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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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InfluentialLoss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function
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BackgroundMethodInfluentialNovel Role of FBXW7 Circular RNA in Repressing Glioma Tumorigenesis
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Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans
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Diverse alternative back-splicing and alternative splicing landscape of circular RNAsPreprint
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Circular RNAs: analysis, expression and potential functions
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Structure and Degradation of Circular RNAs Regulate PKR Activation in Innate Immunity
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Self-citationCircular RNA Expression: Its Potential Regulation and Function
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“With regard to intron pairing, alternative formation of inverted repeated Alu elements in flanking introns and competition between RNA pairings across flanking introns or within individual introns can lead to alternative circularization, resulting in the production of multiple circRNAs and linear transcripts from a si…”
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Circular RNA cSMARCA5 inhibits growth and metastasis in hepatocellular carcinoma
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“Latest studies have shown that the biogenesis of circRNAs occurs by backsplicing unlike the canonical linear RNAs splicing [29], and circRNAs are considered as co-transcriptional products.”
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Circular RNAs are miRNA sponges and can be used as a new class of biomarker
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Oncogenic Role of Fusion-circRNAs Derived from Cancer-Associated Chromosomal Translocations
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Detecting circular RNAs: bioinformatic and experimental challenges
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BackgroundMethodInfluentialNoncoding Effects of Circular RNA CCDC66 Promote Colon Cancer Growth and Metastasis
Hsiao, K., Lin, Y., Gupta, S. K., Chang, N., Yen, L., Sun, H. S., & Tsai, S. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-1883 · Cited by 671
The Biogenesis of Nascent Circular RNAs
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“…requires the canonical spliceosomal machinery (Ashwal-Fluss et al., 2014; Starke et al., 2015; Wang and Wang, 2015) and is modulated by both cis- and trans-regulators (Ashwal-Fluss et al., 2014; Zhang et al., 2014; Conn et al., 2015; Ivanov et al., 2015; Kramer et al., 2015; Starke et al., 2015).”
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Circular RNA Vaccines against SARS-CoV-2 and Emerging Variants
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Self-citationCoordinated circRNA Biogenesis and Function with NF90/NF110 in Viral Infection
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“Circularized RNA products were treated with RNase R as described (Zhang et al., 2014), concentrated by ethanol precipitation, resolved on denaturing urea polyacrylamide gel and then visualized by Ethidium bromide staining.”
BackgroundMethodInfluentialSelf-citationIdentifying and Characterizing circRNA-Protein Interaction
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“Examples where an orthologous gene in human and mouse produces circular RNA in only one of the species may yield insights into the mechanism of its production [22].”
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DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome
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Widespread and Functional RNA Circularization in Localized Prostate Cancer
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Self-citationEmerging role of tumor-related functional peptides encoded by lncRNA and circRNA
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FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons
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“These results are in agreement with the notion that the sequences involved in the control of back-splicing are in general in the proximal intron regions 12,21,22 .”
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circRNADb: A comprehensive database for human circular RNAs with protein-coding annotations
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“This is consistent with previous computational analyses (Jeck et al. 2013; Zhang et al. 2014) as well as experiments in humans (Liang and Wilusz 2014) and S. pombe (Barrett et al. 2015) that revealed a positive correlation between exon length and circularization efficiency.”
BackgroundResultInfluentialSpatio-temporal regulation of circular RNA expression during porcine embryonic brain development
Venø, M. T., Hansen, T. B., Venø, S. T., Clausen, B. H., Grebing, M., Finsen, B. R., Holm, I. E., & Kjems, J. (2015) · Genome biology · doi:10.1186/s13059-015-0801-3 · Cited by 475
“One confounding effect is that base pairing ability within introns counteracts the circRNA promoting effects of complementary sequences in introns across exons [17].”
BackgroundSpecific expression and functions of circular RNAs
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“1B, left).(12,13,18,35,39) The potential prevalence”
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BackgroundMethodInfluentialCircular RNA biogenesis can proceed through an exon-containing lariat precursor
Barrett, S. P., Wang, P., & Salzman, J. (2015) · eLife · doi:10.7554/elife.07540 · Cited by 443
“Circular RNA is a pervasive aspect of eukaryotic gene expression, and recent work has begun to shed light on the regulation and biogenesis of these still largely mysterious RNAs (Ashwal-Fluss et al., 2014; Liang and Wilusz, 2014; Zhang et al., 2014b; Conn et al., 2015).”
BackgroundMethodResultInfluentialA 360° view of circular RNAs: From biogenesis to functions
Wilusz, J. E. (2018) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1478 · Cited by 446
The circ RNA –micro RNA code: emerging implications for cancer diagnosis and treatment
Verduci, L., Strano, S., Yarden, Y., & Blandino, G. (2019) · Molecular Oncology · doi:10.1002/1878-0261.12468 · Cited by 442
“Moreover, it has been shown that Alu elements can compete between them generating multiple circRNAs from a single gene locus (Jeck et al., 2013; Salzman et al., 2013; Zhang et al., 2014).”
BackgroundInfluentialSmall and long non-coding RNAs: Past, present, and future
Chen, L., & Kim, V. N. (2024) · Cell · doi:10.1016/j.cell.2024.10.024 · Cited by 461
Self-citationLiang, D., Tatomer, D. C., Luo, Z., Wu, H., Yang, L. C., Chen, L., Cherry, S. R., & Wilusz, J. E. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.10.034 · Cited by 446
“CIRCexplorer (Zhang et al., 2014) was used to identify circular RNAs from the population of unmapped reads.”
BackgroundMethodInfluentialSelf-citationCircular RNAs in cancer: novel insights into origins, properties, functions and implications.
Li, J., Yang, J., Zhou, P., Le, Y., Zhou, C., Wang, S., Xu, D., Lin, H., & Gong, Z. (2015) · Europe PMC (PubMed Central) · Cited by 430
CircRNAs in cancer metabolism: a review
Yu, T., Wang, Y., Fan, Y., Fang, N., Wang, T., Xu, T., & Shu, Y. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0776-8 · Cited by 427
“Irrespective of these defects, circRNAs are qualified for a potential therapy to precisely regulate metabolism due to their extremely high stability, strong evolutionary conservation, and unique temporal and spatial expression [77, 85].”
BackgroundZhou, C., Molinié, B., Daneshvar, K., Pondick, J. V., Wang, J., Wittenberghe, N. V., Xing, Y., Giallourakis, C. C., & Mullen, A. C. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.027 · Cited by 435
“Transposable Elements are Enriched in the Flanking Regions of m6A-circRNAs Reverse complementary sequence in transposable elements (TEs) in the flanking regions of circRNAs promote the formation of circRNAs (Ashwal-Fluss et al., 2014; Chen et al., 2017; Liang and Wilusz, 2014; Zhang et al., 2014).”
BackgroundResultInfluentialRetrotransposons as regulators of gene expression
Elbarbary, R. A., Lucas, B. A., & Maquat, L. E. (2016) · Science · doi:10.1126/science.aac7247 · Cited by 449
The emerging roles and functions of circular RNAs and their generation
Yu, C., & Kuo, H. (2019) · Journal of Biomedical Science · doi:10.1186/s12929-019-0523-z · Cited by 443
“extends this observation, confirming that the pairing between Alu repetitive elements with reverse orientation regulates the expression of linear and circular isoforms [35, 109].”
BackgroundCircular RNA participates in the carcinogenesis and the malignant behavior of cancer
Zhao, Z., & Shen, J. (2015) · RNA Biology · doi:10.1080/15476286.2015.1122162 · Cited by 424
“The exons in pre-mRNAs that possess flanking intronic complementary sequences may present a preference for the 30 end of an upstream exon, which results in the circularization of exons.(15) This unique sequence-dependent feature is essential for the co-transcriptional biogenesis of circRNAs, because the production rat…”
BackgroundThe emerging landscape of circular RNA in life processes
Qu, S., Zhong, Y., Shang, R., Zhang, X., Song, W., Kjems, J., & Li, H. (2016) · RNA Biology · doi:10.1080/15476286.2016.1220473 · Cited by 424
Self-citationCircRNA: a rising star in gastric cancer
Li, R., Jiang, J., Shi, H., Qian, H., Zhang, X., & Xu, W. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03345-5 · Cited by 415
Self-citationTranscriptome-wide investigation of circular RNAs in rice
Lu, T., Cui, L., Zhou, Y., Zhu, C., Fan, D., Gong, H., Zhao, Q., Zhou, C., Zhao, Y., Lu, D., et al. (2015) · RNA · doi:10.1261/rna.052282.115 · Cited by 412
“Zhang et al. (2014) demonstrate that exon circularization is dependent on flanking intronic complementary sequences.”
BackgroundMethodInfluentialCircRNAs and cancer: Biomarkers and master regulators
Arnaiz, E., Solé, C., Manterola, L., Iparraguirre, L., Otaegui, D., & Lawrie, C. H. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.12.002 · Cited by 411
Fan, X., Zhang, X., Wu, X., Guo, H., Hu, Y., Tang, F., & Huang, Y. (2015) · Genome biology · doi:10.1186/s13059-015-0706-1 · Cited by 415
“These results agree well with previous findings in cultured cell lines [26, 27], indicating the same mechanism of circRNA formation occurs in both cell lines in vitro and mouse preimplantation embryos in vivo.”
BackgroundResultSelf-citationZeng, Y., Du, W. W., Wu, Y., Yang, Z., Awan, F. M., Li, X., Yang, W., Zhang, C., Yang, Q., Yee, A., et al. (2017) · Theranostics · doi:10.7150/thno.19764 · Cited by 408
Plant Noncoding RNAs: Hidden Players in Development and Stress Responses
Yu, Y., Zhang, Y., Chen, X., & Chen, Y. (2019) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100818-125218 · Cited by 399
“Although circRNAs are present in many species, they cannot be detected by transcriptome profiling using polyadenylated RNAs owing to their non-polyadenylated loop structures, and they were only recently identified by specific RNA sequencing approaches (X.O. Zhang et al. 2014).”
BackgroundSelf-citationBiogenesis, identification, and function of exonic circular RNAs
Chen, I., Chen, C., & Chuang, T. (2015) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1294 · Cited by 402
“…46,866 events in 8466 human genes In-house pipeline Zhang et al. (2013)20 Intronic rRNA−&polyA−; rRNA−&RNase R+ 103 events (human) The in-house pipeline Zhang et al. (2014)15 Exonic rRNA−&polyA−; rRNA−&RNase R+ 1662 events (human) CIRCexplorer Fragment based Jeck et al. (2013)11 Exonic…”
Comparison of circular RNA prediction tools
Hansen, T. B., Venø, M. T., Damgaard, C. K., & Kjems, J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1458 · Cited by 390
“…of two non-treated RNA samples derived from Hs68 fibroblast (SRR444655 and SRR444975) and two RNase R treated samples (SRR444974 and SRR445016), we compared five different circRNA predicting algorithms: find circ (7), MapSplice (17), CIRCexplorer (10), cir-cRNA finder (11), and CIRI (12).”
MethodCircles reshaping the RNA world: from waste to treasure
Liu, J., Liu, T., Wang, X., & He, A. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0630-y · Cited by 396
“[23], CIRI [39], and MapSplice [40], are observed surprisingly dramatic differences, specifically regarding the highly expressed circRNAs and the circRNAs derived from proximal splice sites [41].”
BackgroundCSCD: a database for cancer-specific circular RNAs
Xia, S., Feng, J. Q., Chen, K., Ma, Y., Gong, J., Cai, F., Jin, Y., Gao, Y., Xia, L., Chang, H., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx863 · Cited by 397
“To identify cancer-specific circRNAs (CS-circRNAs), four popular algorithms with high performance (32): CIRI2 (31,33), find circ (5), circRNA finder (34) and Circexplorer (35,36) were utilized for detecting the back-splice junction sites of circRNAs.”
MethodThe bioinformatics toolbox for circRNA discovery and analysis
Chen, L., Wang, C., Sun, H., Wang, J., Liang, Y., Wang, Y., & Wong, G. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa001 · Cited by 402
“Notably, one gene can generate different circRNAs, which can be affected by the competition of RNA pairing across the flanking introns [24, 25].”
BackgroundInfluentialSelf-citationWidespread noncoding circular RNA s in plants
Ye, C., Chen, L., Liu, C., Zhu, Q., & Fan, L. (2015) · New Phytologist · doi:10.1111/nph.13585 · Cited by 395
Self-citationCircular RNA – New member of noncoding RNA with novel functions
Hsiao, K., Sun, H. S., & Tsai, S. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370217708978 · Cited by 395
“Alternatively, it has been reported that complementary sequences other than Alu are capable to promote backsplice (Figure 1(a), left).(17,18) Several studies using either the cloned intronic sequence-based assay or CRISPR/Cas9-mediated intronic sequence deletion consolidate the importance of regulatory roles of intron…”
BackgroundA map of human circular RNAs in clinically relevant tissues
Maass, P. G., Glažar, P., Memczak, S., Dittmar, G., Hollfinger, I., Schreyer, L., Sauer, A. V., Toka, O., Aiuti, A., Luft, F. C., et al. (2017) · Journal of Molecular Medicine · doi:10.1007/s00109-017-1582-9 · Cited by 391
“Intronic complementary sequences, inter alia repetitive elements, and the RNA-editing protein, ADAR1, were linked to the circularization of exons [7, 8].”
BackgroundRNA circularization strategies in vivo and in vitro
Petkovic, S., & Müller, S. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv045 · Cited by 386
The Diversity of Long Noncoding RNAs and Their Generation
Wu, H., Yang, L. C., & Chen, L. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.05.004 · Cited by 386
Self-citationWang, L., Long, H., Zheng, Q., Bo, X., Xiao, X., & Li, B. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1046-7 · Cited by 380
Gao, X., Xia, X., Li, F., Zhang, M., Zhou, H., Wu, X., Zhong, J., Zhao, Z., Zhao, K., Liu, D., et al. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00639-4 · Cited by 383
CircRNAs: role in human diseases and potential use as biomarkers
Verduci, L., Tarcitano, E., Strano, S., Yarden, Y., & Blandino, G. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03743-3 · Cited by 382
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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