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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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MethodSelf-citationBiosynthesis of Circular RNA ciRS-7/CDR1as Is Mediated by Mammalian-wide Interspersed Repeats
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“Moreover, Alu elements, complementary repeated sequences in the flanking introns, may also be a common driver of back-splicing [6,7,26,27,28,29].”
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SARS‐CoV‐2, SARS‐CoV, and MERS‐CoV encode circular RNAs of spliceosome‐independent origin
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“Repetitive intronic elements, including the primate‐specific Alu elements, enables intramolecular RNA looping, thereby promoting cellular circRNA biogenesis in cis.(35,42,43) As for RNA recombination in CoVs, the prevailing model predicts that discontinuous RNA synthesis is mediated by homologous motifs called transcr…”
BackgroundCircular RNA Profiling Identifies Novel circPPARA that Promotes Intramuscular Fat Deposition in Pigs
Li, B., He, Y., Wu, W., Tan, X., Wang, Z., Irwin, D. M., Wang, Z., & Zhang, S. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c07358 · Cited by 47
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“S8), in line with reports that flanking introns facilitate circularization (Jeck et al. 2013; Ivanov et al. 2014; Liang and Wilusz 2014; Zhang et al. 2014).”
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Self-citationExpression profiles of circular RNAs in sheep skeletal muscle
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Self-citationLux, S., & Bullinger, L. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1426-1_17 · Cited by 46
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“Alternative circularization coupled with alternative splicing can produce a variety of additional circRNAs from one gene, making such molecules have enriched sequences in conserved nucleotides (X. O. Zhang et al., 2014).”
BackgroundSelf-citationA Comprehensive Map of Intron Branchpoints and Lariat RNAs in Plants
Zhang, X., Zhang, Y., Wang, T., Li, Z., Cheng, J., Ge, H., Tang, Q., Chen, K., Liu, L., Lu, C., et al. (2019) · The Plant Cell · doi:10.1105/tpc.18.00711 · Cited by 46
Self-citationEmerging roles of circular RNAs in gastric cancer metastasis and drug resistance
Wang, X., Zhang, J., Cao, G., Hua, J., Shan, G., & Lin, W. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02432-z · Cited by 46
Roles of Long Noncoding RNAs and Circular RNAs in TranslationPreprint
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“In addition to canonical splicing factors and signals, backsplicing requires specific intronic sequences that mediate circularization, bringing the downstream donor and upstream acceptor sites into close proximity (Ashwal-Fluss et al. 2014; Zhang et al. 2014).”
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“Since the flanking intronic complementary sequences, particularly ALU repeat elements, have the ability to drive exon cyclization [12], we analyzed the parental SMC4 gene and found complementary ALU sequence, which might serve as a possible mechanism for hsa_circ_0067842 formation (Additional file…”
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Self-citationZhuo, C., Zhou, C., Zhu, J., Hou, W., Jiang, D., Tian, H., Wang, L., & Jia, F. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.268969 · Cited by 48
“For the back-splicing of exons, intron-pairing of repeated sequences, including Arthrobacter luteus (Alu) elements which form highly stable base pairs, is a catalyst to drive and enhance circularization, also referred to as direct back-splicing of exons (Jeck et al., 2013; Liang and Wilusz, 2014; Zhang et al., 2014; I…”
BackgroundDiagnostic and Prognostic Value of Circulating CircRNAs in Cancer
Wang, M., Xie, F., Lin, J., Zhao, Y., Zhang, Q., Liao, Z., & Wei, P. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.649383 · Cited by 47
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Emerging roles of circular RNAs in liver cancer
Louis, C., Leclerc, D., & Coulouarn, C. (2021) · JHEP Reports · doi:10.1016/j.jhepr.2021.100413 · Cited by 46
“intronic regions flanking circRNA sequences.(21,22) Thus, one might anticipate that targeting these complementary sequences on pre-messenger RNAs using ASOs may block circRNA biogenesis by preventing the interaction of back-spliced regions.”
BackgroundOptimal design of synthetic circular RNAs
Choi, S.-W., & Nam, J. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01251-w · Cited by 45
“However, some exons are more preferentially processed by circRNAs than others, and the more back-splicing that occurs on an exon, the more exon skipping occurs during forward splicing 24,69 .”
BackgroundInfluentialcircCTIC1 promotes the self-renewal of colon TICs through BPTF-dependent c-Myc expression
Zhan, W., Liao, X., Wang, Y., Li, L., Li, J., Chen, Z., Tian, T., & He, J. (2018) · Carcinogenesis · doi:10.1093/carcin/bgy144 · Cited by 44
CircCDYL inhibits the expression of C-MYC to suppress cell growth and migration in bladder cancer
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“These data show that the distribution of the Alu sites that promote the circulation of a fragment that contains more elements than a single intron has a greater role in the circularization process than the number of Alu sites [66,67].”
BackgroundMa, Y., Zheng, L., Gao, Y., Zhang, W., Zhang, Q., & Xu, Y. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.709512 · Cited by 47
The circRNA-miRNA/RBP regulatory network in myocardial infarction
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“There are three types of circRNAs which are produced via different mechanisms, namely 1) exonic circRNAs (ecircRNAs or ecRNAs) (Zhang et al., 2014); 2) exon-intron circRNAs (EIciRNAs) (Li et al.”
BackgroundSelf-citationYang, X., Ma, X., Mei, C., & Zan, L. (2022) · BMC Genomics · doi:10.1186/s12864-022-08911-z · Cited by 44
“Identification of circRNA: CIRCExplorer2 [63, 64] and CIRI [65] were used to denovo assemble the mapped reads to circular RNAs first.”
MethodThe Circular RNA Profiles of Colorectal Tumor Metastatic Cells
Jiang, W., Zhang, X., Chu, Q., Lu, S., Zhou, L., Lu, X., Liu, C., Mao, L., Ye, C., Timko, M. P., et al. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00034 · Cited by 43
“…canonical spliceosomal machinery (Starke et al., 2015; Chen, 2016) and is dependent upon various cis-regulatory elements such as repetitive complementary sequences (Liang and Wilusz, 2014; Zhang et al., 2014) and trans-acting factors such as Mbl (Ashwal-Fluss et al., 2014), QKI (Conn et al., 2015).”
BackgroundSelf-citationThe Relationship of Circular RNAs With Ovarian Endometriosis
Xu, X., Jia, S., Dai, Y., Zhang, J., Li, X., Shi, J., Leng, J., & Lang, J. (2018) · Reproductive Sciences · doi:10.1177/1933719118759439 · Cited by 40
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“CircRNAs were then predicted using CIRCEXPLORER with default options (Zhang et al., 2014).”
MethodSelf-citationAccentuating CircRNA-miRNA-Transcription Factors Axis: A Conundrum in Cancer Research
Singh, D., Kesharwani, P., Alhakamy, N. A., & Siddique, H. R. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.784801 · Cited by 43
“These cis-acting elements undergo base pairing resulting in the formation of hairpin structure and put forward the 5′splice site present downstream and 3′ splice site present upstream close enough to enable the easy circularisation of circRNAs (Zhang et al., 2014; Chen, 2016; Wu et al., 2019).”
BackgroundCircular RNAs in Cardiovascular Diseases: Regulation and Therapeutic Applications
Wang, L., Xu, G.-E., Spanos, M., Li, G., Lei, Z., Sluijter, J. P. G., & Xiao, J. (2023) · Research · doi:10.34133/research.0038 · Cited by 42
Approaches and challenges in genome-wide circular RNA identification and quantification
Ma, X.-K., Zhai, S.-N., & Yang, L. C. (2023) · Trends in Genetics · doi:10.1016/j.tig.2023.09.006 · Cited by 41
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Self-citationCircular RNA discovery with emerging sequencing and deep learning technologies
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“CircRNA biogenesis is intricately regulated by factors, such as the spliceosome 17 , RBPs 19,49 and flanking intronic complementary sequences 101,102 .”
Comprehensive analysis of circRNA expression profiles in humans by RAISE
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“Previous studies indicated that the expression of circular RNA is related to the genomic origin of the linear transcripts (5,23,24) and that circular RNAs regulate the transcription of host mRNAs (9,50,51).”
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Identification and characterization of circRNAs in Pyrus betulifolia Bunge under drought stress
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Self-citationResearch progress on circularRNAs in pancreatic cancer: emerging but promising
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“Different from lariat-driven circularization, intron complementary pairing-driven circularization is induced by the reverse complementary sequence pairing on the flanking introns to approximate the spatial distance between the splicing sites.(47) Interestingly, most of the flanking intron complementary sequences that…”
BackgroundThe emerging roles of circular RNAs in ovarian cancer
Yang, X., Mei, J., Wang, H., Gu, D., Ding, J., & Liu, C. (2020) · Cancer Cell International · doi:10.1186/s12935-020-01367-9 · Cited by 43
“Intron pairing-driven circularization, a direct back-splicing mechanism, is a process that induces cyclization with the aid of reverse complementary sequences and thus generated an EIciRNA or ecircRNA via intron removal [21] (Fig.”
Self-citationThe Potential Regulatory Roles of Circular RNAs in Tumor Immunology and Immunotherapy
Fang, Z., Jiang, C., & Li, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.617583 · Cited by 42
“This process could be mediated by base pairing between inverted repeat elements or RNA-binding proteins (RBPs), such as QKI and FUS (25, 26).”
BackgroundMa, X.-K., Xue, W., Chen, L., & Yang, L. C. (2021) · Methods · doi:10.1016/j.ymeth.2021.02.008 · Cited by 44
“…junction (BSJ) sites [26 – 28, 30, 31], hundreds of Almost all these computational pipelines, such as find_circ [45], CIRI [46] and CIRCexplorer (version one) [39], were set to identify deep sequencing fragments specifically aligned to BSJ sites for circRNA annotation in early days (Table 1).”
MethodSelf-citationThe Emerging Role of Circular RNAs in Alzheimer’s Disease and Parkinson’s Disease
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Circular RNA circHIPK3 promotes breast cancer progression via sponging MiR-326
Luo, N., Liu, S., Li, X., Hu, Y., & Zhang, K. (2021) · Cell Cycle · doi:10.1080/15384101.2021.1939476 · Cited by 43
“Furthermore, it is well-known that the formation of circRNAs is commonly attributed to the sequences which can be capable of pairing to form RNA duplexes and significantly enhancing backsplicing [28].”
BackgroundInnovative in Silico Approaches for Characterization of Genes and Proteins
Bhat, G. R., Sethi, I., Rah, B., Kumar, R., & Afroze, D. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.865182 · Cited by 47
CircRNAs in tumor immunity and immunotherapy: Perspectives from innate and adaptive immunity
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Circular RNAs as a New Field in Gene Regulation and their Implications in Translational Research
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“Chen and colleagues at Institute of Biophysics, Chinese Academy of Sciences (CAS) characterized the lncRNA ADINR as a novel regulator during adipogenesis.”
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“CircRNA reads were divided by the total number of mapped reads in each sample to obtain RPM (mapped back-splice junction reads per million mapped reads) values [30].”
Identification of tomato circular RNAs responsive to Phytophthora infestans
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Circular RNAs: Promising biomarkers for cancer diagnosis and prognosis
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Evolutionary dynamics of circular RNAs in primates
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CircRNA in ocular neovascular diseases: Fundamental mechanism and clinical potential
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Self-citationHatzimanolis, O., Sykes, A. M., & Cristino, A. S. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-02925-1 · Cited by 44
“…can also elucidate their functional roles, via strategies such as expression vector construction with circRNA-producing exons and their fl anking introns [46, 70, 100, 205, 206] or transfecting cells with synthetic circRNAs generated through in vitro transcription and circularization [207 – 209].”
LncRNAs and CircRNAs from the same gene: Masterpieces of RNA splicing
Huang, M., Zhu, T., Li, L., Xie, P., Li, X., Zhou, H., & Liu, Z. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.11.034 · Cited by 40
Research progress of circular RNAs in lung cancer
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“CiRNA biogenesis, which occurs via a lariat-derived mechanism, depends mainly on a 7-nt GU-rich element near the 5ʹ splice site and an 11-nt C-rich element near the branch point site.(15,20) In addition, John et al.”
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The roles of circRNAs in cancers: Perspectives from molecular functions
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Self-citationCircRNA: An emerging star in the progression of glioma
Peng, D., Luo, L., Zhang, X., Wei, C., Zhang, Z., & Han, L. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113150 · Cited by 38
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“They are produced via the reverse splicing of a precursor mRNA [57] (Figure 4).”
BackgroundGenome-wide analysis of circular RNAs in prenatal and postnatal muscle of sheep
Li, C., Li, X., Yao, Y., Ma, Q., Ni, W., Zhang, X., Cao, Y., Hazi, W., Wang, D., Quan, R., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.21835 · Cited by 39
Self-citationLncRNAs regulating stemness in aging
Sousa‐Franco, A., Rebelo, K., da Rocha, S. T., & de Jesus, B. B. (2018) · Aging Cell · doi:10.1111/acel.12870 · Cited by 38
Global Increase in Circular RNA Levels in Myotonic Dystrophy
Czubak, K., Taylor, K., Piasecka, A., Sobczak, K., Kozlowska, K., Philips, A., Sedehizadeh, S., Brook, J. D., Wojciechowska, M., & Kozłowski, P. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00649 · Cited by 41
A universal approach to investigate circRNA protein coding function
Mo, D., Li, X., Raabe, C. A., Cui, D., Vollmar, J.-F., Rozhdestvensky, T. S., Skryabin, B. V., & Brosius, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-48224-y · Cited by 38
Liu, X., Hu, Z., Zhou, J., Tian, C., Tian, G., He, M., Gao, L., Chen, L., Li, T., Peng, H., et al. (2019) · RNA Biology · doi:10.1080/15476286.2019.1669391 · Cited by 37
Self-citationCoding and Non-Coding RNA Abnormalities in Bipolar Disorder
Luykx, J. J., Giuliani, F., Giuliani, G., & Veldink, J. H. (2019) · Genes · doi:10.3390/genes10110946 · Cited by 40
Clinical and functional significance of circular RNAs in cytogenetically normal AML
Papaioannou, D., Volinia, S., Nicolet, D., Świerniak, M., Petri, A., Mrózek, K., Bill, M., Pepe, F., Walker, C. J., Walker, A. E., et al. (2020) · Blood Advances · doi:10.1182/bloodadvances.2019000568 · Cited by 39
Critical function of circular RNAs in lung cancer
Drulă, R., Braicu, C., Haranguș, A., Nabavi, S. M., Trif, M., Slabý, O., Ionescu, C., Irimie, A., & Berindan‐Neagoe, I. (2020) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1592 · Cited by 38
“The length and strength of these repeat circularization considerably (Zhang et al., 2014).”
BackgroundZhang, W., Qi, L., Chen, R., He, J., Liu, Z., Wang, W., Tu, C., & Li, Z. (2021) · Arthritis Research & Therapy · doi:10.1186/s13075-021-02420-2 · Cited by 39
“Besides, RNA paring can happen in either the repetitive or the non-repetitive complementary sequences [33].”
BackgroundCircular RNAs in the cardiovascular system
Gomes, C. P. C., Salgado‐Somoza, A., Creemers, E. E., Dieterich, C., Luštrek, M., & Devaux, Y. (2018) · Non-coding RNA Research · doi:10.1016/j.ncrna.2018.02.002 · Cited by 39
“It is however known that many circRNAs in mammals are processed from exons with long flanking introns, containing reverse complementary sequences [16,17].”
BackgroundZheng, Y., Hui, T., Chang, Y., Sun, J., Guo, D., Guo, S., Guo, S., Li, B., Wang, Z., & Bai, W. (2020) · Scientific Reports · doi:10.1038/s41598-019-57404-9 · Cited by 38
Ikeda, Y., Morikawa, S., Nakashima, M., Yoshikawa, S., Taniguchi, K., Sawamura, H., Suga, N., Tsuji, A., & Matsuda, S. (2023) · Non-Coding RNA · doi:10.3390/ncrna9020023 · Cited by 41
“CircRNAs are closed loop structures [2], in which the 3′ and 5′ ends are covalently joined [3].”
BackgroundDegradation of circular RNA by the ribonuclease DIS3
Tao, X., Zhai, S.-N., Liu, C., Huang, Y., Wei, J., Guo, Y., Liu, X.-Q., Li, X., Yang, L. C., & Chen, L.-L. (2025) · Molecular Cell · doi:10.1016/j.molcel.2025.01.012 · Cited by 40
Self-citationCircular exonic RNAs: When RNA structure meets topology
Pervouchine, D. D. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.05.002 · Cited by 38
Zeng, N., Wang, T., Chen, M., Yuan, Z., Qin, J., Wu, Y., Gao, L., Shen, Y., Chen, L., & Wen, F. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14436 · Cited by 38
Self-citationHumphreys, D. T., Fossat, N., Demuth, M., Tam, P., & Ho, J. W. K. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz718 · Cited by 38
“For example, at this point in time, the websites for circExplorer (16) and DCC (35) recommends the –chimSegmentMin to be 10 and 20 respectively.”
BackgroundMethodA combined computational pipeline to detect circular RNAs in human cancer cells under hypoxic stress
Liddo, A. D., Machado, C. D. O. F., Fischer, S. E., Ebersberger, S., Heumüller, A. W., Weigand, J. E., Müller-McNicoll, M., & Zarnack, K. (2019) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjz094 · Cited by 37
“While the introns flanking the back-splice sites were generally longer than average annotated introns (Figure 2C; Zhang et al., 2014), the back-spliced exons were similar in length compared to all exons from PCGs (median 125–127 bp vs. 143 bp for all annotated exons; Supplementary Figure S3D).”
InfluentialGuo, W., Mu, K., Zhang, B., Sun, C., Zhao, L., Li, H., Dong, Z., & Cui, Q. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-02882-3 · Cited by 38
CircRNAs and Fusion-circRNAs in cancer: New players in an old game
Visci, G., Tolomeo, D., Agostini, A., Traversa, D., Macchia, G., & Storlazzi, C. T. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2020.109747 · Cited by 38
Chen, Z., He, L., Zhao, L., Zhang, G., Wang, Z., Zhu, P., & Liu, B. (2022) · Advanced Science · doi:10.1002/advs.202105160 · Cited by 37
Knockout of circRNAs by base editing back-splice sites of circularized exons
Gao, X., Ma, X.-K., Li, X., Li, G., Liu, C., Zhang, J., Wang, Y., Wei, J., Chen, J., Chen, L., et al. (2022) · Genome biology · doi:10.1186/s13059-021-02563-0 · Cited by 38
“RNase R treatment was performed as previously described [16] for circRNA enrichment.”
BackgroundMethodInfluentialSelf-citationAlternative splicing: An efficient regulatory approach towards plant developmental plasticity
Muhammad, S., Xu, X., Zhou, W., & Wu, L. (2022) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1758 · Cited by 39
“Another mechanism for circRNA formation is the alternative circularization that can generate a variety of circRNAs from a single gene (Zhang et al., 2014).”
BackgroundCircular RNAs in human diseases
Wang, Y., Zhang, J., Yang, Y. S. H., Liu, Z., Sun, S., Li, R. F., Zhu, H., Tian, L., Zheng, J., Li, J., et al. (2024) · MedComm · doi:10.1002/mco2.699 · Cited by 41
Xu, X., Qiu, P., Ren, Z., Han, Y., Jiang, X., Zhu, W., Tan, S., Yang, W., Oyang, L., Luo, X., et al. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02239-4 · Cited by 42
RNA (Epi)genetics in cardiovascular diseases
Elia, L., & Condorelli, G. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.07.012 · Cited by 37
Circular RNAs—one of the enigmas of the brain
Filippenkov, I. B., Kalinichenko, E. O., Limborska, S. A., & Dergunova, L. V. (2016) · Neurogenetics · doi:10.1007/s10048-016-0490-4 · Cited by 37
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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