Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2

Nucleic Acids Research

Volumn 44, Issue 6, 2016, Pages 2846-2858

  Du, William W ^a,b   Yang, Weining ^a   Liu, Elizabeth ^a,b   Yang, Zhenguo ^a,b   Dhaliwal, Preet ^a,b   Yang, Burton B ^a,b  

^a Canada   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULAR RNA; CYCLIN A; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN E; MESSENGER RNA; RNA; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; CDK2 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, HUMAN; PROTEIN BINDING; UNTRANSLATED RNA;

ANIMAL CELL; ARTICLE; CANCER CELL LINE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; ECTOPIC EXPRESSION; FOXO3 GENE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC ASSOCIATION; INTRON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ANIMAL; ANTIBODY SPECIFICITY; BINDING SITE; CELL CYCLE; CELL LINE; CELL NUCLEUS; CHEMISTRY; CONFORMATION; CYTOLOGY; CYTOPLASM; FIBROBLAST; GENETICS; HUMAN; METABOLISM; NIH 3T3 CELL LINE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; BINDING SITES; CELL CYCLE; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; CYCLIN A; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYTOPLASM; FIBROBLASTS; FORKHEAD BOX PROTEIN O3; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; MICE; NIH 3T3 CELLS; NUCLEIC ACID CONFORMATION; ORGAN SPECIFICITY; PROTEIN BINDING; RNA, UNTRANSLATED; SIGNAL TRANSDUCTION;

EID: 84961687529     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw027     Document Type: Article

References (34)

1. Jeck, W.R. and Sharpless, N.E. (2014) Detecting and characterizing circular RNAs. Nat. Biotechnol., 32, 453-461.
2. AbouHaidar, M.G., Venkataraman, S., Golshani, A., Liu, B. and Ahmad, T. (2014) Novel coding, translation, and gene expression of a replicating covalently closed circular RNA of 220 nt. Proc. Natl. Acad. Sci. U.S.A., 111, 14542-14547.
3. Haimovich, G., Medina, D.A., Causse, S.Z., Garber, M., Millan-Zambrano, G., Barkai, O., Chavez, S., Perez-Ortin, J.E., Darzacq, X. and Choder, M. (2013) Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell, 153, 1000-1011.
4. Wilusz, J.E. and Sharp, P.A. (2013) Molecular biology. A circuitous route to noncoding RNA. Science, 340, 440-441.
5. Ivanov, A., Memczak, S., Wyler, E., Torti, F., Porath, H.T., Orejuela, M.R., Piechotta, M., Levanon, E.Y., Landthaler, M., Dieterich, C. et al. (2015) Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep., 10, 170-177.
6. Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S.D., Gregersen, L.H., Munschauer, M. et al. (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 495, 333-338.
7. Hansen, T.B., Jensen, T.I., Clausen, B.H., Bramsen, J.B., Finsen, B., Damgaard, C.K. and Kjems, J. (2013) Natural RNA circles function as efficient microRNA sponges. Nature, 495, 384-388.
8. Capel, B., Swain, A., Nicolis, S., Hacker, A., Walter, M., Koopman, P., Goodfellow, P. and Lovell-Badge, R. (1993) Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell, 73, 1019-1030.
9. Li, F., Zhang, L., Li, W., Deng, J., Zheng, J., An, M., Lu, J. and Zhou, Y. (2015) Circular RNA ITCH has inhibitory effect on ESCC by suppressing the Wnt/beta-catenin pathway. Oncotarget, 6, 6001-6013.
10. Anderson, M.J., Viars, C.S., Czekay, S., Cavenee, W.K. and Arden, K.C. (1998) Cloning and characterization of three human forkhead genes that comprise an FKHR-like gene subfamily. Genomics, 47, 187-199.
11. Myatt, S.S. and Lam, E.W. (2007) The emerging roles of forkhead box (Fox) proteins in cancer. Nat. Rev. Cancer, 7, 847-859.
12. Cho, E.C., Kuo, M.L., Liu, X., Yang, L., Hsieh, Y.C., Wang, J., Cheng, Y. and Yen, Y. (2014) Tumor suppressor FOXO3 regulates ribonucleotide reductase subunit RRM2B and impacts on survival of cancer patients. Oncotarget, 5, 4834-4844.
13. Du, W.W., Yang, W., Fang, L., Xuan, J., Li, H., Khorshidi, A., Gupta, S., Li, X. and Yang, B.B. (2014) miR-17 extends mouse lifespan by inhibiting senescence signaling mediated by MKP7. Cell Death Dis., 5, e1355.
14. Hinds, P.W., Mittnacht, S., Dulic, V., Arnold, A., Reed, S.I. and Weinberg, R.A. (1992) Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell, 70, 993-1006.
15. Levkau, B., Koyama, H., Raines, E.W., Clurman, B.E., Herren, B., Orth, K., Roberts, J.M. and Ross, R. (1998) Cleavage of p21Cip1/Waf1 and p27Kip1 mediates apoptosis in endothelial cells through activation of Cdk2: role of a caspase cascade. Mol. Cell, 1, 553-563.
16. Harper, J.W., Adami, G.R., Wei, N., Keyomarsi, K. and Elledge, S.J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75, 805-816.
17. Gartel, A.L. and Radhakrishnan, S.K. (2005) Lost in transcription: p21 repression, mechanisms, and consequences. Cancer Res., 65, 3980-3985.
18. Jeyapalan, Z., Deng, Z., Shatseva, T., Fang, L., He, C. and Yang, B.B. (2011) Expression of CD44 3′-untranslated region regulates endogenous microRNA functions in tumorigenesis and angiogenesis. Nucleic Acids Res., 39, 3026-3041.
19. Wu, Y., Zhang, Y., Cao, L., Chen, L., Lee, V., Zheng, P.S., Kiani, C., Adams, M.E., Ang, L.C., Paiwand, F. et al. (2001) Identification of the motif in versican G3 domain that plays a dominant-negative effect on astrocytoma cell proliferation through inhibiting versican secretion and binding. J. Biol. Chem., 276, 14178-14186.
20. He, J., Wu, J., Xu, N., Xie, W., Li, M., Li, J., Jiang, Y., Yang, B.B. and Zhang, Y. (2013) MiR-210 disturbs mitotic progression through regulating a group of mitosis-related genes. Nucleic Acids Res., 41, 498-508.
21. Yang, B.L., Cao, L., Kiani, C., Lee, V., Zhang, Y., Adams, M.E. and Yang, B.B. (2000) Tandem repeats are involved in G1 domain inhibition of versican expression and secretion and the G3 domain enhances glycosaminoglycan modification and product secretion via the complement-binding protein-like motif. J. Biol. Chem., 275, 21255-21261.
22. Cao, L., Yao, Y., Lee, V., Kiani, C., Spaner, D., Lin, Z., Zhang, Y., Adams, M.E. and Yang, B.B. (2000) Epidermal growth factor induces cell cycle arrest and apoptosis of squamous carcinoma cells through reduction of cell adhesion. J. Cell Biochem., 77, 569-583.
23. Shan, S.W., Fang, L., Shatseva, T., Rutnam, Z.J., Yang, X., Du, W., Lu, W.Y., Xuan, J.W., Deng, Z. and Yang, B.B. (2013) Mature miR-17-5p and passenger miR-17-3p induce hepatocellular carcinoma by targeting PTEN, GalNT7 and vimentin in different signal pathways. J. Cell Sci., 126, 1517-1530.
24. Lopez de Silanes, I., Stagno d'Alcontres, M. and Blasco, M.A. (2010) TERRA transcripts are bound by a complex array of RNA-binding proteins. Nat. Commun., 1, 33-34.
25. Wang, P., Xue, Y., Han, Y., Lin, L., Wu, C., Xu, S., Jiang, Z., Xu, J., Liu, Q. and Cao, X. (2014) The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science, 344, 310-313.
26. Yang, W., Du, W.W., Li, X., Yee, A.J. and Yang, B.B. (2015) Foxo3 activity promoted by non-coding effects of circular RNA and Foxo3 pseudogene in the inhibition of tumor growth and angiogenesis. Oncogene, doi:10.1038/onc.2015.460.
27. Salzman, J., Gawad, C., Wang, P.L., Lacayo, N. and Brown, P.O. (2012) Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One, 7, e30733.
28. Wang, P.L., Bao, Y., Yee, M.C., Barrett, S.P., Hogan, G.J., Olsen, M.N., Dinneny, J.R., Brown, P.O. and Salzman, J. (2014) Circular RNA is expressed across the eukaryotic tree of life. PLoS One, 9, e90859.
29. Merrick, K.A., Larochelle, S., Zhang, C., Allen, J.J., Shokat, K.M. and Fisher, R.P. (2008) Distinct activation pathways confer cyclin-binding specificity on Cdk1 and Cdk2 in human cells. Mol. Cell, 32, 662-672.
30. Rottmann, S., Menkel, A.R., Bouchard, C., Mertsching, J., Loidl, P., Kremmer, E., Eilers, M., Luscher-Firzlaff, J., Lilischkis, R. and Luscher, B. (2005) Mad1 function in cell proliferation and transcriptional repression is antagonized by cyclin E/CDK2. J. Biol. Chem., 280, 15489-15492.
31. Mitra, J., Enders, G.H., Azizkhan-Clifford, J. and Lengel, K.L. (2006) Dual regulation of the anaphase promoting complex in human cells by cyclin A-Cdk2 and cyclin A-Cdk1 complexes. Cell Cycle, 5, 661-666.
32. Coverley, D., Laman, H. and Laskey, R.A. (2002) Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat. Cell Biol., 4, 523-528.
33. Yam, C.H., Fung, T.K. and Poon, R.Y. (2002) Cyclin A in cell cycle control and cancer. Cell Mol. Life Sci., 59, 1317-1326.
34. Li, Z., Huang, C., Bao, C., Chen, L., Lin, M., Wang, X., Zhong, G., Yu, B., Hu, W., Dai, L. et al. (2015) Exon-intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol., 22, 256-264