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Complementary Sequence-Mediated Exon Circularization
Open accessAbstract
Exon circularization has been identified from many loci in mammals, but the detailed mechanism of its biogenesis has remained elusive. By using genome-wide approaches and circular RNA recapitulation, we demonstrate that exon circularization is dependent on flanking intronic complementary sequences. Such sequences and their distribution exhibit rapid evolutionary changes, showing that exon circularization is evolutionarily dynamic. Strikingly, exon circularization efficiency can be regulated by competition between RNA pairing across flanking introns or within individual introns. Importantly, alternative formation of inverted repeated Alu pairs and the competition between them can lead to alternative circularization, resulting in multiple circular RNA transcripts produced from a single gene. Collectively, exon circularization mediated by complementary sequences in human introns and the potential to generate alternative circularization products extend the complexity of mammalian posttranscriptional regulation.
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“CircRNA is a highly stable single-stranded RNA with a covalently closed loop structure (Fig. 3), including a large category of non-coding RNAs generated by backsplicing in eukaryotic cells.218–220”
From Advances in COVID-19 mRNA vaccine development (2022) · cites this paper as [218]
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“Circular RNAs (circRNAs) are a class of RNA molecules that are formed by head-to-tail splicing (also known as backsplicing), in which a downstream 50 splice site (SS) is covalently connected to an upstream 30 SS of an RNA molecule (Ashwal-Fluss et al., 2014; Hansen et al., 2013; Ivanov et al., 2015; Memczak et al., 20…”
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BackgroundNon-coding RNAs in Nervous System Development and Disease
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“This mechanism can be mediated by base pairing between inverted repeat elements namely Alu elements [7], or by dimerization of RNA-binding proteins like HQK encoded by QKI [8] or FUS [9] that binds to specific motifs in the flanking introns.”
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“…al. compared the output results of five different algorithms: circRNA_finder (Westholm et al. 2014), find_circ (Memczak et al. 2013), CircExplorer (Zhang et al. 2014), CIRI (Gao et al. 2018; Zhang et al. 2018), and MapSplice (Wang et al. 2010) and used the RNase R to assess the level of false…”
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“The inserted fragment was driven by an EF1α or a CAG promoter, followed by circularizable exons of the human circPOLR2A (9,10) containing the intramolecular dsRNA duplexes 51,52 with flanking intronic complementary sequences (hereafter C_OE mice, Extended Data Fig.”
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“Notable circRNA identification tools are find_circ [71], MapSplice2 [72], Segemehl [73], circExplorer [74], circRNA_finder [75], CIRI [76], ACFS [69], KNIFE [77], NCLscan [78], DCC [79] and UROBORUS [80].”
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“Importantly, in addition to RNA base-pairing formed across flanking introns, RNA base-pairing can also form within an individual intron in linear RNA production (Hossain et al., 2011; Zhang et al., 2014).”
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“com/arraystar-human-circular-rna-mic roarray) and was used in milestone studies in the field.(3,13,14,36,48,49) A number of recent investigations take advantage Arraystar's microarrays and report strong detection and validation efficiency.”
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circGNB1 Facilitates Triple-Negative Breast Cancer Progression by Regulating miR-141-5p-IGF1R Axis
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“It is well known that reverse complementary sequences, especially Alu elements in circRNA-flanking introns, contribute greatly to circRNA formation (11,17).”
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“circRNAs regulate IDD by acting as post-transcriptional regulators, and they can interact with miRNAs as miRNA sponges and ceRNAs in the NPC cytoplasm.(24,25) Our previous research results show that circRNAs are abundant in IDD NPCs and play important roles in regulating IDD.”
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“Intronic Alu elements or proteinmediated long-range looping dynamically modulates the ratio of canonical to back splicing, resulting in the generation of large amounts of circular RNAs (Figure 7D) (Conn et al., 2015; Ivanov et al., 2015; Liang and Wilusz, 2014; Zhang et al., 2014).”
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“Alu elements are suggested as important regulators of circRNA biogenesis, but other inversed repetitive sequences are also adequate to drive RNA circularization [10,14,49].”
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“The pairs in the identical intron sequence facilitate the expulsion and canonical splicing [47].”
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Self-citationSplicing noncoding RNAs from the inside out
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FUCHS—towards full circular RNA characterization using RNAseq
Metge, F., Czaja-Hasse, L. F., Reinhardt, R., & Dieterich, C. (2017) · PeerJ · doi:10.7717/peerj.2934 · Cited by 63
Quantifying circular RNA expression from RNA-seq data using model-based framework
Li, M., Xie, X., Zhou, J., Sheng, M., Yin, X., Ko, E.-A., Zhou, T., & Gu, W. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx129 · Cited by 64
The potential roles of circRNAs in osteoarthritis: a coming journey to find a treasure
Li, H., Zhong, L., Xu, X., Lin, N., & Lu, H.-D. (2018) · Bioscience Reports · doi:10.1042/bsr20180542 · Cited by 66
Computational approaches for circular RNA analysis
Jakobi, T., & Dieterich, C. (2019) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1528 · Cited by 64
Epigenetic Regulation of Alternative Splicing: How LncRNAs Tailor the Message
Pisignano, G., & Ladomery, M. (2021) · Non-Coding RNA · doi:10.3390/ncrna7010021 · Cited by 65
“Since most circRNAs are derived from the middle exons of protein-coding genes [42], their biogenesis can itself affect splicing of their precursor transcripts and lead to altered gene expression outcomes [43].”
BackgroundCircRNA: a rising star in plant biology
Zhang, P., & Dai, M. (2022) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2022.05.004 · Cited by 63
Ming-shan, L., Liu, Y., Zhang, X., Liu, J., & Wang, P. (2018) · Gene · doi:10.1016/j.gene.2018.07.041 · Cited by 63
Self-citationNoncoding RNAs in Cardiac Hypertrophy
Li, Y., Liang, Y., Zhu, Y., Zhang, Y., & Bei, Y. (2018) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-018-9797-x · Cited by 63
Self-citationLin, Y., Yu, Y.-S., Lin, H.-H., & Hsiao, K. (2020) · Cancers · doi:10.3390/cancers12030697 · Cited by 62
Circular RNA: a new star in neurological diseases
Li, T., Jia, Y., Wang, Q., Shao, X.-Q., & Lv, R. (2016) · International Journal of Neuroscience · doi:10.1080/00207454.2016.1236382 · Cited by 63
“that gives rise to a circRNA could encode a single isoform or many [5,15].”
BackgroundCircular RNA profile indicates circular RNA VRK1 is negatively related with breast cancer stem cells
Yan, N., Xu, H., Zhang, J., Xu, L., Zhang, Y., Zhang, L., Xu, Y., & Zhang, F. (2017) · Oncotarget · doi:10.18632/oncotarget.21183 · Cited by 61
“Recently, with the development of bioinformatic approaches and sequencing technology, the abundance of circRNAs were found widespread in organisms [17, 31, 36, 37].”
MethodSelf-citationThe nuclear export of circular RNAs is primarily defined by their length
Li, Z., Kearse, M. G., & Huang, C. (2018) · RNA Biology · doi:10.1080/15476286.2018.1557498 · Cited by 63
Wang, Y., Gao, Y., Zhang, H., Wang, H., Liu, X., Xu, X., Zhang, Z., Kohnen, M. V., Hu, K., Wang, H., et al. (2019) · Plant and Cell Physiology · doi:10.1093/pcp/pcz043 · Cited by 61
“identify circular RNAs by the circularizing junction alignment (Zhang et al. 2014).”
BackgroundSelf-citationCircRNAs: A new perspective of biomarkers in the nervous system
Ma, Y., Liu, Y., & Jiang, Z. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110251 · Cited by 61
Circular RNA: New Regulatory Molecules
Belousova, E. A., Филипенко, М. Л., & Кушлинский, Н. Е. (2018) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-018-4084-z · Cited by 61
Yao, R., Zou, H., & Liao, W. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00332 · Cited by 61
“Intron pairing-driven circularization is accomplished by the direct base-pairing of the introns flanking complementary sequences or inverted repeats (38, 49).”
BackgroundYu, C., Cheng, Z., Cui, S., Mao, X., Li, B., Fu, Y., Wang, H., Jin, H., Ye, Q., Zhao, X., et al. (2020) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-020-01555-5 · Cited by 62
“To construct circFOXM1 ectopic overexpression plasmid, the sequences of exon 4 and exon 5 in FOXM1(amplified from cDNAs of H1299 cells) were cloned into pZW-circRNA vector (a gift from Ling-Ling Chen Lab) [17].”
MethodSelf-citationWang, Y., Wang, H., Xi, F., Wang, H., Han, X., Wei, W., Zhang, H., Zhang, Q., Zheng, Y., Zhu, Q., et al. (2020) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13002 · Cited by 62
Self-citationThe Role of Circular RNAs in Therapy Resistance of Patients With Solid Tumors
Papatsirou, M., Artemaki, P. I., Scorilas, A., & Kontos, C. K. (2020) · Personalized Medicine · doi:10.2217/pme-2020-0103 · Cited by 62
Qin, S., Mao, Y., Xue, C., Xiao, J., Qin, Y., & Zhao, L. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.62767 · Cited by 61
Sensitive, reliable and robust circRNA detection from RNA-seq with CirComPara2
Gaffo, E., Buratin, A., Molin, A. D., & Bortoluzzi, S. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab418 · Cited by 62
“As expected, the CIRCexplorer2 pipelines showed a dramatic reduction (up to −0.14) of the recall and F1-scores (Supplementary Figure S2).”
InfluentialCircular RNAs: New layer of complexity evading breast cancer heterogeneity
Dawoud, A., Zakaria, Z. I., Rashwan, H. H., Braoudaki, M., & Youness, R. A. (2022) · Non-coding RNA Research · doi:10.1016/j.ncrna.2022.09.011 · Cited by 61
“However, single-exon circRNA showed longer length than average exon length [33].”
BackgroundCircular RNAs: Emerging roles and new insights in human cancers
He, Z., & Zhu, Q. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115217 · Cited by 61
Characterization of Circular RNAs
Zhang, Y., Yang, L. C., & Chen, L. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-3378-5_17 · Cited by 61
Self-citationHidden Peptides Encoded by Putative Noncoding RNAs
Matsumoto, A., & Nakayama, K. I. (2018) · Cell Structure and Function · doi:10.1247/csf.18005 · Cited by 61
“This reaction is promoted by the presence of sequences of reverse comple‐ mentarity—such as human Alu repeats—in introns (Zhang et al., 2014).”
BackgroundWang, X., Wang, B., Zou, M., Li, J., Lü, G., Zhang, Q., Liu, F., & Lu, C. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.08.033 · Cited by 61
Processing and roles of snoRNA-ended long noncoding RNAs
Xing, Y., & Chen, L. (2018) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2018.1508411 · Cited by 60
“Intriguingly, it was suggested that sno-lncRNAs could be further processed to produce individual snoRNAs (Yin et al. 2012; Zhang et al. 2014b; Xing et al. 2017), but how they are processed is unclear.”
BackgroundInfluentialSelf-citationEmerging important roles of circRNAs in human cancer and other diseases
Huang, Y., Zhang, C., Xiong, J., & Ren, H. (2020) · Genes & Diseases · doi:10.1016/j.gendis.2020.07.012 · Cited by 62
Metadata
- Authors
- Zhang, X.-O., Wang, H.-B., Zhang, Y., Lu, X., Chen, L.-L., & Yang, L.
- Affiliations
- Chinese Academy of Sciences (CN)
- Second Military Medical University (CN)
- Corresponding author
- Chen, Ling-Ling
- Yang, Li
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-09
- Volume
- 159
- Issue
- 1
- Pages
- 134-147
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W1981726010
- Cited by
- 1,999
- References
- 35
- Citations by year
- 2026: 70 · 2025: 117 · 2024: 200 · 2023: 183 · 2022: 254 · 2021: 280 · 2020: 245 · 2019: 212 · 2018: 176 · 2017: 121 · 2016: 74 · 2015: 54 · 2014: 9
- FWCI
- 35.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (31271376, 2014CB964800, 31322018)
- Max-Planck-Gesellschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Circular RNAs in diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Keywords
- circular RNA, Alu elements, inverted repeats, post-transcriptional regulation, intron evolution, mammalian gene expression
- MeSH terms
- Animals, Base Sequence, Exons, Humans, Introns, Mammals, Molecular Sequence Data, Nucleic Acid Conformation, Genome, Human, Sequence Alignment, Alternative Splicing, Evolution, Molecular, Alu Elements, Embryonic Stem Cells
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