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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Many circRNAs are significantly upregulated at different time points of neuron maturation in vitro.
“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]
circRNAs are highly expressed in the brain from the embryonic stage to adulthood and are substantially upregulated during differentiation and maturation of neurons.
“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]
CircRNAs maintain specificity and conservatism in dynamic expression and are highly enriched in the mammalian brain, independent of linear transcripts.
“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]
CiRS-7 is abundantly expressed in the mammalian brain, where it increases the translation of the miR-7 target mRNA.
“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]
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.
“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]
Compared with other cytoplasmic RNAs, circRNAs seem to be more prone to being localized in synapses and their expression is correlated with neural plasticity.
“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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“, 2015) was reported to suppress circRNA production (Ivanov et al., 2015; Rybak-Wolf et al., 2015).”
BackgroundInfluentialRETRACTED ARTICLE: CircHIPK3 promotes colorectal cancer growth and metastasis by sponging miR-7
Zeng, K., Chen, X., Xu, M., Liu, X., Hu, X., Xu, T., Sun, H., Pan, Y., He, B., & Wang, S. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0454-8 · Cited by 628 · see citing works
“Circular RNAs (circRNA) are highly conserved and stable covalently closed RNA transcripts generated by back-splicing of a single pre-mRNA with gene-regulatory potential 3,4 .”
BackgroundRetractedN6-Methyladenosine Modification Controls Circular RNA Immunity
Chen, Y. G., Chen, R., Ahmad, S., Verma, R., Kasturi, S. P., Amaya, L., Broughton, J. P., Kim, J., Cadena, C., Pulendran, B., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.07.016 · Cited by 572 · see citing works
CircHIPK3 sponges miR‐558 to suppress heparanase expression in bladder cancer cells
Li, Y., Zheng, F., Xiao, X., Xie, F., Tao, D., Huang, C., Liu, D., Wang, M., Wang, L., Zeng, F., et al. (2017) · EMBO Reports · doi:10.15252/embr.201643581 · Cited by 559 · see citing works
Circbank: a comprehensive database for circRNA with standard nomenclature
Liu, M., Wang, Q., Shen, J., Yang, B. B., & Ding, X. (2019) · RNA Biology · doi:10.1080/15476286.2019.1600395 · Cited by 555 · see citing works
“CircRNAs were found to be expressed across various species including human, mouse, fly, worm, plant and yeast [3,5,28,29].”
BackgroundTargeting circular RNAs as a therapeutic approach: current strategies and challenges
He, A. T., Liu, J., Li, F., & Yang, B. B. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00569-5 · Cited by 556 · see citing works
Circular RNAs: Biogenesis, Function and Role in Human Diseases
Greene, J. P., Baird, A., Brady, L., Lim, M. C. J., Gray, S. G., McDermott, R., & Finn, S. P. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00038 · Cited by 554 · see citing works
“It has been implicated in decreasing circRNA production by weakening and editing RNA duplexes which decreases the likelihood of circularization (Rybak-Wolf et al., 2015).”
BackgroundThe novel roles of circRNAs in human cancer
Shang, Q., Yang, Z. H., Jia, R., & Ge, S. (2019) · Molecular Cancer · doi:10.1186/s12943-018-0934-6 · Cited by 548 · see citing works
FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons
Errichelli, L., Modigliani, S. D., Laneve, P., Colantoni, A., Legnini, I., Capauto, D., Rosa, A., Santis, R. D., Scarfò, R., Peruzzi, G., et al. (2017) · Nature Communications · doi:10.1038/ncomms14741 · Cited by 541 · see citing works
Circular RNA in cardiovascular disease
Altesha, M., Ni, T. T., Khan, A., Liu, K., & Zheng, X. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27384 · Cited by 520 · see citing works
An emerging function of circRNA-miRNAs-mRNA axis in human diseases
Rong, D., Sun, H., Li, Z., Liu, S., Dong, C., Fu, K., Tang, W., & Cao, H. (2017) · Oncotarget · doi:10.18632/oncotarget.19154 · Cited by 516 · see citing works
“However, some circRNAs expressions are on the contrary, for example, circRNAs including Rims2, Tulp4 and Elf2 were found to be the major isoform of multiple genes in brain tissues [17].”
BackgroundKramer, M. C., Liang, D., Tatomer, D. C., Gold, B., March, Z. M., Cherry, S. R., & Wilusz, J. E. (2015) · Genes & Development · doi:10.1101/gad.270421.115 · Cited by 494 · see citing works
“…and recent deep sequencing studies have expanded this observation to thousands of circular RNAs expressed across eukaryotes, including humans (Salzman et al. 2012; Jeck et al. 2013; Memczak et al. 2013; Guo et al. 2014; Conn et al. 2015; Kelly et al. 2015), mice (Memczak et al. 2013;…”
BackgroundSpatio-temporal regulation of circular RNA expression during porcine embryonic brain development
Venø, M. T., Hansen, T. B., Venø, S. T., Clausen, B. H., Grebing, M., Finsen, B. R., Holm, I. E., & Kjems, J. (2015) · Genome biology · doi:10.1186/s13059-015-0801-3 · Cited by 475 · see citing works
“expressed in human cortex, while in mouse it is almost exclusively located in the cerebellum [27].”
BackgroundResultSpecific expression and functions of circular RNAs
Mısır, S., Wu, N., & Yang, B. B. (2022) · Cell Death and Differentiation · doi:10.1038/s41418-022-00948-7 · Cited by 482 · see citing works
“The abundance of circRNAs is specific to cell types and tissues during development [7, 8].”
BackgroundInfluentialPatop, I. L., & Kadener, S. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2017.11.007 · Cited by 469 · see citing works
Self-citationKim, K. M., Abdelmohsen, K., Mustapić, M., Kapogiannis, D., & Gorospe, M. (2017) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1413 · Cited by 456 · see citing works
Insights into circular RNA biology
Ebbesen, K. K., Hansen, T. B., & Kjems, J. (2016) · RNA Biology · doi:10.1080/15476286.2016.1271524 · Cited by 454 · see citing works
“However, impaired circRNA biogenesis could be caused by indirect effects of ADAR1.(10,18)”
BackgroundInfluentialA 360° view of circular RNAs: From biogenesis to functions
Wilusz, J. E. (2018) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1478 · Cited by 438 · see citing works
Liang, D., Tatomer, D. C., Luo, Z., Wu, H., Yang, L. C., Chen, L., Cherry, S. R., & Wilusz, J. E. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.10.034 · Cited by 435 · see citing works
“It has instead been suggested that circular RNAs may help form large RNA-protein complexes, e.g., at neuronal synapses (Rybak-Wolf et al., 2015; You et al., 2015); be translated (Abe et al., 2015; Chen and Sarnow, 1995; Kramer et al., 2015; Legnini et al., 2017; Pamudurti et al., 2017; Yang et al.,…”
BackgroundThe emerging roles and functions of circular RNAs and their generation
Yu, C., & Kuo, H. (2019) · Journal of Biomedical Science · doi:10.1186/s12929-019-0523-z · Cited by 431 · see citing works
The emerging landscape of circular RNA in life processes
Qu, S., Zhong, Y., Shang, R., Zhang, X., Song, W., Kjems, J., & Li, H. (2016) · RNA Biology · doi:10.1080/15476286.2016.1220473 · Cited by 421 · see citing works
“CircRNAs can be generated from any region of the genome, and all result in a great diversity of lengths.(17-20,30,35,45,46) The”
BackgroundCheng, Z., Yu, C., Cui, S., Wang, H., Jin, H., Wang, C., Li, B., Qin, M., Yang, C. G., He, J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11162-4 · Cited by 418 · see citing works
CircRNAs and cancer: Biomarkers and master regulators
Arnaiz, E., Solé, C., Manterola, L., Iparraguirre, L., Otaegui, D., & Lawrie, C. H. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.12.002 · Cited by 408 · see citing works
Biogenesis, identification, and function of exonic circular RNAs
Chen, I., Chen, C., & Chuang, T. (2015) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1294 · Cited by 397 · see citing works
Circles reshaping the RNA world: from waste to treasure
Liu, J., Liu, T., Wang, X., & He, A. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0630-y · Cited by 397 · see citing works
“and intensive accumulation in neural tissues [68].”
The bioinformatics toolbox for circRNA discovery and analysis
Chen, L., Wang, C., Sun, H., Wang, J., Liang, Y., Wang, Y., & Wong, G. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa001 · Cited by 394 · see citing works
“One study applied BSJ read and normal splicing junction read ratio (named circular-to-linear ratio, CLR) to represent the ratio of circRNA and linear RNA to obtain an overall expression value [93].”
BackgroundA map of human circular RNAs in clinically relevant tissues
Maass, P. G., Glažar, P., Memczak, S., Dittmar, G. A. G., Hollfinger, I., Schreyer, L., Sauer, A. V., Toka, O., Aiuti, A., Luft, F. C., et al. (2017) · Journal of Molecular Medicine · doi:10.1007/s00109-017-1582-9 · Cited by 388 · see citing works
Self-citationThe Diversity of Long Noncoding RNAs and Their Generation
Wu, H., Yang, L. C., & Chen, L. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.05.004 · Cited by 378 · see citing works
CircRNAs: role in human diseases and potential use as biomarkers
Verduci, L., Tarcitano, E., Strano, S., Yarden, Y., & Blandino, G. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03743-3 · Cited by 377 · see citing works
Dube, U., Del-Aguila, J. L., Li, Z., Budde, J. P., Jiang, S., Hsu, S., Ibanez, L., Fernandez, M. V., Farias, F., Norton, J., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0501-5 · Cited by 345 · see citing works
Circular RNAs Co-Precipitate with Extracellular Vesicles: A Possible Mechanism for circRNA Clearance
Lasda, E. L., & Parker, R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148407 · Cited by 375 · see citing works
CircRNA accumulation in the aging mouse brain
Gruner, H. N., Cortés-López, M., Cooper, D. A., Bauer, M. J., & Miura, P. (2016) · Scientific Reports · doi:10.1038/srep38907 · Cited by 366 · see citing works
Comprehensive characterization of tissue-specific circular RNAs in the human and mouse genomes
Xia, S., Feng, J. Q., Lei, L., Hu, J., Xia, L., Wang, J., Xiang, Y., Liu, L., Zhong, S., Han, L., et al. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw081 · Cited by 362 · see citing works
“We allowed 2 bp window while comparing the backsplice sites as previously described [2].”
BackgroundMethodCircular RNAs open a new chapter in cardiovascular biology
Aufiero, S., Reckman, Y. J., Pinto, Y. M., & Creemers, E. E. (2019) · Nature Reviews Cardiology · doi:10.1038/s41569-019-0185-2 · Cited by 353 · see citing works
Review on circular RNAs and new insights into their roles in cancer
Tang, X., Ren, H., Guo, M., Qian, J., Yang, Y., & Gu, C. (2021) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2021.01.018 · Cited by 353 · see citing works
Screening for functional circular RNAs using the CRISPR–Cas13 system
Li, S., Li, X., Xue, W., Zhang, L., Yang, L.-Z., Cao, S.-M., Lei, Y.-N., Liu, C.-X., Guo, S.-K., Shan, L., et al. (2020) · Nature Methods · doi:10.1038/s41592-020-01011-4 · Cited by 355 · see citing works
CircNet: a database of circular RNAs derived from transcriptome sequencing data
Liu, Y., Li, J., Sun, C.-H., Andrews, E. H., Chao, R.-F., Lin, F.-M., Weng, S.-L., Hsu, S., Huang, C., Cheng, C., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv940 · Cited by 343 · see citing works
“CircRNAs functional correlation with brain function, synaptic plasticity (26,27) and fetal development (28) has recently been reported.”
BackgroundMolecular roles and function of circular RNAs in eukaryotic cells
Holdt, L. M., Kohlmaier, A., & Teupser, D. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2688-5 · Cited by 341 · see citing works
“CircRNAs have been found to be particularly enriched in neuronal tissues of different organisms ranging from Dros‐ ophila to humans [29, 30, 44, 77, 131].”
BackgroundInfluentialDenzler, R., McGeary, S. E., Title, A. C., Agarwal, V., Bartel, D. P., & Stoffel, M. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.09.027 · Cited by 340 · see citing works
“However, very few other circRNAs have more miRNA-binding sites than expected by chance (Guo et al., 2014; Rybak-Wolf et al., 2015), which brings the focus back to linear transcripts as a more abundant source of potential ceRNA candidates.”
BackgroundCircACC1 Regulates Assembly and Activation of AMPK Complex under Metabolic Stress
Li, Q., Wang, Y., Wu, S., Zhou, Z., Ding, X., Shi, R., Thorne, R. F., Zhang, X. D., Hu, W., & Wu, M. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.05.009 · Cited by 339 · see citing works
The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency
Yu, C.-Y., Li, T.-C., Wu, Y.-Y., Yeh, C.-H., Chiang, W., Chuang, C.-Y., & Kuo, H.-C. (2017) · Nature Communications · doi:10.1038/s41467-017-01216-w · Cited by 336 · see citing works
Dou, Y., Cha, D. J., Franklin, J. L., Higginbotham, J. N., Jeppesen, D. K., Weaver, A. M., Prasad, N., Levy, S., Coffey, R. J., Patton, J. G., et al. (2016) · Scientific Reports · doi:10.1038/srep37982 · Cited by 330 · see citing works
Circular RNA mediates cardiomyocyte death via miRNA-dependent upregulation of MTP18 expression
Wang, K., Gan, T.-Y., Li, N., Liu, C.-Y., Zhou, L., Gao, J.-N., Chen, C., Yan, K.-W., Ponnusamy, M., Zhang, Y.-H., et al. (2017) · Cell Death and Differentiation · doi:10.1038/cdd.2017.61 · Cited by 324 · see citing works
Chen, X., Mao, R., Su, W., Yang, X., Geng, Q., Guo, C., Wang, Z., Wang, J., Kresty, L. A., Beer, D. G., et al. (2019) · Autophagy · doi:10.1080/15548627.2019.1634945 · Cited by 322 · see citing works
Exosomal noncoding RNAs in Glioma: biological functions and potential clinical applications
Cheng, J., Meng, J., Zhu, L., & Peng, Y. (2020) · Molecular Cancer · doi:10.1186/s12943-020-01189-3 · Cited by 317 · see citing works
Single-cell and spatial transcriptomics: deciphering brain complexity in health and disease
Piwecka, M., Rajewsky, N., & Rybak-Wolf, A. (2023) · Nature Reviews Neurology · doi:10.1038/s41582-023-00809-y · Cited by 320 · see citing works
Self-citationThe pro-metastasis effect of circANKS1B in breast cancer
Zeng, K., He, B., Yang, B. B., Xu, T., Chen, X., Xu, M., Liu, X., Sun, H., Pan, Y., & Wang, S. (2018) · Molecular Cancer · doi:10.1186/s12943-018-0914-x · Cited by 319 · see citing works
Lessons from non-canonical splicing
Sibley, C. R., Blázquez, L., & Ule, J. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.46 · Cited by 312 · see citing works
Structured elements drive extensive circular RNA translation
Chen, C., Cheng, R., Demeter, J., Chen, J., Weingarten-Gabbay, S., Jiang, L., Snyder, M. P., Weissman, J. S., Segal, E., Jackson, P. K., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.07.042 · Cited by 316 · see citing works
“Because circRNAs are expressed in a tissue-specific and cell line-specific manner (Rybak-Wolf et al., 2015), to accurately estimate the circORF discovery rate (the number of circORFs detected in each dataset), we consider the IRES-containing circRNAs expressed in the corresponding cell line as the denominator.”
BackgroundBiogenesis and Functions of Circular RNAs Come into Focus
Xiao, M., Ai, Y., & Wilusz, J. E. (2020) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.12.004 · Cited by 315 · see citing works
Lu, Q., Liu, T., Feng, H., Yang, R., Zhao, X., Chen, W., Jiang, B., Qin, H., Guo, X., Liu, M., et al. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1040-0 · Cited by 312 · see citing works
“Salient features of circRNAs include significant stability, high abundance, evolutionary conservation, and tissue-specific expression [9, 10].”
BackgroundCircular RNA: An emerging non-coding RNA as a regulator and biomarker in cancer
Chen, B., & Huang, S. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.01.011 · Cited by 308 · see citing works
Biogenesis and Regulatory Roles of Circular RNAs
Yang, L. C., Wilusz, J. E., & Chen, L. (2022) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-120420-125117 · Cited by 303 · see citing works
CircNT5E Acts as a Sponge of miR-422a to Promote Glioblastoma Tumorigenesis
Wang, R., Zhang, S., Chen, X., Li, N., Li, J., Jia, R., Pan, Y., & Liang, H. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0532 · Cited by 298 · see citing works
“Two important studies revealed that the RNA-editing enzyme ADAR1 is involved in circRNA biogenesis and that its knockdown may significantly upregulate circRNA expression in human HEK293 cells and SH-SY5Y cells (41, 45).”
BackgroundResultChen, G., Shi, Y., Liu, M., & Sun, J. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0204-3 · Cited by 291 · see citing works
Circular RNAs: a new frontier in the study of human diseases
Chen, Y., Li, C., Tan, C., & Liu, X. (2016) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2016-103758 · Cited by 293 · see citing works
“Rybak-Wolf et al 42 examined 29 human/mouse RNA sequencing datasets from dissected brain tissues or neuronal-differentiated cell lines.”
BackgroundComprehensive identification of internal structure and alternative splicing events in circular RNAs
Gao, Y., Wang, J., Zheng, Y., Zhang, J., Chen, S., & Zhao, F. (2016) · Nature Communications · doi:10.1038/ncomms12060 · Cited by 292 · see citing works
Circular RNAs in immune responses and immune diseases
Chen, X., Yang, T., Wang, W., Xi, W., Zhang, T., Li, Q., Yang, A., & Wang, T. (2019) · Theranostics · doi:10.7150/thno.29678 · Cited by 291 · see citing works
Circular RNA: an emerging key player in RNA world
Meng, X., Li, X., Zhang, P., Wang, J., Zhou, Y., & Chen, M. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw045 · Cited by 290 · see citing works
Role of circular RNAs in brain development and CNS diseases
Mehta, S. L., Dempsey, R. J., & Vemuganti, R. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101746 · Cited by 281 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript PRR11 proline-rich protein 11 RBPs RNA binding proteins RNA-FISH RNA fluorescence in situ hybridization ROS reactive oxygen species SCI spinal cord injury SIRT1 Sirtuin 1 SMN1 survival motor neuron 1 SOX13 SRY-Box 13 SRSF1 serine and argin…”
BackgroundInfluentialDong, R., Ma, X.-K., Li, G., & Yang, L. C. (2018) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2018.08.001 · Cited by 275 · see citing works
“Although generally expressed at low levels, circRNAs are highly enriched in brains/neurons [18,23,31].”
BackgroundInfluentialCircular RNAs: A Novel Class of Functional RNA Molecules with a Therapeutic Perspective
Santer, L., Bär, C., & Thum, T. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.07.001 · Cited by 277 · see citing works
“ADAR expression level negatively correlates with several circRNAs.(30,31) More recently, it was described that the RNA helicase DHX9 (DExH-Box Helicase 9), which binds double-stranded RNA (dsRNA), is involved in the”
BackgroundCircular RNA BCRC-3 suppresses bladder cancer proliferation through miR-182-5p/p27 axis
Xie, F., Li, Y., Wang, M., Huang, C., Tao, D., Zheng, F., Zhang, H., Zeng, F., Xiao, X., & Jiang, G. (2018) · Molecular Cancer · doi:10.1186/s12943-018-0892-z · Cited by 274 · see citing works
circPTN sponges miR-145-5p/miR-330-5p to promote proliferation and stemness in glioma
Chen, J., Chen, T., Zhu, Y., Li, Y., Zhang, Y., Wang, Y., Li, X., Xie, X., Wang, J., Huang, M., et al. (2019) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-019-1376-8 · Cited by 271 · see citing works
- 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 · 2014: 1 · 2013: 1 · 2012: 1
- 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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