Insights into the biogenesis and potential functions of exonic circular RNA
Open accessAbstract
Circular RNAs (circRNAs) exhibit unique properties due to their covalently closed nature. Models of circRNAs synthesis and function are emerging but much remains undefined about this surprisingly prevalent class of RNA. Here, we identified exonic circRNAs from human and mouse RNA-sequencing datasets, documenting multiple new examples. Addressing function, we found that many circRNAs co-sediment with ribosomes, indicative of their translation potential. By contrast, circRNAs with potential to act as microRNA sponges were scarce, with some support for a collective sponge function by groups of circRNAs. Addressing circRNA biogenesis, we delineated several features commonly associated with circRNA occurrence. CircRNA-producing genes tend to be longer and to contain more exons than average. Back-splice acceptor exons are strongly enriched at ordinal position 2 within genes, and circRNAs typically have a short exon span with two exons being the most prevalent. The flanking introns either side of circRNA loci are exceptionally long. Of note also, single-exon circRNAs derive from unusually long exons while multi-exon circRNAs are mostly generated from exons of regular length. These findings independently validate and extend similar observations made in a number of prior studies. Furthermore, we analysed high-resolution RNA polymerase II occupancy data from two separate human cell lines to reveal distinctive transcription dynamics at circRNA-producing genes. Specifically, RNA polymerase II traverses the introns of these genes at above average speed concomitant with an accentuated slow-down at exons. Collectively, these features indicate how a perturbed balance between transcription and linear splicing creates important preconditions for circRNA production. We speculate that these preconditions need to be in place so that looping interactions between flanking introns can promote back-splicing to raise circRNA production to appreciable levels.
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Average RNA Pol II velocity is higher on genes producing circRNAs than on genes not producing circRNAs, and especially on introns of these genes.
“Indeed, the average RNA Pol II velocity is higher on genes producing circRNAs than on genes not producing circRNAs (Zhang et al, 2016) and especially on introns of these genes (Ragan et al, 2019).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Ragan et al, 2019
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Cites
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
BEDTools: a flexible suite of utilities for comparing genomic features
Quinlan, A. R., & Hall, I. M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq033 · Cited by 27,437 · see citing works
Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J., & Pachter, L. (2010) · Nature Biotechnology · doi:10.1038/nbt.1621 · Cited by 15,556 · see citing works
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., & Salzberg, S. L. (2013) · Genome Biology · doi:10.1186/gb-2013-14-4-r36 · Cited by 12,668 · see citing works
Circular RNAs are a large class of animal RNAs with regulatory potency
Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S. D., Gregersen, L. H., Munschauer, M., et al. (2013) · Nature · doi:10.1038/nature11928 · Cited by 7,990 · see citing works
Natural RNA circles function as efficient microRNA sponges
Hansen, T. B., Jensen, T. I., Clausen, B. H., Bramsen, J. B., Finsen, B., Damgaard, C. K., & Kjems, J. (2013) · Nature · doi:10.1038/nature11993 · Cited by 7,985 · see citing works
Li, J.-H., Liu, S., Zhou, H., Qu, L., & Yang, J.-H. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1248 · Cited by 5,587 · see citing works
Circular RNAs are abundant, conserved, and associated with ALU repeats
Jeck, W. R., Sorrentino, J. A., Wang, K., Slevin, M. K., Burd, C. E., Liu, J., Marzluff, W. F., & Sharpless, N. E. (2013) · RNA · doi:10.1261/rna.035667.112 · Cited by 4,388 · see citing works
circRNA biogenesis competes with pre-mRNA splicing
Ashwal-Fluss, R., Meyer, M., Pamudurti, N. R., Ivanov, A., Bartok, O., Hanan, M., Evantal, N., Memczak, S., Rajewsky, N., & Kadener, S. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.019 · Cited by 3,083 · see citing works
Exon-intron circular RNAs regulate transcription in the nucleus
Li, Z., Huang, C., Bao, C., Chen, L., Lin, M., Wang, X., Zhong, G., Yu, B., Hu, W., Dai, L., et al. (2015) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2959 · Cited by 2,905 · see citing works
Salzman, J., Gawad, C., Wang, P. L., Lacayo, N. J., & Brown, P. O. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030733 · Cited by 2,457 · see citing works
The RNA Binding Protein Quaking Regulates Formation of circRNAs
Conn, S. J., Pillman, K. A., Toubia, J., Conn, V. M., Salmanidis, M., Phillips, C. A., Roslan, S., SCHREIBER, A. W., Gregory, P. A., & Goodall, G. J. (2015) · Cell · doi:10.1016/j.cell.2015.02.014 · Cited by 2,177 · see citing works
Self-citationCirc-ZNF609 is a circular RNA that can be translated and functions in myogenesis
Legnini, I., Di Timoteo, G., Rossi, F., Morlando, M., Briganti, F., Sthandier, O., Fatica, A., Santini, T., Andronache, A., Wade, M., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.02.017 · Cited by 2,173 · see citing works
The Biogenesis, Functions, and Challenges of Circular RNAs
Li, X., Yang, L. C., & Chen, L. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.034 · Cited by 2,043 · see citing works
Complementary Sequence-Mediated Exon Circularization
Zhang, X.-O., Wang, H.-B., Zhang, Y., Lu, X., Chen, L.-L., & Yang, L. (2014) · Cell · doi:10.1016/j.cell.2014.09.001 · Cited by 1,999 · see citing works
Extensive translation of circular RNAs driven by N6-methyladenosine
Yang, Y., Fan, X., Mao, M., Song, X., Wu, P., Zhang, Y., Jin, Y., Yang, Y., Chen, L.-L., Wang, Y., et al. (2017) · Cell Research · doi:10.1038/cr.2017.31 · Cited by 1,855 · see citing works
Pamudurti, N. R., Bartok, O., Jens, M., Ashwal-Fluss, R., Stottmeister, C., Ruhe, L., Hanan, M., Wyler, E., Perez-Hernandez, D., Ramberger, E., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.02.021 · Cited by 1,810 · see citing works
Expanded identification and characterization of mammalian circular RNAs
Guo, J. U., Agarwal, V., Guo, H., & Bartel, D. P. (2014) · Genome biology · doi:10.1186/s13059-014-0409-z · Cited by 1,578 · see citing works
Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome
Linder, B., Grozhik, A. V., Olarerin-George, A. O., Meydan, C., Mason, C. E., & Jaffrey, S. R. (2015) · Nature Methods · doi:10.1038/nmeth.3453 · Cited by 1,569 · see citing works
Roush, S. F., & Slack, F. J. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.07.007 · Cited by 1,332 · see citing works
Circular RNAs in cancer: opportunities and challenges in the field
Kristensen, L. S., Hansen, T. B., Venø, M. T., & Kjems, J. (2017) · Oncogene · doi:10.1038/onc.2017.361 · Cited by 1,328 · see citing works
Circular RNAs: diversity of form and function
Lasda, E. L., & Parker, R. (2014) · RNA · doi:10.1261/rna.047126.114 · Cited by 1,193 · see citing works
Analysis of Intron Sequences Reveals Hallmarks of Circular RNA Biogenesis in Animals
Ivanov, A., Memczak, S., Wyler, E., Torti, F., Porath, H. T., Orejuela, M. R., Piechotta, M., Levanon, E. Y., Landthaler, M., Dieterich, C., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.12.019 · Cited by 1,092 · see citing works
Markham, N. R., & Zuker, M. (2008) · Methods in molecular biology · doi:10.1007/978-1-60327-429-6_1 · Cited by 1,026 · see citing works
Electron microscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells
HSU, M.-T., & COCA-PRADOS, M. (1979) · Nature · doi:10.1038/280339a0 · Cited by 1,021 · see citing works
Westholm, J. O., Miura, P., Olson, S., Shenker, S., Joseph, B. J., Sanfilippo, P., Celniker, S., Graveley, B. R., & Lai, E. C. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.10.062 · Cited by 1,001 · see citing works
Identification of novel transcripts in annotated genomes using RNA-Seq
Roberts, A., Pimentel, H., Trapnell, C., & Pachter, L. S. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr355 · Cited by 963 · see citing works
Short intronic repeat sequences facilitate circular RNA productionPreprint
Liang, D., & Wilusz, J. E. (2014) · Genes & Development · doi:10.1101/gad.251926.114 · Cited by 959 · see citing works
Nigro, J. M., Cho, K. R., Fearon, E. R., Kern, S. E., Ruppert, J. M., Oliner, J., Kinzler, K. W., & Vogelstein, B. (1991) · Cell · doi:10.1016/0092-8674(91)90244-s · Cited by 888 · see citing works
Getting up to speed with transcription elongation by RNA polymerase II
Jonkers, I., & Lis, J. T. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3953 · Cited by 876 · see citing works
TopHat-Fusion: an algorithm for discovery of novel fusion transcripts
Kim, D., & Salzberg, S. L. (2011) · Genome biology · doi:10.1186/gb-2011-12-8-r72 · Cited by 806 · see citing works
Circular RNA Expression: Its Potential Regulation and Function
Salzman, J. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.03.002 · Cited by 805 · see citing works
Exon Circularization Requires Canonical Splice Signals
Starke, S., Jost, I., Roßbach, O., Schneider, T. P., Schreiner, S., Hung, L.-H., & Bindereif, A. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.12.002 · Cited by 768 · see citing works
Initiation of Protein Synthesis by the Eukaryotic Translational Apparatus on Circular RNAs
Chen, C.-Y., & Sarnow, P. (1995) · Science · doi:10.1126/science.7536344 · Cited by 766 · see citing works
Circular RNA Is Expressed across the Eukaryotic Tree of Life
Wang, P. L., Bao, Y., Yee, M., Barrett, S. P., Hogan, G. J., Olsen, M. N., Dinneny, J. R., Brown, P. O., & Salzman, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090859 · Cited by 754 · see citing works
Efficient backsplicing produces translatable circular mRNAs
Wang, Y., & Wang, Z. (2014) · RNA · doi:10.1261/rna.048272.114 · Cited by 665 · see citing works
miR-15a and miR-16-1 in cancer: discovery, function and future perspectives
Aqeilan, R. I., Calin, G. A., & Croce, C. M. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2009.69 · Cited by 650 · see citing works
The Biogenesis of Nascent Circular RNAs
Zhang, Y., Xue, W., Li, X., Zhang, J., Chen, S., Zhang, J.-L., Yang, L., & Chen, L.-L. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.058 · Cited by 643 · see citing works
Jonkers, I., Kwak, H., & Lis, J. T. (2014) · eLife · doi:10.7554/elife.02407 · Cited by 581 · see citing works
Mammalian NET-Seq Reveals Genome-wide Nascent Transcription Coupled to RNA Processing
Nojima, T., Gomes, T., Grosso, A. R. F., Kimura, H., Dye, M. J., Dhir, S., Carmo-Fonseca, M., & Proudfoot, N. J. (2015) · Cell · doi:10.1016/j.cell.2015.03.027 · Cited by 562 · see citing works
Transcriptome-wide discovery of circular RNAs in Archaea
Danan, M., Schwartz, S., Edelheit, S., & Sorek, R. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1009 · Cited by 560 · see citing works
Circular RNAs: Identification, biogenesis and function
Ebbesen, K. K., Kjems, J., & Hansen, T. B. (2015) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2015.07.007 · Cited by 558 · see citing works
TT-seq maps the human transient transcriptome
Schwalb, B., Michel, M., Zacher, B., Frühauf, K., Demel, C., Tresch, A., Gagneur, J., & Cramer, P. (2016) · Science · doi:10.1126/science.aad9841 · Cited by 548 · see citing works
Kramer, 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
Spatio-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
Tilgner, H., Knowles, D. G., Johnson, R., Davis, C., Chakrabortty, S. K., Djebali, S., Curado, J., Snyder, M. P., Gingeras, T., & Guigó, R. (2012) · Genome Research · doi:10.1101/gr.134445.111 · Cited by 463 · see citing works
Circular RNAs: splicing’s enigma variations
Hentze, M. W., & Preiss, T. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.53 · Cited by 455 · see citing works
A 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
Zhou, C., Molinié, B., Daneshvar, K., Pondick, J. V., Wang, J., Wittenberghe, N. V., Xing, Y., Giallourakis, C. C., & Mullen, A. C. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.027 · Cited by 430 · 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
Comparison of circular RNA prediction tools
Hansen, T. B., Venø, M. T., Damgaard, C. K., & Kjems, J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1458 · Cited by 397 · see citing works
RNA circularization strategies in vivo and in vitro
Petkovic, S., & Müller, S. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv045 · Cited by 386 · see citing works
Exon Skipping Is Correlated with Exon Circularization
Kelly, S. L., Greenman, C., Cook, P. R., & Papantonis, A. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.02.018 · Cited by 374 · see citing works
Vicens, Q., & Westhof, É. (2014) · Cell · doi:10.1016/j.cell.2014.09.005 · Cited by 374 · see citing works
Mayer, A., di Iulio, J., Maleri, S., Eser, U., Vierstra, J., Reynolds, A., Sandstrom, R., Stamatoyannopoulos, J. A., & Churchman, L. S. (2015) · Cell · doi:10.1016/j.cell.2015.03.010 · Cited by 367 · see citing works
Splicing and transcription touch base: co-transcriptional spliceosome assembly and function
Herzel, L., Ottoz, D. S. M., Alpert, T., & Neugebauer, K. M. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.63 · Cited by 356 · see citing works
Exon and intron definition in pre‐mRNA splicing
Conti, L. D., Baralle, M., & Buratti, E. (2012) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1140 · Cited by 331 · see citing works
Nucleosomes are well positioned in exons and carry characteristic histone modifications
Andersson, R., Enroth, S., Rada-Iglesias, A., Wadelius, C., & Komorowski, J. (2009) · Genome Research · doi:10.1101/gr.092353.109 · Cited by 325 · see citing works
Characterization of circular RNAs in human, mouse and rat hearts
Werfel, S., Nothjunge, S., Schwarzmayr, T., Strom, T.-M., Meitinger, T., & Engelhardt, S. H. (2016) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2016.07.007 · Cited by 306 · see citing works
Tunable protein synthesis by transcript isoforms in human cells
Floor, S. N., & Doudna, J. A. (2016) · eLife · doi:10.7554/elife.10921 · Cited by 265 · see citing works
CLIPdb: a CLIP-seq database for protein-RNA interactions
Yang, Y., Di, C., Hu, B., Zhou, M., Liu, Y., Song, N., Li, Y., Umetsu, J., & Lu, Z. J. (2015) · BMC Genomics · doi:10.1186/s12864-015-1273-2 · Cited by 238 · see citing works
Circular RNA expression profiles and features in human tissues: a study using RNA-seq data
Xu, T., Wu, J., Han, P., Zhao, Z., & Song, X. (2017) · BMC Genomics · doi:10.1186/s12864-017-4029-3 · Cited by 230 · see citing works
Increased complexity of circRNA expression during species evolution
Dong, R., Ma, X.-K., Chen, L., & Yang, L. C. (2016) · RNA Biology · doi:10.1080/15476286.2016.1269999 · Cited by 216 · see citing works
The emerging role of circular RNAs in transcriptome regulation
Huang, S., Yang, B., Chen, B. J., Bliim, N., Ueberham, U., Arendt, T., & Janitz, M. (2017) · Genomics · doi:10.1016/j.ygeno.2017.06.005 · Cited by 207 · see citing works
Circular RNAs in Heart Failure
Devaux, Y., Creemers, E. E., Boon, R. A., Werfel, S., Thum, T., Engelhardt, S. H., Dimmeler, S., & Squire, I. B. (2017) · European Journal of Heart Failure · doi:10.1002/ejhf.801 · Cited by 178 · see citing works
Kristensen, L. S., Okholm, T. L. H., Venø, M. T., & Kjems, J. (2017) · RNA Biology · doi:10.1080/15476286.2017.1409931 · Cited by 170 · see citing works
Inverted repeats are necessary for circularization of the mouse testis Sry transcript
Dubin, R. A., Kazmi, M. A., & D, H. O. M. (1995) · Gene · doi:10.1016/0378-1119(95)00639-7 · Cited by 154 · see citing works
Circular RNAs: Novel Regulators of Neuronal Development
van Rossum, D., Verheijen, B. M., & Pasterkamp, R. J. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00074 · Cited by 137 · see citing works
Biogenesis of circular RNA s and their roles in cardiovascular development and pathology
Li, M., Ding, W., Sun, T., Tariq, M., Xu, T., Li, P., & Wang, J. (2017) · FEBS Journal · doi:10.1111/febs.14191 · Cited by 111 · see citing works
Profiling and Validation of the Circular RNA Repertoire in Adult Murine Hearts
Jakobi, T., Czaja-Hasse, L. F., Reinhardt, R., & Dieterich, C. (2016) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2016.02.003 · Cited by 102 · see citing works
Perfect timing: splicing and transcription rates in living cells
Alpert, T., Herzel, L., & Neugebauer, K. M. (2017) · WIREs RNA · doi:10.1002/wrna.1401 · Cited by 99 · see citing works
Circular RNAs: A Novel Player in Development and Disease of the Central Nervous System
Xie, L., Mao, M., Xiong, K., & Jiang, B. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00354 · Cited by 69 · see citing works
Wang, X., Zhu, X., Zhang, H., Wei, S., Chen, Y., Chen, Y., Wang, F., Fan, X., Han, S., & Wu, G. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.01.126 · Cited by 69 · see citing works
Zhang, H.-D., Jiang, L., Hou, J., Zhou, S., Zhong, S., Zhu, L., Wang, D., Yang, S., He, Y., Mao, C., et al. (2018) · Epigenomics · doi:10.2217/epi-2018-0002 · Cited by 67 · see citing works
An Unchartered Journey for Ribosomes: Circumnavigating Circular RNAs to Produce Proteins
Tatomer, D. C., & Wilusz, J. E. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.03.011 · Cited by 66 · see citing works
Meerson, A., & Yehuda, H. (2016) · BMC Cancer · doi:10.1186/s12885-016-2938-1 · Cited by 64 · see citing works
Circular RNAs: Coding or noncoding?
Schneider, T. P., & Bindereif, A. (2017) · Cell Research · doi:10.1038/cr.2017.70 · Cited by 60 · see citing works
Liu, J., Kong, F., Lou, S., Yang, D., & Gu, L. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.08.154 · Cited by 50 · see citing works
Moehle, E. A., Braberg, H., Krogan, N. J., & Guthrie, C. (2014) · RNA Biology · doi:10.4161/rna.28646 · Cited by 46 · see citing works
Chen, G., Wang, Q., Yang, Q., Li, Z., Du, Z., Ren, M., Zhao, H., Song, Y., & Zhang, G. (2018) · PLoS ONE · doi:10.1371/journal.pone.0202896 · Cited by 45 · see citing works
miR-4443 Participates in the Malignancy of Breast Cancer
Chen, X., Zhong, S., Lü, P., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0160780 · Cited by 40 · see citing works
Spliceosome Profiling Visualizes Operations of a Dynamic RNP at Nucleotide Resolution
Burke, J. E., Longhurst, A. D., Merkurjev, D., Sales-Lee, J., Rao, B., Moresco, J. J., Yates, J. R., Li, J. J., & Madhani, H. D. (2018) · Cell · doi:10.1016/j.cell.2018.03.020 · Cited by 38 · see citing works
Andergassen, D., Dotter, C. P., Kuliński, T. M., Guenzl, P. M., Bammer, P. C., Barlow, D. P., Pauler, F. M., & Hudson, Q. J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv727 · Cited by 37 · see citing works
Zhang, W., Qiao, B., & Fan, J. (2018) · Die Pharmazie · doi:10.31083/ph.2018.8313 · Cited by 32 · see citing works
Qi, Y., Zhou, Y., Chen, X., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01440 · Cited by 26 · see citing works
Scherer, S. (2010) · Medical Entomology and Zoology · Cited by 22 · see citing works
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RNA polymerase II speed: a key player in controlling and adapting transcriptome composition
Muniz, L., Nicolas, E., & Trouche, D. (2021) · The EMBO Journal · doi:10.15252/embj.2020105740 · Cited by 203 · see citing works
“Indeed, the average RNA Pol II velocity is higher on genes producing circRNAs than on genes not producing circRNAs (Zhang et al , 2016) and especially on introns of these genes (Ragan et al , 2019).”
- Authors
- Ragan, C., Goodall, G. J., Shirokikh, N. E., & Preiss, T.
- Affiliations
- Australian National University (AU)
- South Australia Pathology (AU)
- Corresponding author
- Shirokikh, Nikolay E.
- Preiss, Thomas
- Venue
- Scientific Reports
- Published
- 2019-02-14
- Volume
- 9
- Issue
- 1
- Pages
- 2048-2048
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC6376117
- OpenAlex
- W2914866051
- Cited by
- 137
- References
- 88
- Citations by year
- 2026: 1 · 2025: 18 · 2024: 14 · 2023: 20 · 2022: 15 · 2021: 31 · 2020: 26 · 2019: 12
- FWCI
- 6.95
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- ANU Open Research (Australian National University) (submittedVersion, cc-by)
- UniSA Research Outputs Repository (University of South Australia) (submittedVersion, other-oa)
- Funders
- Department of Health | National Health and Medical Research Council (GNT1126711)
- Department of Education and Training | Australian Research Council (DP130101928, DP180100111)
- 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 › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- circRNA biogenesis, back-splicing, circRNA translation, microRNA sponge, RNA polymerase II occupancy, transcriptional dynamics, exon length
- MeSH terms
- RNA, Circular, Animals, Base Sequence, Exons, Humans, Introns, RNA, RNA Splicing, Alternative Splicing, Databases, Genetic, MicroRNAs, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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