Circular RNA circCTNNA1 promotes colorectal cancer progression by sponging miR-149-5p and regulating FOXM1 expression.
Aged
Animals
Base Sequence
Carcinogenesis
/ genetics
Cell Cycle Checkpoints
/ genetics
Cell Line, Tumor
Cell Movement
/ genetics
Cell Proliferation
/ genetics
Colorectal Neoplasms
/ genetics
DNA, Neoplasm
/ biosynthesis
Disease Progression
Female
Forkhead Box Protein M1
/ genetics
Gene Expression Profiling
Gene Expression Regulation, Neoplastic
Gene Knockdown Techniques
Humans
Male
Mice, Inbred BALB C
Mice, Nude
MicroRNAs
/ genetics
Middle Aged
Neoplasm Invasiveness
RNA, Circular
/ genetics
RNA, Messenger
/ genetics
Survival Analysis
Up-Regulation
/ genetics
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
22 07 2020
22 07 2020
Historique:
received:
29
01
2020
accepted:
21
05
2020
revised:
19
05
2020
entrez:
24
7
2020
pubmed:
24
7
2020
medline:
25
3
2021
Statut:
epublish
Résumé
Circular RNAs (circRNAs) are an emerging class of non-coding RNAs, identified to participate in multiple malignancies. Nevertheless, the clinical significance, biological function, and regulatory mechanisms of circRNAs in colon cancer (CC) remain largely unclear. In this study, the circRNA expression profile in CC and matched normal tissues was analyzed using circRNA microarrays. A novel circRNA, circCTNNA1, was significantly upregulated in CC, and its level was associated with advanced tumor-node-metastasis stage and poor prognosis of patients with CC. Functional experiments, including Cell Counting Kit-8, colony formation, 5-ethynyl-2'-deoxyuridine, transwell, wound healing, flow cytometric analysis, and in vivo tumorigenesis assay were then performed to investigate the oncogenic role of circCTNNA1. The results revealed that circCTNNA1 promoted CC cell proliferation, migration, and invasion in vitro and in vivo. Mechanistically, RNA pull-down, RNA immunoprecipitation, dual-luciferase reporter assays, and fluorescent in situ hybridization were performed to unveil that circCTNNA1 can serve as a competing endogenous RNA of miR-149-5p to counteract the suppressive effect of miR-149-5p on downstream target Forkhead Box M1 (FOXM1). In summary, our study demonstrated that circCTNNA1 facilitated CC proliferation and invasion via the circCTNNA1/miR-149-5p/FOXM1 axis, and it might function as a novel diagnostic or therapeutic target for patients with CC.
Identifiants
pubmed: 32699205
doi: 10.1038/s41419-020-02757-7
pii: 10.1038/s41419-020-02757-7
pmc: PMC7376054
doi:
Substances chimiques
DNA, Neoplasm
0
FOXM1 protein, human
0
Forkhead Box Protein M1
0
MIRN149 microRNA, human
0
MicroRNAs
0
RNA, Circular
0
RNA, Messenger
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
557Références
Bray, F. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: Cancer J. Clin.68, 394–424 (2018).
Smith, F. M., Cresswell, K., Myint, A. S. & Renehan, A. G. Is “watch-and-wait” after chemoradiotherapy safe in patients with rectal cancer? BMJ363, k4472 (2018).
doi: 10.1136/bmj.k4472
Keum, N. & Giovannucci, E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat. Rev. Gastro. Hepat.16, 713–732 (2019).
Kristensen, L. S. et al. The biogenesis, biology and characterization of circular RNAs. Nat Rev. Genet.20, 675–691 (2019).
Zhang, X. et al. Circular RNA circNRIP1 acts as a microRNA-149-5p sponge to promote gastric cancer progression via the AKT1/mTOR pathway. Mol. Cancer18, 20 (2019).
doi: 10.1186/s12943-018-0935-5
Patop, I. L., Wüst, S. & Kadener, S. Past, present, and future of circRNAs. EMBO J.38, e100836 (2019).
doi: 10.15252/embj.2018100836
Shang, Q., Yang, Z., Jia, R. & Ge, S. The novel roles of circRNAs in human cancer. Mol. Cancer18, 6 (2019).
doi: 10.1186/s12943-018-0934-6
Liu, H. et al. Circular RNA YAP1 inhibits the proliferation and invasion of gastric cancer cells by regulating the miR-367-5p/p27 axis. Mol. Cancer17, 151 (2018).
doi: 10.1186/s12943-018-0902-1
Rong, D. et al. CircPSMC3 suppresses the proliferation and metastasis of gastric cancer by acting as a competitive endogenous RNA through sponging miR-296-5p. Mol. Cancer18, 25 (2019).
doi: 10.1186/s12943-019-0958-6
Wang, R. et al. EIF4A3-induced circular RNA MMP9 (circMMP9) acts as a sponge of miR-124 and promotes glioblastoma multiforme cell tumorigenesis. Mol. Cancer17, 166 (2018).
doi: 10.1186/s12943-018-0911-0
Han, D. et al. Circular RNA circMTO1 acts as the sponge of microRNA-9 to suppress hepatocellular carcinoma progression. Hepatology66, 1151–1164 (2017).
doi: 10.1002/hep.29270
Jin, M., Shi, C., Yang, C., Liu, J. & Huang, G. Upregulated circRNA ARHGAP10 Predicts an Unfavorable Prognosis in NSCLC through Regulation of the miR-150-5p/GLUT-1 Axis. Molecular therapy. Nucleic Acid.18, 219–231 (2019).
Ye, F. et al. circFBXW7 Inhibits Malignant Progression by Sponging miR-197-3p and Encoding a 185-aa Protein in Triple-Negative Breast Cancer. Molecular therapy. Nucleic Acid.18, 88–98 (2019).
Shan, C. et al. Biogenesis, functions and clinical significance of circRNAs in gastric cancer. Mol. Cancer18, 136 (2019).
doi: 10.1186/s12943-019-1069-0
Hsiao, K. Y. et al. Noncoding effects of circular RNA CCDC66 promote colon cancer growth and metastasis. Cancer Res.77, 2339–2350 (2017).
doi: 10.1158/0008-5472.CAN-16-1883
Zheng, X. et al. A novel protein encoded by a circular RNA circPPP1R12A promotes tumor pathogenesis and metastasis of colon cancer via Hippo-YAP signaling. Mol. Cancer18, 47 (2019).
doi: 10.1186/s12943-019-1010-6
Ju, H. Q. et al. A circRNA signature predicts postoperative recurrence in stage II/III colon cancer. EMBO Mol. Med.11, e10168 (2019).
doi: 10.15252/emmm.201810168
Benusiglio, P. R. et al. Clinical implications of CTNNA1 germline mutations in asymptomatic carriers. Gastric Cancer.22, 899–903 (2019).
doi: 10.1007/s10120-018-00907-7
Majewski, I. J. et al. An α-E-catenin (CTNNA1) mutation in hereditary diffuse gastric cancer. The. J. Pathol.229, 621–629 (2013).
doi: 10.1002/path.4152
Salmena, L., Poliseno, L., Tay, Y., Kats, L. & Pandolfi, P. P. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell146, 353–358 (2011).
doi: 10.1016/j.cell.2011.07.014
Liu, L. et al. mA mRNA methylation regulates CTNNB1 to promote the proliferation of hepatoblastoma. Mol. Cancer18, 188 (2019).
doi: 10.1186/s12943-019-1119-7
Wang, Y. G. et al. hsa_circ_0091570 acts as a ceRNA to suppress hepatocellular cancer progression by sponging hsa-miR-1307. Cancer Lett.460, 128–138 (2019).
doi: 10.1016/j.canlet.2019.06.007
Liu, J. et al. Circ-SERPINE2 promotes the development of gastric carcinoma by sponging miR-375 and modulating YWHAZ. Cell Prolif.52, e12648 (2019).
pubmed: 31199037
pmcid: 6668981
Laissue, P. The forkhead-box family of transcription factors: key molecular players in colorectal cancer pathogenesis. Mol. Cancer18, 5 (2019).
doi: 10.1186/s12943-019-0938-x
Macedo, J. C. et al. FoxM1 repression during human aging leads to mitotic decline and aneuploidy-driven full senescence. Nat. Commun.9, 2834 (2018).
doi: 10.1038/s41467-018-05258-6
Zhang, Y. et al. Pan-cancer analysis of clinical relevance of alternative splicing events in 31 human cancers. Oncogene38, 6678–6695 (2019).
doi: 10.1038/s41388-019-0910-7
Cheng, Z. et al. circTP63 functions as a ceRNA to promote lung squamous cell carcinoma progression by upregulating FOXM1. Nat. Commun.10, 3200 (2019).
doi: 10.1038/s41467-019-11162-4
Li, D. et al. circANKS1B regulates FOXM1 expression and promotes cell migration and invasion by functioning as a sponge of the miR-149 in colorectal cancer. OncoTargets Ther.12, 4065–4073 (2019).
doi: 10.2147/OTT.S201310
Luo, X. et al. Long non-coding RNA CCAL/miR-149/FOXM1 axis promotes metastasis in gastric cancer. Cell Death Dis.9, 993 (2018).
doi: 10.1038/s41419-018-0969-z
Yu, G., Wang, L. G., Han, Y. & He, Q. Y. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics: J. Integr. Biol.16, 284–287 (2012).
doi: 10.1089/omi.2011.0118