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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 are abundant, conserved, and associated with ALU repeats
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Emerging roles of circRNAs in the pathological process of myocardial infarction
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“The accuracy and comprehensiveness of circRNA identification strategies are determined by the rigor and reliability of the algorithm; however, there is little overlap in the results of the identification of various algorithms; thus choosing appropriate algorithms and combination of different bioinformatics tools shoul…”
MethodSelf-citationThe role of Alu elements in the cis-regulation of RNA processing
Daniel, C., Behm, M., & Öhman, M. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1990-3 · Cited by 62
“Several studies demonstrate that in humans, the complementary sequences often consist of inverted Alu repeats [83, 96, 97].”
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Circular RNAs: The Brain Transcriptome Comes Full Circle
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Circular RNA expression and function in the brain
Sekar, S., & Liang, W. S. (2019) · Non-coding RNA Research · doi:10.1016/j.ncrna.2019.01.001 · Cited by 64
RNA structures in alternative splicing and back‐splicing
Xu, B., Meng, Y., & Jin, Y. (2020) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1626 · Cited by 63
“…2014; Conn et al., 2015; Errichelli et al., 2017); the other is that the flanking introns are reversely complementary to form secondary structures that connects flanking introns together (Ivanov et al., 2015; Jeck et al., 2013; Liang & Wilusz, 2014; Zhang et al., 2014; Zhang, Xue, et al., 2016).”
BackgroundInfluentialFu, X.-Z., Zhang, X., Qiu, J.-Y., Zhou, X., Yuan, M., He, Y., Chun, C.-P., Cao, L., Ling, L.-L., & Peng, L.-Z. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-2087-1 · Cited by 61
Self-citationLighting Up CircRNA Using a Linear DNA Nanostructure
Jiao, J., Xiang, Y., Duan, C., Liu, Y., Li, C., & Li, G. (2020) · Analytical Chemistry · doi:10.1021/acs.analchem.0c02146 · Cited by 60
Loop-Mediated Isothermal Amplification Detection of SARS-CoV-2 and Myriad Other Applications
Moore, K. J. M., Cahill, J., Aidelberg, G., Aronoff, R., Bektaş, A., Bezdan, D., Butler, D., Chittur, S. V., Codyre, M., Federici, F., et al. (2021) · Journal of Biomolecular Techniques JBT · doi:10.7171/jbt.21-3203-017 · Cited by 59
“Some disadvantages of this method (Zhang et al. 2014) include a low signal to noise ratio (improved by adding Calcium (Almasi et al. 2012)), the relatively low abundance of real-time turbidimeters, and incompatibility with minimally processed turbid samples.”
MethodDeciphering the roles of lncRNAs in breast development and disease
Richard, J. L. C., & Eichhorn, P. J. A. (2018) · Oncotarget · doi:10.18632/oncotarget.24591 · Cited by 62
Long non-coding RNAs in vascular biology and disease
Jaé, N., Heumüller, A. W., Fouani, Y., & Dimmeler, S. (2019) · Vascular Pharmacology · doi:10.1016/j.vph.2018.03.003 · Cited by 62
Methods for analysis of circular RNAs
Pandey, P. R., Munk, R. B., Kundu, G., De, S., Abdelmohsen, K., & Gorospe, M. (2019) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1566 · Cited by 61
“Intron-pairing and lariat-driven circularization rely on reverse complementary motifs of introns to promote the circularization through alternative 50 to 30 splicing (Ivanov et al., 2015; X. O. Zhang et al., 2014).”
BackgroundCircAST: Full-Length Assembly and Quantification of Alternatively Spliced Isoforms in Circular RNAs
Wu, J., Li, Y., Wang, C., Cui, Y., Xu, T., Wang, C., Wang, X., Sha, J., Jiang, B., Wang, K., et al. (2019) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2019.03.004 · Cited by 59
“In previous studies, the reads of exon model per million mapped reads (RPM) metric has been used to evaluate the expression of circRNAs [14].”
MethodInfluentialCircRNAs: a new target for the diagnosis and treatment of digestive system neoplasms
Li, J., Xu, Q., Huang, Z., Mao, N., Lin, Z., Cheng, L., Sun, B., & Wang, G. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03495-0 · Cited by 59
Characterization of conserved circular RNA in polyploid Gossypium species and their ancestors
Zhao, T., Wang, L., Li, S., Xu, M., Guan, X., & Zhou, B. (2017) · FEBS Letters · doi:10.1002/1873-3468.12868 · Cited by 58
“sequences, which can promote the circulation of circRNAs in mammals [18].”
BackgroundResultInfluentialAnalysis of the circular RNA transcriptome in endometrial cancer
Chen, B. J., Byrne, F. L., Takenaka, K., Modesitt, S. C., Olzomer, E. M., Mills, J. D., Farrell, R., Hoehn, K. L., & Janitz, M. (2017) · Oncotarget · doi:10.18632/oncotarget.23534 · Cited by 57
Circular RNAs in digestive system cancer: potential biomarkers and therapeutic targets.
Sheng, J., Liu, L., Wang, M.-R., & Li, P. (2018) · Europe PMC (PubMed Central) · Cited by 57
Circular RNAs: A New Piece in the Colorectal Cancer Puzzle
Artemaki, P. I., Scorilas, A., & Kontos, C. K. (2020) · Cancers · doi:10.3390/cancers12092464 · Cited by 57
“However, alternative circularization is a rather complicated process, in which RBPs are implicated [30].”
BackgroundCircular RNAs: Functions and Clinical Significance in Cardiovascular Disease
Zhang, L., Zhang, Y., Wang, Y., Zhao, Y., Ding, H., & Li, P. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.584051 · Cited by 58
Self-citationHNRNPM controls circRNA biogenesis and splicing fidelity to sustain cancer cell fitness
Ho, J., Tullio, F. D., Schwarz, M. C., Low, D. H. P., Incarnato, D., Gay, F. P. H., Tabaglio, T., Zhang, J., Wollmann, H., Chen, L., et al. (2021) · eLife · doi:10.7554/elife.59654 · Cited by 60
“…long introns, RNA secondary and tertiary structures, stemming from competitive long-and short-range pairings between short inverted repeat (IR) sequences, have been shown to be partially required for appropriate splice site selection ( Rogic et al., 2008 ; Zhang et al., 2014 ; Jeck et al., 2013 ).”
Self-citationN6-Methyladenosine Modification Opens a New Chapter in Circular RNA Biology
Wu, J., Guo, X., Wen, Y., Huang, S.-Q., Yuan, X., Tang, L., & Sun, H. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.709299 · Cited by 55
Mechanisms Regulating Abnormal Circular RNA Biogenesis in Cancer
Huang, Y., & Zhu, Q. (2021) · Cancers · doi:10.3390/cancers13164185 · Cited by 57
“Most highly expressed circRNAs are composed of multiple internal exons of pre-mRNAs and contain few introns, indicating that back-splicing and canonical splicing are coupled [20].”
BackgroundGao, F., Xu, Q., Tang, Z., Zhang, N., Huang, Y., Li, Z., Dai, Y., Yu, Q., & Zhu, J. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03494-5 · Cited by 57
“Alu elements are well-known retrotransposons, members of the short interspersed nuclear element (SINE) family of repetitive elements, and IARs around exons promote circRNA formation [40, 41].”
BackgroundSun, J., Xie, M., Huang, Z., Li, H., Chen, T., Sun, R., Wang, J., Xi, Q., Wu, T., & Zhang, Y. (2017) · Journal of Animal Science · doi:10.2527/jas.2016.0867 · Cited by 58
“In the present study, we used previously published algorithms (Zhang et al., 2014) to annotate the back-spliced exons for circRNA prediction.”
MethodSelf-citationReaders of the m6A epitranscriptomic code
Berlivet, S., Scutenaire, J., Deragon, J., & Bousquet‐Antonelli, C. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2018.12.008 · Cited by 65
Ye, Y.-L., Yin, J. J., Hu, T., Zhang, L., Wu, L., & Pang, Z. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i41.6273 · Cited by 57
Protein-Related Circular RNAs in Human Pathologies
Wawrzyniak, O., Zarębska, Ż., Kuczyński, K., Gotz‐Więckowska, A., & Rolle, K. (2020) · Cells · doi:10.3390/cells9081841 · Cited by 58
“Alu elements are widely distributed along intronic sequences, allowing multiple RNA pairings and competitive IRAlu formation and leading to alternative circularization [18,19].”
BackgroundAdvances in the Identification of Circular RNAs and Research Into circRNAs in Human Diseases
Jiao, S., Song, W. C., Huang, S., Liu, M., & Gao, B. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.665233 · Cited by 57
Roles of ncRNAs as ceRNAs in Gastric Cancer
Ye, J., Li, J., & Zhao, P. (2021) · Genes · doi:10.3390/genes12071036 · Cited by 54
“According to its components, they can be divided into three categories: exon circular RNAs (ecircRNAs) [169], intron circular RNAs (ciRNAs) [170], and exon–intron circular RNAs (EIciRNAs) [171], each of which has different molecular structures but have similar binding sites and regulatory functions, and provides a tem…”
BackgroundCircular RNA—Is the Circle Perfect?
Caba, L., Florea, L., Gug, C., Dimitriu, D. C., & Gorduza, E. V. (2021) · Biomolecules · doi:10.3390/biom11121755 · Cited by 56
Dattilo, D., Timoteo, G. D., Setti, A., Giuliani, A., Peruzzi, G., Beltran-Nebot, M., Centrón-Broco, A., Mariani, D., Mozzetta, C., & Bozzoni, I. (2023) · Nature Communications · doi:10.1038/s41467-023-37578-7 · Cited by 56
Exosomal circRNAs in cancer: Implications for therapy resistance and biomarkers
Lin, Z., Ji, Y., Zhou, J., Li, G., Wu, Y., Liu, W., Li, Z., & Liu, T. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216245 · Cited by 57
Chen, Z., Song, J., Xie, L., Xu, G., Zheng, C., Xia, X., Lu, F., Ma, X., Zou, F., Jiang, J., et al. (2023) · Cell Death and Differentiation · doi:10.1038/s41418-023-01190-5 · Cited by 59
Self-citationCircRNA as an Achilles heel of cancer: characterization, biomarker and therapeutic modalities
Zhang, J., Luo, Z., Yang, Z. K., Duan, M., Qiu, Z., & Huang, C. (2024) · Journal of Translational Medicine · doi:10.1186/s12967-024-05562-4 · Cited by 58
Izuogu, O. G., Alhasan, A. A., Mellough, C., Collin, J., Gallon, R., Hyslop, J., Mastrorosa, F. K., Ehrmann, I. E., Lako, M., Elliott, D. J., et al. (2018) · BMC Genomics · doi:10.1186/s12864-018-4660-7 · Cited by 55
“CircRNA biogenesis can be promoted by intronic homology [5, 8, 9], and knock-down of the dsRNA editing enzyme ADAR1 [10, 11], or the RNA helicase DHX9 which can interact with ADAR1 [12], leads to upregulation of circRNA expression.”
BackgroundMolecular functions and specific roles of circRNAs in the cardiovascular system
Holdt, L. M., Kohlmaier, A., & Teupser, D. (2018) · Non-coding RNA Research · doi:10.1016/j.ncrna.2018.05.002 · Cited by 55
“A first possible explanation for competition between mRNA formation and circRNA formation concerns the accessibility of splice sites as a result of competition between different flanking introns to pair with each other in the pre-mRNA [32] (Fig.”
BackgroundMethodInfluentialPre-mRNA structures forming circular RNAs
Welden, J. R., & Stamm, S. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.194410 · Cited by 56
Identification of the long, edited dsRNAome of LPS-stimulated immune cellsPreprint
Blango, M. G., & Bass, B. (2016) · Genome Research · doi:10.1101/gr.203992.116 · Cited by 56
“For example, circularization of exons to create circular RNAs (circRNAs) is promoted by complementary Alu repeats in flanking introns (Dubin et al. 1995; Liang and Wilusz 2014; Zhang et al. 2014; Ivanov et al. 2015).”
BackgroundCircular RNA: A novel potential biomarker for skin diseases
Wu, X., Xiao, Y., Ma, J., & Wang, A. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.104841 · Cited by 55
Research progress on circular RNA vaccines
Bai, Y., Liu, D., He, Q., Liu, J., Mao, Q., & Liang, Z. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1091797 · Cited by 61
Evaluation of the inclusion of circular RNAs in mRNA profiling in forensic body fluid identification
Zhang, Y., Liu, B., Shao, C., Xu, H., Xue, A., Zhao, Z., Shen, Y., Tang, Q., & Xie, J. (2017) · International Journal of Legal Medicine · doi:10.1007/s00414-017-1690-7 · Cited by 55
“In fact, different expression levels of circRNAs from a single gene were observed in previous reports [19, 23].”
MethodSelf-citationLv, T., Miao, Y., Jin, K., Han, S., Xu, T., Qiu, Z., & Zhang, X. (2018) · Cancer Medicine · doi:10.1002/cam4.1613 · Cited by 56
Self-citationTargeting Non-coding RNA in Vascular Biology and Disease
Hung, J., Miscianinov, V., Sluimer, J. C., Newby, D. E., & Baker, A. H. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01655 · Cited by 57
Current status and potential role of circular RNAs in neurological disorders
Lu, S., Yang, X. F., Wang, C., Chen, S., Lu, S., Yan, W., Xiong, K., Liu, F., & Yan, J. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14724 · Cited by 57
Han, C., Wang, S., Wang, H., & Zhang, J. (2020) · Cancer Biotherapy and Radiopharmaceuticals · doi:10.1089/cbr.2019.3492 · Cited by 55
“10 They have been found to be involved in regulating various physiological and pathological processes in human cancers.”
Self-citationChao, F., Song, Z., Wang, S., Ma, Z., Zhuo, Z., Meng, T., Xu, G., & Chen, G. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.360 · Cited by 54
Circular RNA in disease: Basic properties and biomedical relevance
Chen, X., Zhou, M., Yant, L. J., & Huang, C. (2022) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1723 · Cited by 53
“The competition between those inverted repeated ALU pairs can lead to diverse alternative circularization forms, resulting in multiple circRNA isoforms produced from a single gene (Zhang et al., 2014).”
BackgroundcircMbl Functions in cis and in trans to Regulate Gene Expression With Impacts on Physiology
Pamudurti, N. R., Patop, I. L., Krishnamoorthy, A., Bartok, O., Maya, R., Lerner, N., Ashwal-Fluss, R., Konakondla, J. V. V., Beatus, T., & Kadener, S. (2021) · Cell Reports · doi:10.1016/j.celrep.2022.110740 · Cited by 54
“…biosynthesis is promoted by the presence of complementary sequences in flanking introns and/or by specific splicing factors (Aktas et al., 2017; Ashwal-Fluss et al., 2014; Conn et al., 2015; Errichelli et al., 2017; Ivanov et al., 2015; Knupp et al., 2021; Kramer et al., 2015; Zhang et al., 2014).”
Circ-UBR5: An exonic circular RNA and novel small nuclear RNA involved in RNA splicing
Qin, M., Wei, G., & Sun, X. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.06.112 · Cited by 54
Jiang, F., & Shen, X. (2019) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-019-0178-5 · Cited by 54
Genome-wide identification and functional analysis of circRNAs in Zea mays
Tang, B., Hao, Z., Zhu, Y., Zhang, H., & Li, G. (2018) · PLoS ONE · doi:10.1371/journal.pone.0202375 · Cited by 54
Rapid Development of Targeting circRNAs in Cardiovascular Diseases
Zhang, C., Huo, S. T., Wu, Z., Chen, L., Wen, C., Chen, H., Du, W. W., Wu, N., Guan, D., Lian, S., et al. (2020) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2020.06.022 · Cited by 56
“The inchoate back-splicing mechanism depends on complementary intron matches, which exist widely in the exonic circRNA formation process.(5) In 2003, twomodels of exonic circRNA formation were proposed: “lariat-driven circularization,” and “intron pairing-driven circularization.”
BackgroundSelf-citationRegulation of microRNAs function by circular RNAs in human cancer
Han, C., Seebacher, N. A., Hornicek, F. J., Kan, Q., & Duan, Z. (2017) · Oncotarget · doi:10.18632/oncotarget.19930 · Cited by 55
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“1.0) [10]; Then, back-spliced 92 ordering reads were extracted for circRNA prediction using CIRCexplorer [11].”
InfluentialCircular RNA in Lung Cancer Research: Biogenesis, Functions, and Roles
Zhang, C., Ma, L., Niu, Y., Wang, Z., Xu, X., Li, Y., & Yu, Y. (2020) · International Journal of Biological Sciences · doi:10.7150/ijbs.39212 · Cited by 53
Tian, T., Zhao, Y., Zheng, J., Jin, S., Liu, Z., & Wang, T. (2021) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2021.06.017 · Cited by 53
“The upstream 3¿ splice donor (splice acceptor) site is covalently joined with a downstream 5¿ splice site (splice donor).(69,70) Alternatively, the retention of the introns flanking the exon results in the formation of EIciRNAs, whereas the removal of these introns results in the formation of ecircRNAs.”
BackgroundCircular RNAs in cardiovascular diseases
Mei, X., & Chen, S. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107991 · Cited by 55
Circular RNAs Acting as miRNAs’ Sponges and Their Roles in Stem Cells
Xiao, J., Joseph, S., Xia, M., Teng, F., Chen, X., Huang, R., Zhai, L., & Deng, W. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11102909 · Cited by 55
CirRNAPL: A web server for the identification of circRNA based on extreme learning machine
Niu, M., Zhang, J., Li, Y., Wang, C., Liu, Z.-Q., Ding, H., Zou, Q., & Ma, Q. (2020) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2020.03.028 · Cited by 53
“used non-polyadenylation and rnaser-treated RNA-seq data from H9 human embryonic stem cells to predict reverse splicing junctions, and they systematically characterized circRNA using the newly developed pipeline CIRCexplorer [27].”
MethodHost-derived circular RNAs display proviral activities in Hepatitis C virus-infected cells
Chen, T., Talló-Parra, M., Cao, Q. M., Kadener, S., Böttcher, R., Pérez‐Vilaró, G., Boonchuen, P., Somboonwiwat, K., Díez, J., & Sarnow, P. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008346 · Cited by 54
The biogenesis, function and clinical significance of circular RNAs in breast cancer
Zeng, Y., Zou, Y., Gao, G., Zheng, S., Song, W. C., Xie, X., & Tang, H. (2021) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2020.0485 · Cited by 52
Hafez, A. K., Zimmerman, A. J., Papageorgiou, G., Chandrasekaran, J., Amoah, S. K., Lin, R., Lozano, E., Pierotti, C. E., Dell’Orco, M., Hartley, B. J., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2021.110282 · Cited by 52
Identification of circRNAs linked to Alzheimer's disease and related dementias
Puri, S., Hu, J., Sun, Z., Lin, M., Stein, T. D., Farrer, L. A., Wolozin, B. L., & Zhang, X. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.12960 · Cited by 54
“(2) The percentage of mapped and unmapped reads was evaluated.”
BackgroundSelf-citationCircles in the heart and cardiovascular system
Lim, T. B., Lavenniah, A., & Foo, R. (2019) · Cardiovascular Research · doi:10.1093/cvr/cvz227 · Cited by 54
The emerging roles of exosomal circRNAs in diseases
Guo, X., Tan, W., & Wang, C. (2020) · Clinical & Translational Oncology · doi:10.1007/s12094-020-02485-6 · Cited by 51
Fang, X., Li, M., Yu, T., Liu, G., & Wang, J. (2020) · Genes & Diseases · doi:10.1016/j.gendis.2020.06.011 · Cited by 52
“circRNAs are generated from pre-mRNA via back-splicing post-transcriptionally, which results in the circularization of exons and pairing of flanking introns, forming a lariat structure.(41,42) The distinct m6A distribution pattern in mRNA and circRNAs suggests that RNAs are also N6-methylated posttranscriptionally.”
BackgroundCircular RNAs in cell differentiation and development
Timoteo, G. D., Rossi, F., & Bozzoni, I. (2020) · Development · doi:10.1242/dev.182725 · Cited by 52
“In some cases, they were shown to be sufficient to trigger back splicing (Zhang et al., 2014).”
BackgroundInvestigating the Potential Roles of SINEs in the Human Genome
Zhang, X.-O., Pratt, H., & Weng, Z. (2021) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-111620-100736 · Cited by 55
“…in the human genome (59, 83, 129), and large-scale analyses show that back-spliced exons are generally flanked by long introns, wherein inverted complementary Alu elements can form IR Alu s to bring distal splice sites into close proximity and facilitate back-splicing (59, 76, 129) ( Figure 3 a ).”
Self-citationLiu, B., Liu, N., Zhu, X., Yang, L., Ye, B., Li, H., Zhu, P., Lu, T., Tian, Y., & Fan, Z. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00680-1 · Cited by 49
“CircRNAs originate from precursor mRNAs (pre-mmRNAs) and may comprise exons, introns, or exon–introns.(9) CircRNAs harbor a long half-life and are resistant to exonuclease degradation.”
BackgroundSelf-citationAn interaction between eIF4A3 and eIF3g drives the internal initiation of translation
Chang, J., Shin, M.-K., Park, J., Hwang, H. J., Locker, N., Ahn, J., Kim, D., Baek, D., Park, Y., Lee, Y., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad763 · Cited by 52
“Because circRNAs lack a 5 (cid:2) -cap structure ( 11 ,12 ), internal initiation of translation is the only way to synthesize proteins.”
BackgroundCircular RNA as a source of neoantigens for cancer vaccines
Ren, Y., Manoharan, T., Liu, B., Cheng, C. Z. M., Siew, B. E., Cheong, W., Lee, K. Y., Tan, I. J.-W., Lieske, B., Tan, K., et al. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2023-008402 · Cited by 53
“7 8–11 The process of back splicing generates new exon−exon junctions and translational frames in the circularized RNA, which could potentially give rise to unique cancer-specific peptides or proteins.”
BackgroundCircular RNA CircVAPA Regulates Breast Cancer Cell Migration and Invasion Via Sponging miR-130a-5p
Zhou, S., Chen, W., Yang, S., Li, J., Zhang, J., Zhang, H.-D., Zhong, S., & Tang, J. (2020) · Epigenomics · doi:10.2217/epi-2019-0124 · Cited by 51
Circular RNA in Diseased Heart
Wang, Y., & Liu, B. (2020) · Cells · doi:10.3390/cells9051240 · Cited by 51
Angiogenesis-related non-coding RNAs and gastrointestinal cancer
Razavi, Z. S., Asgarpour, K., Mahjoubin‐Tehran, M., Rasouli, S., Khan, H. Z., Shahrzad, M. K., Hamblin, M. R., & Mirzaei, H. (2021) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2021.04.002 · Cited by 51
“The spliceosome plays a key role in circRNA biogenesis, relying on trans-acting factors and cis-regulatory elements.(277) In one study by Zhang et al.”
BackgroundCircRNA circFOXK2 facilitates oncogenesis in breast cancer via IGF2BP3/miR-370 axis
Zhang, W., Liu, H., Jiang, J., Yang, Y., Wang, W., & Jia, Z. (2021) · Aging · doi:10.18632/aging.203347 · Cited by 52
“Unaligned reads were used for subsequent circRNA analysis using CIRCexplorer2 [58] and Find_circ [59].”
MethodVea, À., Llorente‐Cortés, V., & de Gonzalo‐Calvo, D. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1426-1_10 · Cited by 51
Research progress on plant noncoding RNAs in response to low-temperature stress
Huo, C., Zhang, B., & Wang, R. (2021) · Plant Signaling & Behavior · doi:10.1080/15592324.2021.2004035 · Cited by 51
“CircRNAs were not discovered through specific RNA sequencing methods until recent years.(103)”
MethodCircular RNAs: Functions and Prospects in Glioma
Zheng, H., Hu, S., Liu, Z., Wei-xin, S., Zhao, Y., & Li, M. (2018) · Journal of Molecular Neuroscience · doi:10.1007/s12031-018-1211-2 · Cited by 49
Sun, Y., Zhang, H., Fan, M., He, Y., & Guo, P. (2020) · Archives of Virology · doi:10.1007/s00705-020-04589-4 · Cited by 50
Exploring the regulatory roles of circular RNAs in Alzheimer’s disease
Zhang, Y., Zhao, Y., Liu, Y., Wang, M., Yu, W., & Zhang, L. (2020) · Translational Neurodegeneration · doi:10.1186/s40035-020-00216-z · Cited by 47
“CircRNAs are generally expressed in cell type-specific and tissue-specific manners [7, 9].”
BackgroundSelf-citationLi, P., Yu, H., Zhang, G., Kang, L., Qin, B., Cao, Y. Q., Luo, J., Chen, X., Wang, Y., Qin, M., et al. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.10.13 · Cited by 49
“34 Research suggested a different set of rules may govern m 6 A biogenesis in circR-NAs compared with mRNAs.”
An in vivo strategy for knockdown of circular RNAs
Pamudurti, N. R., Patop, I. L., Krishnamoorthy, A., Ashwal-Fluss, R., Bartok, O., & Kadener, S. (2020) · Cell Discovery · doi:10.1038/s41421-020-0182-y · Cited by 49
Reduction of A-to-I RNA editing in the failing human heart regulates formation of circular RNAs
Kokot, K. E., Kneuer, J. M., John, D., Rebs, S., Möbius-Winkler, M. N., Erbe, S., Müller, M., Andritschke, M., Gaul, S., Sheikh, B. N., et al. (2022) · Basic Research in Cardiology · doi:10.1007/s00395-022-00940-9 · Cited by 49
CircRNA: Functions, Applications and Prospects
Xu, F., Xiao, Q., Du, W. W., Wang, S., & Yang, B. B. (2024) · Biomolecules · doi:10.3390/biom14121503 · Cited by 49
SGANRDA: semi-supervised generative adversarial networks for predicting circRNA–disease associations
Wang, L., Yan, X., You, Z., Zhou, X., Li, H., & Huang, Y. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab028 · Cited by 48
Inverted Alu repeats: friends or foes in the human transcriptome
Lee, K., Ku, J., Ku, D., & Kim, Y. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01177-3 · Cited by 48
“Nonetheless, due to their circular structure, circRNAs are highly stable, and human cells express tens of thousands of cir-cRNAs 56 – 58 .”
BackgroundGaffo, E., Bonizzato, A., Kronnie, G. T., & Bortoluzzi, S. (2017) · Non-Coding RNA · doi:10.3390/ncrna3010008 · Cited by 48
“Recently, several computational methods for the detection of back-splice events from RNA-seq data have been developed, such as find_circ [10], CIRCexplorer [14], circRNA_finder [15], testrealign [16], CIRI [17], KNIFE [18], UROBORUS [19], NCLscan [20], PTESFinder [21], and Acfs [22].”
MethodInfluentialCircView: a visualization and exploration tool for circular RNAs
Feng, J. Q., Xiang, Y., Xia, S., Liu, H., Wang, J., Ozguc, F. M., Lei, L., Kong, R., Diao, L., He, C., et al. (2017) · Briefings in Bioinformatics · doi:10.1093/bib/bbx070 · Cited by 48
Deep learning of the back-splicing code for circular RNA formation
Wang, J., & Wang, L. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz382 · Cited by 48
Redefining transcriptional regulation of the APOE gene and its association with Alzheimer’s disease
Lee, E.-G., Tulloch, J., Chen, S., Leong, L., Saxton, A. D., Kraemer, B. C., Darvas, M., Keene, C. D., Shutes‐David, A., Todd, K. W., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0227667 · Cited by 49
Emerging roles of circular RNAs in innate immunity
Li, I., & Chen, Y. G. (2020) · Current Opinion in Immunology · doi:10.1016/j.coi.2020.10.010 · Cited by 49
Circular and long non-coding RNAs and their role in ophthalmologic diseases
Wawrzyniak, O., Zarębska, Ż., Rolle, K., & Gotz‐Więckowska, A. (2018) · Acta Biochimica Polonica · doi:10.18388/abp.2018_2639 · Cited by 47
Deng, N., Lei, D., Huang, J., Yang, Z., Fan, C., & Wang, S. (2019) · Pregnancy Hypertension · doi:10.1016/j.preghy.2019.06.009 · Cited by 47
Circular RNA circGLIS3 promotes bladder cancer proliferation via the miR-1273f/SKP1/Cyclin D1 axis
Wu, S., Yang, J., Xu, H., Wang, X., Zhang, R., Lu, W., Yang, J., Li, X., Chen, S., Zou, Y., et al. (2021) · Cell Biology and Toxicology · doi:10.1007/s10565-021-09591-3 · Cited by 47
Novel insights into the interaction between N6-methyladenosine modification and circular RNA
Xu, T., He, B., Sun, H., Xiong, M., Nie, J., Wang, S., & Pan, Y. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.01.007 · Cited by 48
Yu, L., Zhu, H., Wang, Z., Huang, J., Zhu, Y., Fan, G., Wang, Y., Chen, X., & Zhou, G. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01624-7 · Cited by 49
“Mechanistically, it was reported that specific repeat sequences in genome, such as Alu elements, could promote circularization in cells [41, 42], so the differences in specific genomic location may partially contribute to the elevated circFIRRE level, but the specific mechanism in transcription imbalance remains to be…”
BackgroundEndogenous Multiple Exon Skipping and Back-Splicing at the DMD Mutation Hotspot
Suzuki, H., Aoki, Y., Kameyama, T., SAITO, T. K., Masuda, S., Tanihata, J., Nagata, T., Mayeda, A., Takeda, S., & Tsukahara, T. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17101722 · Cited by 47
“Therefore, the current model proposes that back-splicing can be caused at the proximal ends of the interacting introns of a pre-mRNA [18,19].”
BackgroundInfluentialCircular PVT1: an oncogenic non-coding RNA with emerging clinical importance
Adhikary, J., Chakraborty, S., Dalal, S., Basu, S., Dey, A., & Ghosh, A. (2019) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2019-205891 · Cited by 47
The emerging role of circular RNAs in breast cancer
Zhou, S., Chen, W., Yang, S., Xu, Z., Hu, J.-H., Zhang, H.-D., Zhong, S., & Tang, J. (2019) · Bioscience Reports · doi:10.1042/bsr20190621 · Cited by 47
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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