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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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“Subsequently, computational methods revealed that introns surrounding circularized exons were enriched with repetitive sequences, such as Alu elements, with, on average, three Alu elements upstream and another three in the inverse orientation downstream (Li et al., 2015b; Liang & Wilusz, 2014; Zhang et al., 2014).”
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“CircRNAs may encompass just one or multiple exons, which indicates the potential for alternatively spliced isoforms.(3,22,28) They may also consist of intronic RNA sequences that are formed when intronic lariats fail to debranch.”
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Chen, L., & Yang, L. C. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.01.002 · Cited by 152
“circRNA Formation Mediated by Intronic IRAlus Nearly half of Alu repeats are located in introns [27].”
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A Parkinson's disease CircRNAs Resource reveals a link between circSLC8A1 and oxidative stress
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“In this study, TopHatFusion was used to identify candidate fusion junction sites with the same parameters used in CIRCexplorer.(13,29) Distance between 2 fusion junction sites was set to be 5 kb and 50 kb for rice and humans, respectively.”
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“The biogenesis and formation of exonic circRNA mainly include three types of circularization driven by lariats [66, 67], intron-pairing [68, 69], and RNA-binding proteins (RBPs) [70, 71], which are described below.”
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Nanomedicine-Based Approaches for mRNA Delivery
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BackgroundOn the genetic basis of tail-loss evolution in humans and apes
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“Notably, inverted Alu pairs can facilitate the biogenesis of exonic circular RNAs (circRNAs) through ‘backsplicing’ 43,44 .”
BackgroundSelf-citationInsights into the biogenesis and potential functions of exonic circular RNA
Ragan, C., Goodall, G. J., Shirokikh, N. E., & Preiss, T. (2019) · Scientific Reports · doi:10.1038/s41598-018-37037-0 · Cited by 137
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“In exosomes, circRNAs are enriched and stable [19] and can be transferred into target cells [20, 21].”
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Kong, Z., Wan, X., Lu, Y., Zhang, Y., Huang, Y., Xu, Y., Liu, Y., Zhao, P., Xiang, X., Li, L., et al. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14791 · Cited by 138
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Advances in circular RNAs and their roles in breast Cancer
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“From the raw FASTQ files, adapter contamination was removed and sequences were aligned to the Macaca mulatta (rheMac2) genome with TopHat2 (v2.”
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“CircRNAs are mainly generated from exons of protein-coding genes [59].”
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“Cell-type gene expression was found in (Zhang et al , 2014a,b).”
Circular RNAs in kidney disease and cancer
van Zonneveld, A. J., Kölling, M., Bijkerk, R., & Lorenzen, J. M. (2021) · Nature Reviews Nephrology · doi:10.1038/s41581-021-00465-9 · Cited by 126
Heat stress alters genome-wide profiles of circular RNAs in Arabidopsis
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A guide to naming human non‐coding RNA genes
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“Recent studies have suggested roles for circRNAs in competitive regulation of pre-mRNA splicing (Ashwal-Fluss et al , 2014; Zhang et al , 2014), competitive binding to microRNAs (Hansen et al , 2013; Memczak et al , 2013), regulation of RNA polymerase II (Li et al , 2015) and involvement in innate…”
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“To further evaluate the sensitivity and precision of NCLscan for simultaneously detecting intergenic and intragenic NCL transcripts, we applied NCLscan and eight other tools (STAR, MapSplice2, CRAC, segemehl, TopHat-Fusion, find circ (29), CIRCexplorer (80) and CIRI (81)) to simulated RNA-seq datasets.”
BackgroundMethodInfluentialCircular RNA expression in cutaneous squamous cell carcinoma
Sand, M. S., Bechara, F. G., Gambichler, T., Sand, D., Bromba, M., Hahn, S. A., Stockfleth, E., & Hessam, S. (2016) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2016.05.012 · Cited by 124
The emerging role and clinical implication of human exonic circular RNA
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“In the intron-paring model, circularization via backsplicing is associated with base-pairing across different introns especially between repetitive sequences such as ALU repeats, while the lariat-driven circularization occurs by joining the splice sites of the exons that are skipped during linear RNA formation.(8,18,1…”
BackgroundTransCirc: an interactive database for translatable circular RNAs based on multi-omics evidence
Huang, W., Ling, Y., Zhang, S., Xia, Q., Cao, R., Fan, X., Fang, Z., Wang, Z., & Zhang, G. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa823 · Cited by 127
“CIRCexplorer (38) and CIRI2 (34) were used to detect reads spanning back-splice junction in ribosome/polysome profiling.”
MethodIdentification and characterization of circular RNAs in zebrafish
Shen, Y., Guo, X., & Wang, W. (2016) · FEBS Letters · doi:10.1002/1873-3468.12500 · Cited by 123
Geng, X., Jia, Y., Zhang, Y., Shi, L., Li, Q., Zang, A., & Wang, H. (2019) · Epigenomics · doi:10.2217/epi-2019-0295 · Cited by 123
Self-citationXiang, Q., Kang, L., Wang, J., Liao, Z., Song, Y., Zhao, K., Wang, K., Cao, Y., & Zhang, Y. (2020) · EBioMedicine · doi:10.1016/j.ebiom.2020.102679 · Cited by 124
Self-citationA comprehensive review of circRNA: from purification and identification to disease marker potential
Xu, S., Zhou, L., Ponnusamy, M., Zhang, L., Dong, Y., Zhang, Y., Wang, Q., Liu, J., & Wang, K. (2018) · PeerJ · doi:10.7717/peerj.5503 · Cited by 121
Self-citationIntriguing circles: Conflicts and controversies in circular RNA research
Li, H., Ma, X., & Li, H. (2019) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1538 · Cited by 121
“…is associated with trans-acting factors like RNA binding proteins (RBPs) (Aktas et al., 2017; Conn et al., 2015), transcription factors (J. Meng et al., 2018; Shan et al., 2017), and cis-regulatory elements like reverse complementary matches (RCMs) (Jeck et al., 2013; X. O. Zhang et al., 2014).”
BackgroundMethodLi, H., Lan, T., Liu, H., Liu, C., Dai, J., Xu, L., Cai, Y., Hou, G., Xie, K., Liao, M., et al. (2021) · Hepatology · doi:10.1002/hep.32232 · Cited by 124
“[19] The efficiency of circRNA circularization, especially exonderived ones, can be regulated by RBPs- mediated RNA pairing across flanking introns.[18,20] To explore the mechanisms of cGGNBP2 circularization, we examined the sequences of flanking introns of cGGNBP2 and found highly reverse complementary sequences bet…”
BackgroundCircular RNAs: An emerging type of RNA in cancer
Hou, L., & Zhang, J. (2017) · International Journal of Immunopathology and Pharmacology · doi:10.1177/0394632016686985 · Cited by 120
Dong, W., Li, H., Qing, X., Huang, D., & Li, H. (2016) · Scientific Reports · doi:10.1038/srep39080 · Cited by 119
Computational Strategies for Exploring Circular RNAs
Gao, Y., & Zhao, F. (2018) · Trends in Genetics · doi:10.1016/j.tig.2017.12.016 · Cited by 124
Saaoud, F., Charles Drummer, I. V., Shao, Y., Sun, Y., Lu, Y., Xu, K., Ni, D., Jiang, X., Wang, H., & Yang, X. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107715 · Cited by 121
Self-citationRNA sequencing and Prediction Tools for Circular RNAs Analysis
López-Jiménez, E. A., Rojas, A. M., & Andrés‐León, E. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1426-1_2 · Cited by 121
An intriguing RNA species—perspectives of circularized RNA
Shen, T., Han, M., Wei, G., & Ni, T. (2015) · Protein & Cell · doi:10.1007/s13238-015-0202-0 · Cited by 115
“The second is the intron-pairing-driven model, which emphasizes that flanking inverted repeats aside back-spliced exons are crucial for the direct splicing and ligation between the downstream donor site and the upstream acceptor site (Jeck et al., 2013; Jeck and Sharpless, 2014; Zhang et al., 2014).”
BackgroundInfluentialFOXP1 circular RNA sustains mesenchymal stem cell identity via microRNA inhibition
Cherubini, A., Barilani, M., Rossi, R. L., Jalal, M., Rusconi, F., Buono, G., Ragni, E., Cantarella, G., Simpson, H., Péault, B., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz199 · Cited by 117
Nuclear export of circular RNA
Ngo, L. H., Bert, A. G., Dredge, B. K., Williams, T. D., Murphy, V. J., Li, W., Hamilton, W. B., Carey, K. T., Toubia, J., Pillman, K. A., et al. (2024) · Nature · doi:10.1038/s41586-024-07060-5 · Cited by 121
Chen, L., Zhang, P., Fan, Y., Huang, J., Li, Q., Li, Q., JianBing, Y. A. N., Muehlbauer, G. J., Schnable, P. S., Dai, M., et al. (2017) · New Phytologist · doi:10.1111/nph.14901 · Cited by 119
“Like Alu sequences in humans (Zhang et al., 2014), LLEs, LRE and DLEs have divergent or convergent distribution patterns around circRNAs, ensuring the formation of reverse complementary pairs of LLEs (LLERCPs), LREs (LRERCPs) and DLEs (DLERCPs).”
BackgroundInfluentialSelf-citationCircRNA Expression Profile in Early-Stage Lung Adenocarcinoma Patients
Zhao, J., Li, L., Wang, Q., Han, H., Zhan, Q., & Xu, M. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000485953 · Cited by 117
Identification of RNA structures and their roles in RNA functions
Cao, X., Zhang, Y., Ding, Y., & Wan, Y. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00748-6 · Cited by 124
Self-citationDong, R., Zhang, X.-O., Zhang, Y., Ma, X.-K., Chen, L., & Yang, L. C. (2016) · Cell Research · doi:10.1038/cr.2016.42 · Cited by 113
Self-citationZhang, J., Lu, J. L., Xie, H., Wang, D.-P., Ni, H., Zhu, Y., Ren, L., Meng, X., & Wang, R. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1430-7 · Cited by 114
The therapeutic potential of circular RNAs
O’Leary, E. T., Jiang, Y., Kristensen, L. S., Hansen, T. B., & Kjems, J. (2025) · Nature Reviews Genetics · doi:10.1038/s41576-024-00806-x · Cited by 131
“Broad characterization of the circRNA landscape using next-generation sequencing has shown that inverted repeats, typically in the form of Alu elements, are highly enriched in the vicinity of backsplicing events 8,98 .”
Circular RNAs: Unexpected outputs of many protein-coding genes
Wilusz, J. E. (2016) · RNA Biology · doi:10.1080/15476286.2016.1227905 · Cited by 116
“Multiple groups have now translated knowledge about circular RNA biogenesis mechanisms into methods for expressing circular RNAs from introns(42) or exons in cells.(25,26,37,40,41,61,65,69,82,92) In most cases, exonic circular RNA expression plasmids consist of a promoter driving only the exon(s) that circularize alon…”
BackgroundInfluentialNew insight into circRNAs: characterization, strategies, and biomedical applications
Feng, X., Zhu, S.-X., Pu, K., Huang, H., Chen, Y., & Wang, W. (2023) · Experimental Hematology and Oncology · doi:10.1186/s40164-023-00451-w · Cited by 119
“If the intron has a unique inverted repeat sequence (such as Alu) [12, 52], after base pairing occurs, the splicing donor is brought close to the splicing acceptor, which promotes nucleophilic attack and splicing and can also promote the production of cir-cRNA.”
BackgroundInfluentialCircular RNAs: Isolation, characterization and their potential role in diseases
Liu, L., Wang, J., Khanabdali, R., Kalionis, B., Tai, X., & Xia, S. (2017) · RNA Biology · doi:10.1080/15476286.2017.1367886 · Cited by 112
“Zhang et al.(17) discovered almost 10 thousand circRNAs in human”
InfluentialProceedings of the 16th Annual UT-KBRIN Bioinformatics Summit 2016: bioinformatics
Rouchka, E. C., Chariker, J. H., Tieri, D. A., Park, J. W., Rajurkar, S. D., Singh, V., Verma, N. K., Cui, Y., FARMAN, M. L., Condon, B. J., et al. (2017) · BMC Bioinformatics · doi:10.1186/s12859-017-1781-y · Cited by 112
Self-citationIdentification of cucumber circular RNAs responsive to salt stress
Zhu, Y., Jia, J., Yang, L., Xia, Y., Zhang, H., Jia, J., Zhou, R., Nie, P.-Y., Yin, J., Ma, D. M., et al. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1712-3 · Cited by 115
Self-citationBiogenesis of circular RNA s and their roles in cardiovascular development and pathology
Li, M., Ding, W., Sun, T., Tariq, M., Xu, T., Li, P., & Wang, J. (2017) · FEBS Journal · doi:10.1111/febs.14191 · Cited by 115
Wang, J., Yang, Y., Jin, L., Ling, X., Liu, T., Chen, T., Ji, Y., Yu, W., & Zhang, B. (2018) · BMC Plant Biology · doi:10.1186/s12870-018-1332-3 · Cited by 110
CircPrimer: a software for annotating circRNAs and determining the specificity of circRNA primers
Zhong, S., Wang, J., Zhang, Q., Xu, H., & Feng, J. (2018) · BMC Bioinformatics · doi:10.1186/s12859-018-2304-1 · Cited by 113
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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