Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs

Nature Communications

Volumn 7, Issue , 2016, Pages

  Zheng, Qiupeng ^a,b   Bao, Chunyang ^a   Guo, Weijie ^a,b   Li, Shuyi ^a,b   Chen, Jie ^a   Chen, Bing ^a   Luo, Yanting ^a   Lyu, Dongbin ^a   Li, Yan ^a   Shi, Guohai ^a   Liang, Linhui ^a   Gu, Jianren ^b   He, Xianghuo ^a   Huang, Shenglin ^a  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCHIPK3 RNA; MESSENGER RNA; MESSENGER RNA PRECURSOR; MICRORNA; MICRORNA 124; MICRORNA 152; MICRORNA 193A; MICRORNA 29A; MICRORNA 29B; MICRORNA 338; MICRORNA 379; MICRORNA 584; MICRORNA 654; RIBOSOME RNA; UNCLASSIFIED DRUG; HIPK3 PROTEIN, HUMAN; LUCIFERASE; MIRN124 MICRORNA, HUMAN; PROTEIN SERINE THREONINE KINASE; RNA; RNA, CIRCULAR; SIGNAL PEPTIDE; SMALL INTERFERING RNA;

CANCER; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; EUKARYOTE; GENE EXPRESSION; GROWTH RATE; GROWTH REGULATOR; PROTEIN; RNA;

ARTICLE; BINDING SITE; CANCER TISSUE; CELL PROLIFERATION; CONTROLLED STUDY; CRISPR CAS SYSTEM; DOWN REGULATION; EXON; FEMALE; GENE EXPRESSION PROFILING; GENE SILENCING; HIPK3 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUCIFERASE ASSAY; NUCLEOTIDE SEQUENCE; REGULATORY MECHANISM; RNA SEQUENCE; TUMOR GENE; UPREGULATION; ANTAGONISTS AND INHIBITORS; ANTIBODY SPECIFICITY; CELL CYCLE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HCT 116 CELL LINE; HELA CELL LINE; LIVER CELL; METABOLISM; MOLECULAR GENETICS; REPORTER GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

EUKARYOTA;

BASE SEQUENCE; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENES, REPORTER; HCT116 CELLS; HELA CELLS; HEPATOCYTES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUCIFERASES; MICRORNAS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PROTEIN-SERINE-THREONINE KINASES; RNA; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION;

EID: 84964355812     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11215     Document Type: Article

References (41)

1. Jeck, W. R. & Sharpless, N. E. Detecting and characterizing circular RNAs. Nat. Biotechnol. 32, 453-461 (2014).
2. Lasda, E. & Parker, R. Circular RNAs: diversity of form and function. RNA 20, 1829-1842 (2014).
3. Nigro, J. M. et al. Scrambled exons. Cell 64, 607-613 (1991).
4. Cocquerelle, C., Mascrez, B., Hetuin, D. & Bailleul, B. Mis-splicing yields circular RNA molecules. FASEB J. 7, 155-160 (1993).
5. Zaphiropoulos, P. G. Circular RNAs from transcripts of the rat cytochrome P450 2C24 gene: correlation with exon skipping. Proc. Natl Acad. Sci. USA 93, 6536-6541 (1996).
6. Salzman, J., Gawad, C., Wang, P. L., Lacayo, N. & Brown, P. O. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE 7, e30733 (2012).
7. Jeck, W. R. et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19, 141-157 (2013).
8. Memczak, S. et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333-338 (2013).
9. Glazar, P., Papavasileiou, P. & Rajewsky, N. circBase: a database for circular RNAs. RNA 20, 1666-1670 (2014).
10. Rybak-Wolf, A. et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol. Cell 58, 870-885 (2015).
11. Guo, J. U., Agarwal, V., Guo, H. & Bartel, D. P. Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 15, 409 (2014).
12. Salzman, J., Chen, R. E., Olsen, M. N., Wang, P. L. & Brown, P. O. Cell-type specific features of circular RNA expression. PLoS Genet. 9, e1003777 (2013).
13. You, X. et al. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat. Neurosci. 18, 603-610 (2015).
14. Li, Y. et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 25, 981-984 (2015).
15. Starke, S. et al. Exon circularization requires canonical splice signals. Cell Rep. 10, 103-111 (2015).
16. Zhang, X. O. et al. Complementary sequence-mediated exon circularization. Cell 159, 134-147 (2014).
17. Liang, D. & Wilusz, J. E. Short intronic repeat sequences facilitate circular RNA production. Genes Dev. 28, 2233-2247 (2014).
18. Ashwal-Fluss, R. et al. circRNA biogenesis competes with pre-mRNA splicing. Mol. Cell 56, 55-66 (2014).
19. Ivanov, A. et al. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 10, 170-177 (2015).
20. Conn, S. J. et al. The RNA binding protein quaking regulates formation of circRNAs. Cell 160, 1125-1134 (2015).
21. Chen, L. L. & Yang, L. Regulation of circRNA biogenesis. RNA Biol. 12, 381-388 (2015).
22. Hansen, T. B. et al. Natural RNA circles function as efficient microRNA sponges. Nature 495, 384-388 (2013).
23. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
24. Pruitt, K. D., Tatusova, T., Brown, G. R. & Maglott, D. R. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res. 40, D130-D135 (2012).
25. Blin, K. et al. DoRiNA 2.0-upgrading the doRiNA database of RNA interactions in post-transcriptional regulation. Nucleic Acids Res. 43, D160-D167 (2015).
26. Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (2005).
27. Krek, A. et al. Combinatorial microRNA target predictions. Nat. Genet. 37, 495-500 (2005).
28. Hatziapostolou, M. et al. An HNF4alpha-miRNA inflammatory feedback circuit regulates hepatocellular oncogenesis. Cell 147, 1233-1247 (2011).
29. Furuta, M. et al. miR-124 and miR-203 are epigenetically silenced tumorsuppressive microRNAs in hepatocellular carcinoma. Carcinogenesis 31, 766-776 (2010).
30. Tsuruta, T. et al. miR-152 is a tumor suppressor microRNA that is silenced by DNA hypermethylation in endometrial cancer. Cancer Res. 71, 6450-6462 (2011).
31. Iliopoulos, D., Rotem, A. & Struhl, K. Inhibition of miR-193a expression by Max and RXRalpha activates K-Ras and PLAU to mediate distinct aspects of cellular transformation. Cancer Res. 71, 5144-5153 (2011).
32. Mott, J. L., Kobayashi, S., Bronk, S. F. & Gores, G. J. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26, 6133-6140 (2007).
33. Ueno, K. et al. Tumour suppressor microRNA-584 directly targets oncogene Rock-1 and decreases invasion ability in human clear cell renal cell carcinoma. Br. J. Cancer 104, 308-315 (2011).
34. Ostling, P. et al. Systematic analysis of microRNAs targeting the androgen receptor in prostate cancer cells. Cancer Res. 71, 1956-1967 (2011).
35. Begley, D. A., Berkenpas, M. B., Sampson, K. E. & Abraham, I. Identification and sequence of human PKY, a putative kinase with increased expression in multidrug-resistant cells, with homology to yeast protein kinase Yak1. Gene 200, 35-43 (1997).
36. Curtin, J. F. & Cotter, T. G. JNK regulates HIPK3 expression and promotes resistance to Fas-mediated apoptosis in DU 145 prostate carcinoma cells. J. Biol. Chem. 279, 17090-17100 (2004).
37. Westholm, J. O. et al. Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 9, 1966-1980 (2014).
38. Tay, Y., Rinn, J. & Pandolfi, P. P. The multilayered complexity of ceRNA crosstalk and competition. Nature 505, 344-352 (2014).
39. Hsu, F. et al. The UCSC known genes. Bioinformatics 22, 1036-1046 (2006).
40. Zheng, Q. et al. Precise gene deletion and replacement using the CRISPR/Cas9 system in human cells. BioTechniques 57, 115-124 (2014).
41. Lal, A. et al. Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet. 7, e1002363 (2011).