellular proliferation, migration and invasion and impeded metastatic colonization in mouse models. Microarray analyses revealed that miR-25 expression was upregulated by RBM24 expression in NPC cells. Similarly, ectopic miR-25 expression suppressed NPC cellular growth and motility by targeting the pro-oncogenic lncRNA MALAT1, and the knockdown of MALAT1 expression exhibited similar effects as RBM24 restoration in NPC cells. Overall, these findings suggest a novel role of RBM24 as a tumor suppressor. Mechanistically, RBM24 acts at least in part through upregulating the expression of miR-25, which in turn targets MALAT1 for degradation.

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References

Yuan L, Liu Z, Lin Z, Xu L, Zhong Q, Zeng M . Recurrent FGFR3-TACC3 fusion gene in nasopharyngeal carcinoma. Cancer Biol Ther. 2014; 15(12):1613-21. PMC: 4622012. DOI: 10.4161/15384047.2014.961874. View

Liu N, Chen N, Cui R, Li W, Li Y, Wei R . Prognostic value of a microRNA signature in nasopharyngeal carcinoma: a microRNA expression analysis. Lancet Oncol. 2012; 13(6):633-41. DOI: 10.1016/S1470-2045(12)70102-X. View

Poon K, Tan K, Wei Y, Peng Ng C, Colman A, Korzh V . RNA-binding protein RBM24 is required for sarcomere assembly and heart contractility. Cardiovasc Res. 2012; 94(3):418-27. DOI: 10.1093/cvr/cvs095. View

Nie Y, Liu X, Qu S, Song E, Zou H, Gong C . Long non-coding RNA HOTAIR is an independent prognostic marker for nasopharyngeal carcinoma progression and survival. Cancer Sci. 2013; 104(4):458-64. PMC: 7657223. DOI: 10.1111/cas.12092. View

Li B, Zuo Q, Zhao Y, Xiao B, Zhuang Y, Mao X . MicroRNA-25 promotes gastric cancer migration, invasion and proliferation by directly targeting transducer of ERBB2, 1 and correlates with poor survival. Oncogene. 2014; 34(20):2556-65. DOI: 10.1038/onc.2014.214. View

Li J, Liu S, Zhou H, Qu L, Yang J . starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res. 2013; 42(Database issue):D92-7. PMC: 3964941. DOI: 10.1093/nar/gkt1248. View

Wang H, Ach R, Curry B . Direct and sensitive miRNA profiling from low-input total RNA. RNA. 2006; 13(1):151-9. PMC: 1705746. DOI: 10.1261/rna.234507. View

Wang X, Meng X, Li H, Liu W, Shen S, Gao Z . MicroRNA-25 expression level is an independent prognostic factor in epithelial ovarian cancer. Clin Transl Oncol. 2014; 16(11):954-8. DOI: 10.1007/s12094-014-1178-6. View

Schmitt A, Chang H . Gene regulation: Long RNAs wire up cancer growth. Nature. 2013; 500(7464):536-7. PMC: 5332550. DOI: 10.1038/nature12548. View

10.

Xu E, Zhang J, Zhang M, Jiang Y, Cho S, Chen X . RNA-binding protein RBM24 regulates p63 expression via mRNA stability. Mol Cancer Res. 2013; 12(3):359-69. PMC: 3962715. DOI: 10.1158/1541-7786.MCR-13-0526. View

11.

Xie L, Hu Z, Wang X, Li Z . [Expression of long noncoding RNA MALAT1 gene in human nasopharyngeal carcinoma cell lines and its biological significance]. Nan Fang Yi Ke Da Xue Xue Bao. 2013; 33(5):692-7. View

12.

Van Kouwenhove M, Kedde M, Agami R . MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer. 2011; 11(9):644-56. DOI: 10.1038/nrc3107. View

13.

Hong R, Ting L, Ko J, Hsu M, Sheen T, Lou P . Induction chemotherapy with mitomycin, epirubicin, cisplatin, fluorouracil, and leucovorin followed by radiotherapy in the treatment of locoregionally advanced nasopharyngeal carcinoma. J Clin Oncol. 2001; 19(23):4305-13. DOI: 10.1200/JCO.2001.19.23.4305. View

14.

Ciafre S, Galardi S . microRNAs and RNA-binding proteins: a complex network of interactions and reciprocal regulations in cancer. RNA Biol. 2013; 10(6):935-42. PMC: 4111733. DOI: 10.4161/rna.24641. View

15.

Grifone R, Xie X, Bourgeois A, Saquet A, Duprez D, Shi D . The RNA-binding protein Rbm24 is transiently expressed in myoblasts and is required for myogenic differentiation during vertebrate development. Mech Dev. 2014; 134:1-15. DOI: 10.1016/j.mod.2014.08.003. View

16.

Yu L, Lu J, Zhang B, Liu X, Wang L, Li S . miR-26a inhibits invasion and metastasis of nasopharyngeal cancer by targeting EZH2. Oncol Lett. 2013; 5(4):1223-1228. PMC: 3629195. DOI: 10.3892/ol.2013.1173. View

17.

Glisovic T, Bachorik J, Yong J, Dreyfuss G . RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 2008; 582(14):1977-86. PMC: 2858862. DOI: 10.1016/j.febslet.2008.03.004. View

18.

Lu J, He M, Wang L, Chen Y, Liu X, Dong Q . MiR-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of EZH2. Cancer Res. 2011; 71(1):225-33. DOI: 10.1158/0008-5472.CAN-10-1850. View

19.

Yang J, Hung L, Licht T, Kostin S, Looso M, Khrameeva E . RBM24 is a major regulator of muscle-specific alternative splicing. Dev Cell. 2014; 31(1):87-99. DOI: 10.1016/j.devcel.2014.08.025. View

20.

Moore M, Proudfoot N . Pre-mRNA processing reaches back to transcription and ahead to translation. Cell. 2009; 136(4):688-700. DOI: 10.1016/j.cell.2009.02.001. View