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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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Exon Skipping Is Correlated with Exon Circularization
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“…when complementary sequences from different introns base-pair and bring the intervening splice sites close together (Liang and Wilusz 2014; Zhang et al. 2014), but circRNA levels are also controlled by the combinatorial action of RNA-binding proteins (Ashwal-Fluss et al. 2014; Conn et al.…”
The pro-metastasis effect of circANKS1B in breast cancer
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Self-citationA Circular RNA Protects Dormant Hematopoietic Stem Cells from DNA Sensor cGAS-Mediated Exhaustion
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“14 15 20 Until now, it remains unclear whether circRNAs can act as ceRNAs to regulate the viability and functions of NPCs, and the pathological process of IVDD.”
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“Without 30 polyadenylated tails, circRNAs had been largely missed by the enrichment of polyadenylated RNAs for deep sequencing (referred to as poly(A) RNA-seq), but were successfully captured by two nonpolyadenylated RNA isolation strategies prior to deep sequencing (referred to as ribo or poly(A) RNA-seq, respectivel…”
MethodInfluentialSelf-citationCircSERPINE2 protects against osteoarthritis by targeting miR-1271 and ETS-related gene
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“Some tools, such as find-circ [3], CIRI [86], MapSplice [16], CIRCexplorer [19], circRNA finder [87], and Acfs [88], have been developed to annotate circRNAs, and large amounts of circRNAs are stable and conserved and exhibit cell/tissue-specific expression.”
MethodCircular RNAs: A Novel Class of Functional RNA Molecules with a Therapeutic Perspective
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“According to the recent literature, they may regulate alternative splicing [10, 14], bind and sequester RNAbinding proteins and ribonucleoprotein complexes [6, 15], be translated, bind in trans to other RNA sequences [5], or regulate miRNA expression [6, 15].”
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Accurate quantification of circular RNAs identifies extensive circular isoform switching events
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Self-citationGoing circular: history, present, and future of circRNAs in cancer
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“According to the differences of origins, circRNAs can be divided into three groups: exonic circRNAs (ecRNAs) [28, 29], exon-intron circRNA (elciRNAs) [30] and circular intronic RNAs (ciRNAs) [31] (Fig.”
BackgroundSelf-citationHanan, M., Soreq, H., & Kadener, S. (2017) · RNA Biology · doi:10.1080/15476286.2016.1255398 · Cited by 229
“ADAR editing enzymes can efficiently bind and edit reverse complementary sequences, leading to the disruption of RNA secondary structures, which in some cases are key for the modulation of circRNAs production.(2,28) Indeed, intronic complementary sequences surrounding circRNAs are enriched in A-to-I editing cites, inc…”
BackgroundCircular RNA enrichment in platelets is a signature of transcriptome degradation
Alhasan, A. A., Izuogu, O. G., Al‐Balool, H. H., Steyn, J. S., Evans, A., Colzani, M., Ghevaert, C., Mountford, J. C., Marenah, L., Elliott, D. J., et al. (2015) · Blood · doi:10.1182/blood-2015-06-649434 · Cited by 229
“This confirms that these structures include circRNAs.”
BackgroundMethodInfluentialLong non-coding RNAs: emerging players regulating plant abiotic stress response and adaptation
Jha, U. C., Nayyar, H., Jha, R., Khurshid, M., Zhou, M., Mantri, N. L., & Siddique, K. H. M. (2020) · BMC Plant Biology · doi:10.1186/s12870-020-02595-x · Cited by 227
Circular RNAs: emerging cancer biomarkers and targets
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Self-citationCapturing the interactome of newly transcribed RNA
Bao, X., Guo, X., Yin, M., Tariq, M., Lai, Y., Kanwal, S., Zhou, J., Li, N., Lv, Y., Pulido-Quetglas, C., et al. (2018) · Nature Methods · doi:10.1038/nmeth.4595 · Cited by 222
Self-citationLi, X., Wang, Z. J., Ye, C., Zhao, B., Li, Z.-L., & Yang, Y. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-1006-x · Cited by 222
“0) [17] and CIRCexplorer2 softwares [18].”
Roles of circular RNAs in immune regulation and autoimmune diseases
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Long noncoding RNAs: Re-writing dogmas of RNA processing and stability
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“As pre-mRNAs generally contain multiple intronic repeats, distinct circRNAs can be produced depending on which repeats base pair to one another [155].”
BackgroundEmerging Epigenetic Regulation of Circular RNAs in Human Cancer
Wu, J., Qi, X., Liu, L., Hu, X. T., Liu, J., Yang, J., Yang, J., Lu, L., Zhang, Z., Ma, S., et al. (2019) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.04.011 · Cited by 221
“At present, algorithms used for circRNA research include map-splice,(27) Circ Seq,(10) CIRI,(28) and Circ explorer.(29) The CIRI annotation-related algorithm can not only detect circRNAs transcribed from introns or intergenomic regions but also be applied to the sequencing data of annotated or unannotated eukaryotes.”
MethodMicroarray is an efficient tool for circRNA profiling
Li, S., Teng, S., Xu, J., Su, G., Zhang, Y., Zhao, J., Zhang, S., Wang, H., Qin, W., Lü, Z., et al. (2018) · Briefings in Bioinformatics · doi:10.1093/bib/bby006 · Cited by 225
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Self-citationIncreased complexity of circRNA expression during species evolution
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“Although inefficiently catalyzed by the spliceosome and generally expressed at low levels,(6-8) circRNA formation can be facilitated by both RNA pairing of orientation-opposite complementary sequences across flanking introns and protein factors that are capable of binding flanking introns to bridge unfavorable backspl…”
BackgroundMethodSelf-citationA novel plasma circular RNA circ FARSA is a potential biomarker for non‐small cell lung cancer
Hang, D., Zhou, J., Qin, N., Zhou, W., Ma, H., Jin, G., Hu, Z., Dai, J., & Shen, H. (2018) · Cancer Medicine · doi:10.1002/cam4.1514 · Cited by 219
The emerging landscape of circular RNA ciRS-7 in cancer (Review)
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Metazoan tRNA introns generate stable circular RNAs in vivo
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“Despite their ubiquity, the functions of endogenous circRNAs are largely unknown (Hentze and Preiss 2013; Lasda and Parker 2014), and methods for generating and studying them in vivo are few and far between (Ford and Ares 1994; Zhang et al. 2014; Petkovic and Müller 2015).”
BackgroundMa, C., Wang, X., Yang, F., Zang, Y., Liu, J., Wang, X., Xu, X., Li, W., Jia, J., & Liu, Z. (2020) · Molecular Cancer · doi:10.1186/s12943-020-01268-5 · Cited by 208
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Circular RNAs: A novel type of non-coding RNA and their potential implications in antiviral immunity
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Self-citationAgeing-associated changes in transcriptional elongation influence longevity
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“Another potential indicator of transcriptional noise is the increased formation of circular RNAs (circRNAs) 39,40 , that is, of back-spliced transcripts with covalently linked 3′ and 5′ ends 41 .”
Regulatory Role of Circular RNAs and Neurological Disorders
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“ization, especially in the case that ecircRNAs contain a single exon [30, 33, 35].”
BackgroundCoding or Noncoding, the Converging Concepts of RNAs
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“1.1), before the output was processed using CIRCexplorer.”
BackgroundMethodInfluentialNon-coding RNAs in cardiovascular cell biology and atherosclerosis
Fasolo, F., Gregoli, K. D., Mäegdefessel, L., & Johnson, J. L. (2019) · Cardiovascular Research · doi:10.1093/cvr/cvz203 · Cited by 203
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“The study concluded that a single gene produces multiple circular RNAs [17].”
BackgroundCircular RNAs: a new frontier for cancer diagnosis and therapy
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“Reverse-oriented repeats that usually appear in the introns on both sides of the exons in ecRNAs can be important for the circularization of exons [8].”
BackgroundComprehensive landscape and future perspectives of circular RNAs in colorectal cancer
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Circular RNAs in Cardiovascular Disease: An Overview
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“Therefore, circRNAs are interrelated with each other, and the competitive balance among them can affect the expression of mRNA [12, 36].”
BackgroundInfluentialShi, L., Yan, P., Liang, Y., Sun, Y., Shen, J., Zhou, S., Lin, H. M., Liang, X. H., & Cai, X. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.556 · Cited by 199
“Another RNA-binding protein, QKI, seems not to participate in the AR-related biogenesis of circRNAs based on our data.(33) ADAR1 has been shown to be critical during cancer development via abnormal A-to-I RNA editing(26) and this function in HCC has also been documented.”
BackgroundFunctions and clinical significance of circular RNAs in glioma
Sun, J., Li, B., Shu, C., Ma, Q., & Wang, J. (2020) · Molecular Cancer · doi:10.1186/s12943-019-1121-0 · Cited by 195
Cartilage Homeostasis and Osteoarthritis
Fujii, Y., Liu, L., Yagasaki, L., Inotsume, M., Chiba, T., & Asahara, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116316 · Cited by 206
Transposable Elements in Human Cancer: Causes and Consequences of Deregulation
Anwar, S. L., Wulaningsih, W., & Lehmann, U. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18050974 · Cited by 209
“Numerous long circular ncRNAs are found in fibroblasts and act in a similar manner to “sponges” for miRNAs, in which intronic Alu sequences that flank exon and the alternative formation of inverted Alu pairs are suggested to greatly contribute to RNA circularization [148,149].”
BackgroundCircular RNA circDLC1 inhibits MMP1-mediated liver cancer progression via interaction with HuR
Liu, H., Lan, T., Li, H., Xu, L., Chen, X., Liao, H., Chen, X., Du, J., Cai, Y., Wang, J., et al. (2020) · Theranostics · doi:10.7150/thno.53227 · Cited by 191
The Emerging Function and Mechanism of ceRNAs in Cancer
Wang, Y., Hou, J., He, D., Sun, M., Zhang, P., Yu, Y., & Chen, Y. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.02.001 · Cited by 187
Hall, I. F., Climent, M., Quintavalle, M., Farina, F. M., Schorn, T., Zani, S., Carullo, P., Kunderfranco, P., Civilini, E., Condorelli, G., et al. (2019) · Circulation Research · doi:10.1161/circresaha.118.314240 · Cited by 188
Circular RNAs as Therapeutic Agents and Targets
Holdt, L. M., Kohlmaier, A., & Teupser, D. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01262 · Cited by 189
Chen, J., Wu, Y., Luo, X., Jin, D., Zhou, W., Ju, Z., Wang, D., Meng, Q., Wang, H., Fu, X., et al. (2021) · Theranostics · doi:10.7150/thno.59546 · Cited by 190
Self-citationcircRNA-miRNA-mRNA regulatory network in human lung cancer: an update
Liang, Z., Guo, C., Zou, M., Meng, P., & Zhang, T.-T. (2020) · Cancer Cell International · doi:10.1186/s12935-020-01245-4 · Cited by 190
Dai, X., Chen, C., Yang, Q., Xue, J., Chen, X., Sun, B., Luo, F., Liu, X., Xiao, T., Xu, H., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0485-1 · Cited by 184
Circular RNA expression in human hematopoietic cells is widespread and cell-type specific
Nicolet, B. P., Engels, S., Aglialoro, F., van den Akker, E., Lindern, M. V., & Wolkers, M. C. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky721 · Cited by 188
“01 (33) to detect, filter and annotate circRNA (see supplementary method).”
BackgroundCircular RNAs in Brain and Other Tissues: A Functional Enigma
Chen, W., & Schuman, E. M. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.06.006 · Cited by 182
“In addition, neuronal genes often have long introns and it is known that circularized exons are more frequently flanked by longer introns [16,30,31,39].”
Improved circRNA Identification by Combining Prediction Algorithms
Hansen, T. B. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00020 · Cited by 181
“…(Zeng et al., 2017), and we previously analyzed and compared the output from 5 different algorithms (Hansen et al., 2015): circRNA_finder (Westholm et al., 2014), CIRCexplorer (Zhang et al., 2014), CIRI (Gao et al., 2015), find_circ (Memczak et al., 2013), and MapSplice (Wang et al., 2010).”
MethodEger, N., Schoppe, L., Schuster, S., Laufs, U., & Boeckel, J. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1426-1_4 · Cited by 184
RNA circles with minimized immunogenicity as potent PKR inhibitors
Liu, C., Guo, S.-K., Fang, N., Xu, Y.-F., Yang, L. C., & Chen, L. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.11.019 · Cited by 178
Self-citationCircular RNAs in Heart Failure
Devaux, Y., Creemers, E. E., Boon, R. A., Werfel, S., Thum, T., Engelhardt, S. H., Dimmeler, S., & Squire, I. B. (2017) · European Journal of Heart Failure · doi:10.1002/ejhf.801 · Cited by 177
The potential of using blood circular RNA as liquid biopsy biomarker for human diseases
Wen, G., Zhou, T., & Gu, W. (2020) · Protein & Cell · doi:10.1007/s13238-020-00799-3 · Cited by 183
Tracing the expression of circular RNAs in human pre-implantation embryos
Dang, Y., Yan, L., Hu, B., Fan, X., Ren, Y., Li, R., Lian, Y., Yan, J., Li, Q., Zhang, Y., et al. (2016) · Genome biology · doi:10.1186/s13059-016-0991-3 · Cited by 177
“(XLSX 245 kb) Additional file 6: Table S5.”
BackgroundMethodResultInfluentialSelf-citationLi, Z., Ruan, Y., Zhang, H., Shen, Y., Li, T., & Xiao, B. (2019) · Cancer Science · doi:10.1111/cas.14211 · Cited by 173
Lavenniah, A., Luu, T. D. A., Li, Y. P., Lim, T. B., Jiang, J., Ackers-Johnson, M. A., & Foo, R. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.04.006 · Cited by 181
“Longer flanking introns promote more efficient back-splicing than shorter flanking introns and this has been well reported.(28,30,31) In our study, we used the longer flanking introns to maximize circularization efficiency.”
MethodWang, Y., Kumari, M., Chen, G., Hong, M.-H., Yuan, J. P., Tsai, J.-L., & Wu, H. (2023) · Journal of Biomedical Science · doi:10.1186/s12929-023-00977-5 · Cited by 198
“Thus, circRNAs have a median half-life of at least 2.5 times longer than linear mRNA isoforms in mammalian cells [132, 266].”
BackgroundInfluentialComprehensive characterization of circular RNAs in ~ 1000 human cancer cell lines
Ruan, H., Xiang, Y., Ko, J., Li, S., Jing, Y., Zhu, X., Ye, Y., Zhang, Z., Mills, T., Feng, J. Q., et al. (2019) · Genome Medicine · doi:10.1186/s13073-019-0663-5 · Cited by 169
“To achieve the most reliable precision and sensitivity, as well as balanced performance [32], we combined four circRNA prediction methods, CIRI2 [33], CIRCexplorer2 [34], circRNA_finder [35], and find_circ [3], with default settings, to identify circRNAs from the CCLE RNA-seq dataset.”
MethodInfluentialNon-coding RNAs: the new central dogma of cancer biology
Saw, P. E., Xu, X., Chen, J., & Song, E. (2020) · Science China Life Sciences · doi:10.1007/s11427-020-1700-9 · Cited by 180
“Unlike the canonical splicing of linear RNA, circRNAs are formed via backsplicing (Zhang et al., 2014c).”
BackgroundInfluentialZhang, C., Han, X., Yang, L., Fu, J., Sun, C., Huang, S., Xiao, W., Gao, Y., Liang, Q., Wang, X., et al. (2020) · Theranostics · doi:10.7150/thno.48264 · Cited by 172
Self-citationPeng, Y., Xu, Y., Zhang, X., Deng, S., Yuan, Y., Luo, X., Hossain, M. T., Zhu, X., Du, K., Hu, F., et al. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01457-w · Cited by 175
“Most circRNAs are produced by the back splicing of exons, a non-canonical splicing process [2, 3].”
BackgroundSelf-citationKristensen, L. S., Okholm, T. L. H., Venø, M. T., & Kjems, J. (2017) · RNA Biology · doi:10.1080/15476286.2017.1409931 · Cited by 170
Reconstruction of full-length circular RNAs enables isoform-level quantification
Zheng, Y., Ji, P., Chen, S., Hou, L., & Zhao, F. (2019) · Genome Medicine · doi:10.1186/s13073-019-0614-1 · Cited by 171
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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