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Circular RNAs in the Mammalian Brain Are Highly Abundant, Conserved, and Dynamically Expressed
Open accessAbstract
Circular RNAs (circRNAs) are an endogenous class of animal RNAs. Despite their abundance, their function and expression in the nervous system are unknown. Therefore, we sequenced RNA from different brain regions, primary neurons, isolated synapses, as well as during neuronal differentiation. Using these and other available data, we discovered and analyzed thousands of neuronal human and mouse circRNAs. circRNAs were extraordinarily enriched in the mammalian brain, well conserved in sequence, often expressed as circRNAs in both human and mouse, and sometimes even detected in Drosophila brains. circRNAs were overall upregulated during neuronal differentiation, highly enriched in synapses, and often differentially expressed compared to their mRNA isoforms. circRNA expression correlated negatively with expression of the RNA-editing enzyme ADAR1. Knockdown of ADAR1 induced elevated circRNA expression. Together, we provide a circRNA brain expression atlas and evidence for important circRNA functions and values as biomarkers.
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In the citing paper
“Many circRNAs are significantly upregulated at different time points of neuron maturation in vitro.293”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [293]
In the citing paper
“They are highly expressed in the brain from the embryonic stage to adulthood and substantially upregulated during the differentiation and maturation of neurons.293”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [293]
In the citing paper
“CircRNAs maintain specificity and conservatism in the process of dynamic expression and are highly enriched in the mammalian brain, independent of linear transcripts [62].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [62]
In the citing paper
“CiRS-7 is abundantly expressed in the mammalian brain [49,62], where it increases the translation of the miR-7 target mRNA [14,49].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [62]
In the citing paper
“A study by Rybak et al. demonstrated that more than half of 15,849 mouse circRNAs, which are highly abundant, conserved, and dynamically expressed in the brain, are upregulated during the maturation of neurons [62,65].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [62]
In the citing paper
“Compared with other cytoplasmic RNAs, circRNAs seem to be more prone to being localized in synapses and their expression is correlated with neural plasticity, which further supports an important function of circRNAs in synaptic transmission [50,62].”
From Circular RNAs in depression: Biogenesis, function, expression, and therapeutic potential (2021) · cites this paper as [62]
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“Circular RNAs (circRNAs) are highly conserved and covalently stable, and are closed RNA transcripts that are produced by a single pre‐messenger (m)RNA back splicing with potential gene regulation.(4,5) Due to their closed structure, circRNAs are stable and resistant to RNA degradative pathways; circRNAs therefore show…”
BackgroundShen, Y., Zhang, N., Chai, J., Wang, T., Ma, C., Han, L., & Yang, M. (2022) · Cancer Research · doi:10.1158/0008-5472.can-22-1923 · Cited by 102
Emerging functions of the Quaking RNA ‐binding proteins and link to human diseases
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“A recent report showed that varied levels of circRNA expression occur in different brain regions with the olfactory bulb, prefrontal cortex, cerebellum, and hippocampus expressing specific sets of circRNAs.(57) Given the high expression of QKI in several cell types and areas in the brain, it is plausible to speculate…”
BackgroundUsing plasma circRNA_002453 as a novel biomarker in the diagnosis of lupus nephritis
Ouyang, Q., Huang, Q., Jiang, Z., Zhao, J., Shi, G., & Yang, M. (2018) · Molecular Immunology · doi:10.1016/j.molimm.2018.07.029 · Cited by 97
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Circular RNAs in the tumour microenvironment
Ma, Z., Shuai, Y., Gao, X., Wen, X., & Ji, J. (2020) · Molecular Cancer · doi:10.1186/s12943-019-1113-0 · Cited by 96
“Interestingly, circRNAs are expressed in tissue-specific and developmental stage-specific manners [8, 29].”
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circRNA Expression Profiles in Human Bone Marrow Stem Cells Undergoing Osteoblast Differentiation
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RETRACTED: Circular RNA PVT1 promotes metastasis via miR-145 sponging in CRC
Wang, Z., Su, M., Xiang, B., Zhao, K., & Qin, B. (2019) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2019.03.121 · Cited by 96
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“As mentioned previously, circRNAs have been shown to have a time- and tissue-specific expression pattern [20,23,30].”
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Wang, L., Jia, Y., Lu, L., Zhang, Y., Wang, L., Hu, G.-S., Liu, Y.-C., Ding, J., Shen, H., Zhao, F., et al. (2020) · Theranostics · doi:10.7150/thno.45302 · Cited by 95
“Many circRNAs have been found to be dynamically regulated and functional in physiological process of aging [33, 34] and development [16, 35-37].”
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The role of circRNAs in cancers
Zhu, L., He, Y., Hou, J., Chen, X., Zhou, S., Yang, S., Li, J., Zhang, H.-D., Hu, J., Zhong, S., et al. (2017) · Bioscience Reports · doi:10.1042/bsr20170750 · Cited by 95
Li, L., Zhu, Z., Zhao, W., Tao, S., Li, B., Xu, S.-Z., Wang, J., Zhang, M., Wu, J., Leng, R., et al. (2018) · Immunology · doi:10.1111/imm.12940 · Cited by 95
Circular RNAs: a rising star in respiratory diseases
Wang, J., Zhu, M., Pan, J., Chen, C., Xia, S., & Song, Y. (2019) · Respiratory Research · doi:10.1186/s12931-018-0962-1 · Cited by 94
“The silencing of ADAR1 increases the expression of intracellular circRNAs, and the mechanism by which this occurs possibly is associated with the ability of ADAR1 to melt the dsRNA hairpin structure when inverted complementary sequences are present in the flanking introns of circularized exons [29] .”
BackgroundKuo, M., Liu, S. C.-H., Hsu, Y.-F., & Wu, R. (2021) · Journal of Biomedical Science · doi:10.1186/s12929-021-00775-x · Cited by 99
Du, J., Lan, T., Liao, H., Feng, X., Chen, X., Liao, W., Hou, G., Xu, L., Feng, Q., Xie, K., et al. (2022) · Molecular Cancer · doi:10.1186/s12943-021-01482-9 · Cited by 95
“Their prominent features of higher stability than parental linear RNAs, highly conserved expression across species, and tissue- or developmental stage-specific expression suggest that circRNAs may possess multiple biological processes [7, 8].”
BackgroundAn integrated transcriptional analysis of the developing human retina
Mellough, C., Bauer, R., Collin, J., Dorgau, B., Zerti, D., Dolan, D., Jones, C. M., Izuogu, O. G., Yu, M., Hallam, D., et al. (2019) · Development · doi:10.1242/dev.169474 · Cited by 97
“, 2015), RNA editing (Rybak-Wolf et al., 2015; Aktas et al., 2017), RNA-binding proteins (Kramer et al.”
BackgroundAcfs: accurate circRNA identification and quantification from RNA-Seq data
You, X. A., & Conrad, T. (2016) · Scientific Reports · doi:10.1038/srep38820 · Cited by 94
Role of extracellular vesicles in tumour microenvironment
Tao, S., & Guo, S. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00643-5 · Cited by 102
Stagsted, L. V. W., O’Leary, E. T., Ebbesen, K. K., & Hansen, T. B. (2021) · eLife · doi:10.7554/elife.63088 · Cited by 95
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“Consistent with previous studies in other tissues (Rybak-Wolf et al., 2015), these heartexpressed circRNAs were usually derived from coding sequences (CDS, 58.7”
BackgroundResultInfluentialCircular RNAs of the nucleophosmin (NPM1) gene in acute myeloid leukemia
Lux, S., Blätte, T. J., Grasedieck, S., Cocciardi, S., ROUHI, A. M., Jongen‐Lavrencic, M., Paschka, P., Krönke, J., Gaidzik, V. I., Döhner, H., et al. (2017) · Haematologica · doi:10.3324/haematol.2017.172866 · Cited by 93
“Hundreds of circRNAs are, for example, differentially expressed during epithelial-mesenchymal transition,(37) and circRNAs are globally up-regulated during neuronal differentiation.(38) For the first time, we have shown that the expression of circRNAs, in line with mRNA, miRNA and lncRNA expression, is deregulated in…”
BackgroundLin, X., & Chen, Y. (2018) · Medical science monitor basic research/Medical science monitor. Basic research · doi:10.12659/msmbr.909737 · Cited by 93
“Circular RNA (circRNA) is a novel type of endogenous noncoding RNA that is expressed widely in different species and has been demonstrated to be a class of RNA with tissue/developmental stage-specificity, which makes circRNA a potential diagnostic and prognostic biomarkers [3].”
BackgroundZhou, Z., Niu, Y., Huang, G.-X., Lu, J., Chen, A., & Zhu, L. (2018) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2018.07.011 · Cited by 94
“Then we detected the conservation of circular RNA expression between human and rat by the method that was previously described.(59,60) In brief, by using the UCSC liftOver tool, the 50 and 30 flank coordinates of each differently expressed circular RNA from our profile were converted to human genome coordinates.”
MethodWang, X., Cao, X., Dong, D., Shen, X., Cheng, J., Jiang, R., Yang, Z., Peng, S., Huang, Y., Lan, X., et al. (2019) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.10.019 · Cited by 92
Li, W., Yang, F., Sun, C., Huang, J., Zhang, H., Li, X., Wang, G., Zhang, N., Che, J., Zhang, W., et al. (2020) · Theranostics · doi:10.7150/thno.43239 · Cited by 93
“shown to regulate circRNA biogenesis [25-28].”
Lauretti, E., Dabrowski, K. R., & Praticò, D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101425 · Cited by 97
CircRNA: A novel potential strategy to treat thyroid cancer (Review)
Zhu, G., Chang, X., Kang, Y., Zhao, X., Tang, X., Ma, C., & Fu, S. (2021) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2021.5034 · Cited by 95
Chen, J., Liu, G., Wu, Y., Ma, J., Wu, H.-F., Xie, Z., Chen, S., Yang, Y., Wang, S., Shen, P., et al. (2020) · Molecular Cancer · doi:10.1186/s12943-020-01193-7 · Cited by 92
Circular RNA of cattle casein genes are highly expressed in bovine mammary gland
Zhang, C., Wu, H. C., Wang, Y., Zhu, S., Liu, J., Fang, X., & Chen, H. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10381 · Cited by 90
“A recent study found that the majority of mouse brain circRNAs were also expressed as circRNAs in the human brain, and some of them were detected in Drosophila brains (Rybak-Wolf et al., 2015).”
BackgroundcircHLA-C Plays an Important Role in Lupus Nephritis by Sponging miR-150
Luan, J., Jiao, C., Kong, W., Fu, J., Qu, W., Chen, Y., Zhu, X., Zeng, Y., Guo, G., Qi, H., et al. (2017) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2017.12.006 · Cited by 92
“Recent studies demonstrated the expression of circRNAs as a cell-type-specific and tissue-specific manner.(5,8,9) In terms of the expression of circRNAs in the kidney, Wang et al.”
BackgroundA Zfp609 circular RNA regulates myoblast differentiation by sponging miR-194-5p
Wang, Y., Li, M., Wang, Y., Liu, J., Zhang, M., Fang, X., Chen, H., & Zhang, C. (2018) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2018.09.039 · Cited by 92
Circular RNAs in the pathogenesis of atherosclerosis
Cao, Q., Guo, Z., Du, S., Ling, H., & Song, C. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117837 · Cited by 94
Signature of circular RNAs in human induced pluripotent stem cells and derived cardiomyocytes
Lei, W., Feng, T., Fang, X., You, Y., Yang, J., Zhao, Z., Liu, J., Shen, Z., Deng, W., & Hu, S. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0793-5 · Cited by 92
CircRNA accumulation: A new hallmark of aging?
Knupp, D., & Miura, P. (2018) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2018.05.001 · Cited by 92
Non-coding RNAs in polycystic ovary syndrome: a systematic review and meta-analysis
Mu, L., Sun, X., Tu, M., & Zhang, D. (2021) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-020-00687-9 · Cited by 91
Nuclear export and translation of circular repeat-containing intronic RNA in C9ORF72-ALS/FTD
Wang, S., Latallo, M. J., Zhang, Z., Huang, B., Bobrovnikov, D. G., Dong, D., Livingston, N. M., Tjoeng, W., Hayes, L. R., Rothstein, J. D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25082-9 · Cited by 92
RNA-based therapeutics for neurological diseases
Anthony, K. (2022) · RNA Biology · doi:10.1080/15476286.2021.2021650 · Cited by 93
“Nonetheless, their potential as both therapeutic agents and targets is an emerging and relevant area of investigation for neurological diseases, especially since they are highly expressed in the brain [140].”
BackgroundDeep Insights in Circular RNAs: from biogenesis to therapeutics
Mumtaz, P. T., Taban, Q., Dar, M. A., Mir, S., Haq, Z. U., Zargar, S. M., Shah, R. A., & Ahmad, S. M. (2020) · Biological Procedures Online · doi:10.1186/s12575-020-00122-8 · Cited by 94
Biomarkers for Heart Failure Prognosis: Proteins, Genetic Scores and Non-coding RNAs
Shrivastava, A., Haase, T., Zeller, T., & Schulte, C. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.601364 · Cited by 92
“circRNAs appear to influence gene expression by competing with splicing of their linear counterparts (173, 218, 221).”
BackgroundRao, X., Lai, L., Li, X., Wang, L., Ai, L., & Yang, Q. (2020) · IUBMB Life · doi:10.1002/iub.2438 · Cited by 90
“eukaryotic cells, and has a tissue and developmental-stage specific expression pattern.(6) In terms of function, recent studies have shown that circRNA is rich in miRNA binding sites and act asmiRNA sponge to block or reduce the inhibitory effect of miRNA on target genes, thus increasing gene expression.”
BackgroundWong, C. H., Lou, U. K., Fung, F. K. C., TONG, J. H. M., Zhang, C., To, K., Chan, S. L., & Chen, Y. (2022) · Molecular Cancer · doi:10.1186/s12943-021-01481-w · Cited by 91
Circular RNAs in Muscle Function and Disease
Greco, S., Cardinali, B., Falcone, G., & Martelli, F. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113454 · Cited by 89
“Notably, circRNA abundance and circular to linear ratio generally increased during differentiation, as also observed upon neuronal differentiation [31], possibly related to the high stability of circRNAs accumulating in terminally differentiated cells over time.”
BackgroundTo edit or not to edit: regulation of ADAR editing specificity and efficiency
Deffit, S. N., & Hundley, H. A. (2015) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1319 · Cited by 89
Jin, C., Wang, A., Linbo, L., Wang, G., & Li, G. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27482 · Cited by 89
Emerging Roles of Exosomal Circular RNAs in Cancer
Seimiya, T., Otsuka, M., Iwata, T., Shibata, C., Tanaka, E., Suzuki, T., & Koike, K. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.568366 · Cited by 92
“Furthermore, the abundance of circRNAs is not correlated with that of the cognate linear RNA (Salzman et al., 2013), indicating distinct regulatory mechanisms and cellular functions of circRNAs.”
BackgroundCircular RNAs’ cap-independent translation protein and its roles in carcinomas
He, L., Man, C., Xiang, S., Yao, L., Wang, X., & Fan, Y. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01417-4 · Cited by 90
Cheng, Q., Wang, J., Li, M., Fang, J., Ding, H., Meng, J., Zhang, J., Fang, X., Liu, H., Ma, C., et al. (2022) · Redox Biology · doi:10.1016/j.redox.2022.102430 · Cited by 89
Xu, Y., Qiu, A., Peng, F., Tan, X., Wang, J., & Gong, X. (2020) · Neoplasma · doi:10.4149/neo_2020_200417n414 · Cited by 87
Advances in transcriptome analysis of human brain aging
Ham, S., & Lee, S. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00522-6 · Cited by 82
Circular RNA Expression in Basal Cell Carcinoma
Sand, M. S., Bechara, F. G., Sand, D., Gambichler, T., Hahn, S. A., Bromba, M., Stockfleth, E., & Hessam, S. (2016) · Epigenomics · doi:10.2217/epi-2015-0019 · Cited by 85
Circular RNAs as Promising Biomarkers: A Mini-Review
Abu, N., & Jamal, R. A. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00355 · Cited by 86
circFADS2 regulates lung cancer cells proliferation and invasion via acting as a sponge of miR-498
Zhao, F., Han, Y., Liu, Z., Zhao, Z., Li, Z., & Jia, K. (2018) · Bioscience Reports · doi:10.1042/bsr20180570 · Cited by 84
Li, Q.-H., Liu, Y., Chen, S., Zong, Z., Du, Y., Sheng, X., & Zhao, Y. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.108832 · Cited by 85
Huang, C., Deng, H., Wang, Y., Jiang, H., Xu, R., Zhu, X., Huang, Z., & Zhao, X. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14477 · Cited by 86
CircRNA Is a Rising Star in Researches of Ocular Diseases
Zhang, C., Hu, J., & Yu, Y. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00850 · Cited by 84
circRNA is a potential target for cardiovascular diseases treatment
Ju, J., Song, Y., Chen, X., Wang, T., Liu, C.-Y., & Wang, K. (2021) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-021-04286-z · Cited by 85
“The comparison of human and mouse circRNA datasets revealed that 15% of circRNAs are precisely conserved splice sites in orthologous genes, and 10% of circRNAs are conserved in the human, mouse, and rat hearts [13, 15, 35].”
BackgroundCharacterization of circular RNA s landscape in multiple system atrophy brain
Chen, B. J., Mills, J. D., Takenaka, K., Bliim, N., Halliday, G. M., & Janitz, M. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13752 · Cited by 84
“Subsequently, RNA was spiked with 10% C. elegans RNA, for normalization of qPCR quantification, as previously described (Rybak-Wolf et al. 2015).”
BackgroundMethodInfluentialShen, M., Li, T., Zhang, G., Wu, P., Chen, F., Lou, Q., Chen, L., Yin, X., Zhang, T., & Wang, J. (2019) · BMC Genomics · doi:10.1186/s12864-019-5462-2 · Cited by 86
Wang, S., Xue, X., Wang, R., Li, X., Li, Q., Wang, Y., Xie, P., Kang, Y.-H., Meng, R., & Feng, X. (2018) · Cancer Management and Research · doi:10.2147/cmar.s174778 · Cited by 82
“It was reported that circZNF609 was indispensable for the growth of central nervous system.(12) Strikingly, a more recent study found that circZNF609 could be translated into a protein, which was involved in controlling myoblast proliferation.”
BackgroundWu, Y., Hong, Z., Xu, W., Chen, J., Wang, Q., Chen, J., Ni, W., Mei, Z., Xie, Z., Ma, Y., et al. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.09.002 · Cited by 82
“efficiency of backsplicing compared with linear splicing.(11,12) Multiple functions of circRNAs have been identified.”
BackgroundZhou, Z., Du, D., Chen, A., & Zhu, L. (2017) · Gene · doi:10.1016/j.gene.2017.12.020 · Cited by 82
Human Survival Motor Neuron genes generate a vast repertoire of circular RNAs
Ottesen, E. W., Luo, D., Seo, J., Singh, N. N., & Singh, R. N. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz034 · Cited by 82
Present Scenario of Circular RNAs (circRNAs) in Plants
Zhao, W., Chu, S., & Jiao, Y. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00379 · Cited by 85
Noncoding AUG circRNAs constitute an abundant and conserved subclass of circles
Stagsted, L. V. W., Nielsen, K. M., Daugaard, I., & Hansen, T. B. (2019) · Life Science Alliance · doi:10.26508/lsa.201900398 · Cited by 82
Chuang, T., Chen, Y., Chen, C.-Y., Mai, T., Wang, Y.-D., Yeh, C.-S., Yang, M.-Y., Hsiao, Y., Chang, T., Kuo, T.-C., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky032 · Cited by 80
“This result seems to reflect previous reports that ADAR1 expression was negatively correlated with circRNA biogenesis (16,52), although interactions between ADAR and these two types of NCL events await further investigation.”
BackgroundResultZou, Y., Zheng, S., Xiao, W., Xie, X., Yang, A., Gao, G., Xiong, Z., Xue, Z., Tang, H., & Xie, X. (2019) · Carcinogenesis · doi:10.1093/carcin/bgz071 · Cited by 81
How are circRNAs translated by non-canonical initiation mechanisms?
Diallo, L. H., Tatin, F., David, F., Godet, A.-C., Zamora, A., Prats, A., Garmy-Susini, B. H., & Lacazette, É. (2019) · Biochimie · doi:10.1016/j.biochi.2019.06.015 · Cited by 84
Sam68 binds Alu-rich introns in SMN and promotes pre-mRNA circularization
Pagliarini, V., Jolly, A., Bielli, P., Rosa, V. D., de la Grange, P., & Sette, C. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1117 · Cited by 79
“Since circRNAs accumulate in brain with ageing (43) and their dysregulation possibly contributes to neurodegenerative diseases (44), modulating their expression in the brain may have both physiological and pathological consequences.”
BackgroundExportin 4 depletion leads to nuclear accumulation of a subset of circular RNAs
Chen, L., Wang, Y., Lin, J., Song, Z., Wang, Q., Zhao, W., Wang, Y., Xiu, X., Deng, Y., Li, X., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33356-z · Cited by 88
Potential Diagnostic Power of Blood Circular RNA Expression in Active Pulmonary Tuberculosis
Qian, Z., Liu, H., Li, M., Shi, J., Li, N., Zhang, Y., Zhang, X., Lv, J., Xie, X., Bai, Y., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.12.007 · Cited by 81
“Dynamic circRNA profiles are related to neurogenesis (Rybak-Wolf et al., 2015), mouse brain development”
BackgroundInfluentialHan, Z., Zhang, Y., Sun, Y., Chen, J., Chang, C., Wang, X., & Yeh, S. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-1575 · Cited by 82
Jin, M., Shi, C., Yang, C., Liu, J., & Huang, G. (2019) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.08.016 · Cited by 80
“The circular covalently bonded structure means that they do not have a 50-to-30 polarity or poly(A) tail, which endows them with a higher tolerance to exonucleases.(6) It has been found that many circRNAs originate from protein-coding genes.”
BackgroundRetractedZhang, H., Shen, Y., Li, Z., Ruan, Y., Li, T., Xiao, B., & Sun, W. (2019) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.23049 · Cited by 80
Circular RNAs—The Road Less Traveled
Guria, A., Sharma, P., Natesan, S., & Pandi, G. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2019.00146 · Cited by 79
“The knocking down of ADAR1 and ADAR2 in human and mouse cell lines and inDrosophila increases circRNA expression without perturbing the linear RNA transcript (Ivanov et al., 2015; Rybak-Wolf et al., 2015).”
BackgroundZhang, J., Li, Y., Qi, J., Yu, X., Ren, H., Zhao, X., Xin, W., He, S., Zheng, X., Ma, C., et al. (2020) · Hypertension · doi:10.1161/hypertensionaha.119.13715 · Cited by 82
“We then judged that circ-calm4 was conserved based on phyloP analysis (phylogenetic P; Figure S1D).(21) For quantitative analysis of circRNAs, a specific primer, called the divergent primer, was designed for the backsplice junction site with as short a length as possible to enhance the amplification efficiency at the…”
MethodEmerging Role of Circular RNAs in Cancer
Liu, J., Zhang, X., Yan, M., & Li, H. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00663 · Cited by 77
“Moreover, circRNAs may have higher sequence conservation than other types of RNA in mammals (41).”
BackgroundThe Landscape of Circular RNA Expression in the Human Brain
Gokoolparsadh, A., Anwar, F., & Voineagu, I. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.07.029 · Cited by 79
Hu, K., Liu, X., Li, Y., Li, Q., Xu, Y., Zeng, W., Zhong, G., & Yu, C. (2020) · Medical Science Monitor · doi:10.12659/msm.922253 · Cited by 79
“Circular RNAs (circRNAs) are a class of non-coding transcripts that contain covalently closed loop structures [12].”
BackgroundIntegrated Multi-Omics for Novel Aging Biomarkers and Antiaging Targets
Wu, L., Xie, X., Liang, T., Ma, J., Yang, L., Yang, J., Li, L., Xi, Y., Li, H., Zhang, J., et al. (2021) · Biomolecules · doi:10.3390/biom12010039 · Cited by 87
Lin, X., Han, M., Cheng, L., Chen, J., Zhang, Z., Shen, T., Wang, M., Wen, B., Ni, T., & Han, C. (2016) · RNA Biology · doi:10.1080/15476286.2016.1218588 · Cited by 80
“A recent study reported the identification of 15,849 circRNAs in the mouse brain using RNA samples without RNase R treatment.(34) We re-processed this raw data using the CIRI program and recovered 13,282 circRNAs and compared this data with our g-circRNA set.”
MethodCircRNAs as biomarkers of cancer: a meta-analysis
Wang, M., Yang, Y., Xu, J., Bai, W., Ren, X., & Wu, H. (2018) · BMC Cancer · doi:10.1186/s12885-018-4213-0 · Cited by 80
Annotation and functional clustering of circRNA expression in rhesus macaque brain during aging
Xu, K., Chen, D., Wang, Z., Ma, J., Zhou, J. P., Chen, N., Lv, L., Zheng, Y., Hu, X., Zhang, Y., et al. (2018) · Cell Discovery · doi:10.1038/s41421-018-0050-1 · Cited by 80
Cancer-related circular RNA: diverse biological functions
Cheng, D., Wang, J., Dong, Z., & Li, X. (2021) · Cancer Cell International · doi:10.1186/s12935-020-01703-z · Cited by 79
“For instance, it has been reported that 4522 out of 15,849 circRNAs in mice possess homologous sequences in humans [14].”
BackgroundThe Implications of ncRNAs in the Development of Human Diseases
López-Jiménez, E. A., & Andrés‐León, E. (2021) · Non-Coding RNA · doi:10.3390/ncrna7010017 · Cited by 83
NOVA2 regulates neural circRNA biogenesis
Knupp, D., Cooper, D. A., Saito, Y., Darnell, R. B., & Miura, P. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab523 · Cited by 76
“CircRNAs are enriched in brain tissues on a genomewide level (27–30) and are dramatically upregulated during neural differentiation and maturation (15,29,30).”
BackgroundQu, Z., Meng, F., Shi, J., Deng, G., Zeng, X., Ge, J., Li, Y., Liu, L., Chen, P., Jiang, Y., et al. (2021) · mBio · doi:10.1128/mbio.01017-21 · Cited by 79
“when linear transcript expression also increases but rarely by the same factor (48, 49).”
BackgroundCircular RNAs and glioblastoma multiforme: focus on molecular mechanisms
Salami, R., Salami, M., Mafi, A., Vakili, O., & Asemi, Z. (2022) · Cell Communication and Signaling · doi:10.1186/s12964-021-00809-9 · Cited by 76
“First, circRNAs are greatly expressed in nervous tissues [68], suggesting that they may be contributed to many CNS-related processes, like the synaptic transmission [69], aging [70] neurogenesis, and brain development [71, 72].”
BackgroundExploring the cellular landscape of circular RNAs using full-length single-cell RNA sequencing
Wu, W., Zhang, J., Cao, X., Cai, Z., & Zhao, F. (2022) · Nature Communications · doi:10.1038/s41467-022-30963-8 · Cited by 77
Gao, J., Ao, Y.-Q., Zhang, L.-X., Deng, J., Wang, S., Wang, H., Jiang, J.-H., & Ding, J. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02505-z · Cited by 79
“Their relatively stable structure, species conservation, and high abundance suggest that circRNAs may serve as reliable biomarkers for cancers [8].”
BackgroundDai, X., Zhang, N., Cheng, Y., Yang, T., Chen, Y. P., Liu, Z., Wang, Z., Yang, C., & Jiang, Y. (2018) · Carcinogenesis · doi:10.1093/carcin/bgy061 · Cited by 77
Circular RNA; a new biomarker for breast cancer: A systematic review
Jahani, S., Nazeri, E., Majidzadeh‐A, K., Jahani, M., & Esmaeili, R. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29558 · Cited by 79
“The RNA‐editing activity of ADAR1 suppresses the expression of circRNA (Rybak‐Wolf et al., 2015).”
BackgroundSuenkel, C., Cavalli, D., Massalini, S., Calegari, F., & Rajewsky, N. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.083 · Cited by 78
Self-citationCircR2Cancer: a manually curated database of associations between circRNAs and cancers
Lan, W., Zhu, M., Chen, Q., Chen, B., Liu, J., Li, M., & Chen, Y. P. (2020) · Database · doi:10.1093/database/baaa085 · Cited by 77
“In addition, circRNA is not affected by RNA exonuclease, and its expression is more stable and less prone to degradation (2).”
BackgroundCircular RNAs in the human brain are tailored to neuron identity and neuropsychiatric disease
Dong, X., Bai, Y., Liao, Z., Gritsch, D., Liu, X., Wang, T., Borges-Monroy, R., Ehrlich, A., Serrano, G. E., Feany, M. Β., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40348-0 · Cited by 83
“This expands on a postulated role for circRNAs in synaptosomes 4,5 and synaptic plasticity 4 in animals.”
InfluentialWarning SINEs: Alu elements, evolution of the human brain, and the spectrum of neurological disease
Larsen, P. A., Hunnicutt, K. E., Larsen, R. J., Yoder, A. D., & Saunders, A. M. (2018) · Chromosome Research · doi:10.1007/s10577-018-9573-4 · Cited by 79
“2015), formation of regulatory circRNAs that are enriched in the central nervous system (CNS) and concentrated at synapses (Jeck et al. 2013; Rybak-Wolf et al. 2015; Chen and Schuman 2016; Floris et al. 2017), regulation of genes that are essential for proper neuron function (e.”
BackgroundInfluentialEmerging Role of Circular RNAs as Potential Biomarkers for the Diagnosis of Human Diseases
Ojha, R., Nandani, R., Chatterjee, N., & Prajapati, V. K. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-1426-1_12 · Cited by 76
Metadata
- Authors
- Rybak-Wolf, A., Stottmeister, C., Glažar, P., Jens, M., Pino, N., Giusti, S., Hanan, M., Behm, M., Bartok, O., Ashwal-Fluss, R., Herzog, M., Schreyer, L., Papavasileiou, P., Ivanov, A., Öhman, M., Refojo, D., Kadener, S., & Rajewsky, N.
- Affiliations
- Max Delbrück Center (DE)
- Max Planck Institute of Psychiatry (DE)
- Hebrew University of Jerusalem (IL)
- Stockholm University (SE)
- Corresponding author
- Rajewsky, Nikolaus
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2015-06
- Volume
- 58
- Issue
- 5
- Pages
- 870-885
- ISSN
- 1097-2765 (ISSN-L)
- OpenAlex
- W1991082489
- Semantic Scholar
- 2d5cc6120582eee013b4aab9138fa48d35f384f1
- Cited by
- 2,423
- References
- 40
- Citations by year
- 2026: 68 · 2025: 143 · 2024: 238 · 2023: 246 · 2022: 312 · 2021: 358 · 2020: 344 · 2019: 284 · 2018: 203 · 2017: 122 · 2016: 74 · 2015: 23
- FWCI
- 61.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Americanae (AECID Library) (publishedVersion, other-oa)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-nd)
- 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, mammalian brain, neuronal differentiation, synapses, ADAR1, RNA editing, Drosophila brain, circRNA biomarkers
- MeSH terms
- RNA, Circular, Animals, Base Sequence, Brain, Cell Line, Drosophila melanogaster, Humans, Molecular Sequence Data, Organ Specificity, RNA, RNA, Messenger, Synapses, Sequence Analysis, DNA, Mice, Neurogenesis
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