Co-transcriptional splicing regulates 3′ end cleavage during mammalian erythropoiesis
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Abstract
Pre-mRNA processing steps are tightly coordinated with transcription in many organisms. To determine how co-transcriptional splicing is integrated with transcription elongation and 3' end formation in mammalian cells, we performed long-read sequencing of individual nascent RNAs and precision run-on sequencing (PRO-seq) during mouse erythropoiesis. Splicing was not accompanied by transcriptional pausing and was detected when RNA polymerase II (Pol II) was within 75-300 nucleotides of 3' splice sites (3'SSs), often during transcription of the downstream exon. Interestingly, several hundred introns displayed abundant splicing intermediates, suggesting that splicing delays can take place between the two catalytic steps. Overall, splicing efficiencies were correlated among introns within the same transcript, and intron retention was associated with inefficient 3' end cleavage. Remarkably, a thalassemia patient-derived mutation introducing a cryptic 3'SS improved both splicing and 3' end cleavage of individual β-globin transcripts, demonstrating functional coupling between the two co-transcriptional processes as a determinant of productive gene output.
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PRO-seq was conducted largely according to published protocols, with slight modifications.
“Pro-seq was conducted largely according to published protocols with slight modifications (Reimer et al., 2021).”
From Mapping information-rich genotype-phenotype landscapes with genome-scale Perturb-seq (2022) · cites this paper as Reimer et al., 2021
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The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · 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
Cutadapt removes adapter sequences from high-throughput sequencing reads
Martin, M. (2011) · EMBnet.journal · doi:10.14806/ej.17.1.200 · Cited by 33,889 · 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
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
Minimap2: Pairwise alignment for nucleotide sequences
Li, H. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty191 · Cited by 14,807 · see citing works
deepTools2: a next generation web server for deep-sequencing data analysis
Ramírez, F., Ryan, D. P., Grüning, B., Bhardwaj, V., Kilpert, F., Richter, A. S., Heyne, S., Dündar, F., & Manke, T. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw257 · Cited by 8,096 · see citing works
Initial sequencing and comparative analysis of the mouse genome
Mouse Genome Sequencing Consortium (2002) · Nature · doi:10.1038/nature01262 · Cited by 7,187 · see citing works
Quality control and preprocessing of metagenomic datasets
Schmieder, R., & Edwards, R. A. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr026 · Cited by 4,989 · see citing works
Maximum Entropy Modeling of Short Sequence Motifs with Applications to RNA Splicing Signals
Yeo, G. W.-M., & Burge, C. B. (2004) · Journal of Computational Biology · doi:10.1089/1066527041410418 · Cited by 2,042 · see citing works
Nascent RNA Sequencing Reveals Widespread Pausing and Divergent Initiation at Human Promoters
Core, L. J., Waterfall, J. J., & Lis, J. T. (2008) · Science · doi:10.1126/science.1162228 · Cited by 1,986 · see citing works
The Encyclopedia of DNA elements (ENCODE): data portal update
Davis, C. A., Hitz, B. C., Sloan, C. A., Chan, E. T., Davidson, J. M., Gabdank, I., Hilton, J. A., Jain, K., Baymuradov, U. K., Narayanan, A. K., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gkx1081 · Cited by 1,717 · see citing works
Alternative splicing as a regulator of development and tissue identity
Baralle, F. E., & Giudice, J. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.27 · Cited by 1,333 · see citing works
iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution
König, J., Zarnack, K., Rot, G., Curk, T., Kayikci, M., Zupan, B., Turner, D. J., Luscombe, N. M., & Ule, J. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1838 · Cited by 1,126 · 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
Precise Maps of RNA Polymerase Reveal How Promoters Direct Initiation and Pausing
Kwak, H., Fuda, N. J., Core, L. J., & Lis, J. T. (2013) · Science · doi:10.1126/science.1229386 · Cited by 849 · see citing works
Quality and quantity control of gene expression by nonsense-mediated mRNA decay
Kurosaki, T., Popp, M. W., & Maquat, L. E. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0126-2 · Cited by 834 · see citing works
Coupling mRNA processing with transcription in time and space
Bentley, D. L. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3662 · Cited by 828 · see citing works
Nascent transcript sequencing visualizes transcription at nucleotide resolution
Churchman, L. S., & Weissman, J. S. (2011) · Nature · doi:10.1038/nature09652 · Cited by 823 · see citing works
RNA Splicing by the Spliceosome
Wilkinson, M. E., Charenton, C., & Nagai, K. (2019) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-091719-064225 · Cited by 714 · see citing works
A Slow RNA Polymerase II Affects Alternative Splicing In Vivo
de la Mata, M., Alonso, C. R., Kadener, S., Fededa, J. P., Blaustein, M., Pelisch, F., Cramer, P., Bentley, D., & Kornblihtt, A. R. (2003) · Molecular Cell · doi:10.1016/j.molcel.2003.08.001 · Cited by 683 · see citing works
Jonkers, I., Kwak, H., & Lis, J. T. (2014) · eLife · doi:10.7554/elife.02407 · Cited by 581 · see citing works
Enge, M., Arda, H. E., Mignardi, M., Beausang, J., Bottino, R., Kim, S. K., & Quake, S. R. (2017) · Cell · doi:10.1016/j.cell.2017.09.004 · Cited by 568 · 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
Promoter-proximal pausing of RNA polymerase II: a nexus of gene regulationPreprint
Core, L. J., & Adelman, K. (2019) · Genes & Development · doi:10.1101/gad.325142.119 · Cited by 560 · see citing works
Self-citationMahat, D. B., Kwak, H., Booth, G. T., Jonkers, I. H., Danko, C. G., Patel, R. K., Waters, C. T., Munson, K. M., Core, L. J., & Lis, J. T. (2016) · Nature Protocols · doi:10.1038/nprot.2016.086 · Cited by 492 · see citing works
U1 snRNP Determines mRNA Length and Regulates Isoform Expression
Berg, M. G., Singh, L. N., Younis, I., Liu, Q., Pinto, A. M., Kaida, D., Zhang, Z., Cho, S., Sherrill-Mix, S. A., Wan, L., et al. (2012) · Cell · doi:10.1016/j.cell.2012.05.029 · Cited by 464 · see citing works
An encyclopedia of mouse DNA elements (Mouse ENCODE)
Mouse ENCODE Consortium, Stamatoyannopoulos, J. A., Snyder, M., Hardison, R., Ren, B., Gingeras, T., Gilbert, D. M., Groudine, M., Bender, M., Kaul, R., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-8-418 · Cited by 446 · 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
Global transcriptome analyses of human and murine terminal erythroid differentiation
An, X., Schulz, V., Li, J., Wu, K., Liu, J., Xue, F., Hu, J., Mohandas, N., & Gallagher, P. G. (2014) · Blood · doi:10.1182/blood-2014-01-548305 · Cited by 361 · 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
Self-citationThe Cellular EJC Interactome Reveals Higher-Order mRNP Structure and an EJC-SR Protein Nexus
Singh, G., Küçükural, A., Cenik, C., Leszyk, J., Shaffer, S. A., Weng, Z., & Moore, M. J. (2012) · Cell · doi:10.1016/j.cell.2012.10.007 · Cited by 328 · see citing works
SR proteins are NXF1 adaptors that link alternative RNA processing to mRNA exportPreprint
Müller-McNicoll, M., Botti, V., Domingues, A. M. D. J., Brandl, H., Schwich, O. D., Steiner, M. C., Curk, T., Poser, I., Zarnack, K., & Neugebauer, K. M. (2016) · Genes & Development · doi:10.1101/gad.276477.115 · Cited by 320 · see citing works
Self-citationCo-transcriptional splicing of constitutive and alternative exons
Pandya‐Jones, A., & Black, D. L. (2009) · RNA · doi:10.1261/rna.1714509 · Cited by 300 · see citing works
Identification of a Nuclear Exosome Decay Pathway for Processed Transcripts
Meola, N., Domanski, M., Karadoulama, E., Chen, Y., Gentil, C., Pultz, D., Vitting-Seerup, K., Lykke-Andersen, S., Andersen, J. S., Sandelin, A., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.09.025 · Cited by 290 · see citing works
Pre-mRNA splicing is facilitated by an optimal RNA polymerase II elongation rate
Fong, N., Kim, H., Zhou, Y., Ji, X., Qiu, J., Saldi, T., Diener, K., Jones, K., Fu, X.-D., & Bentley, D. L. (2014) · Genes & Development · doi:10.1101/gad.252106.114 · Cited by 287 · see citing works
Veloso, A., Kirkconnell, K. S., Magnuson, B., Biewen, B., Paulsen, M. T., Wilson, T. E., & Ljungman, M. (2014) · Genome Research · doi:10.1101/gr.171405.113 · Cited by 281 · see citing works
SR Proteins: Binders, Regulators, and Connectors of RNA
Jeong-Yu, S. (2017) · Molecules and Cells · doi:10.14348/molcells.2017.2319 · Cited by 270 · see citing works
Splicing-Dependent RNA Polymerase Pausing in Yeast
Alexander, R. D., Innocente, S. A., Barrass, J. D., & Beggs, J. D. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.11.005 · Cited by 251 · see citing works
Global impact of RNA polymerase II elongation inhibition on alternative splicing regulationPreprint
Ip, J. Y. Y., Schmidt, D., Pan, Q., Ramani, A. K., Fraser, A. G., Odom, D. T., & Blencowe, B. J. (2010) · Genome Research · doi:10.1101/gr.111070.110 · Cited by 237 · see citing works
Splicing Kinetics and Coordination Revealed by Direct Nascent RNA Sequencing through Nanopores
Drexler, H. L., Choquet, K., & Churchman, L. S. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.11.017 · Cited by 234 · see citing works
Wuarin, J., & Schibler, U. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.11.7219 · Cited by 233 · see citing works
Kinetic competition during the transcription cycle results in stochastic RNA processing
Coulon, A., Ferguson, M., de Turris, V., Palangat, M., Chow, C. C., & Larson, D. R. (2014) · eLife · doi:10.7554/elife.03939 · Cited by 228 · see citing works
Base substitution in an intervening sequence of a beta+-thalassemic human globin gene.
Spritz, R. A., Jagadeeswaran, P., Choudary, P. V., Biro, P. A., Elder, J. T., deRiel, J. K., Manley, J. L., Gefter, M. L., Forget, B. G., & Weissman, S. M. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.4.2455 · Cited by 227 · see citing works
Molecular Mechanisms for CFIm-Mediated Regulation of mRNA Alternative Polyadenylation
Zhu, Y., Wang, X., Forouzmand, E., Jeong, J., Qiao, F., Sowd, G. A., Engelman, A., Xie, X. S., Hertel, K. J., & Shi, Y. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.11.031 · Cited by 221 · see citing works
Inefficient processing impairs release of RNA from the site of transcription
Custódio, N., Carmo‐Fonseca, M., Geraghty, F., Periera, H. S., Grosveld, F. G., & Antoniou, M. N. (1999) · The EMBO Journal · doi:10.1093/emboj/18.10.2855 · Cited by 220 · see citing works
Splicing of Nascent RNA Coincides with Intron Exit from RNA Polymerase II
Oesterreich, F. C., Herzel, L., Straube, K., Hujer, K., Howard, J., & Neugebauer, K. M. (2016) · Cell · doi:10.1016/j.cell.2016.02.045 · Cited by 218 · see citing works
Self-citationWidespread Inducible Transcription Downstream of Human Genes
Vilborg, A., Passarelli, M. C., Yario, T. A., Tycowski, K. T., & Steitz, J. A. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.06.016 · Cited by 206 · see citing works
The roles of RNA processing in translating genotype to phenotype
Manning, K. S., & Cooper, T. A. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.139 · Cited by 206 · see citing works
Live-Cell Visualization of Pre-mRNA Splicing with Single-Molecule Sensitivity
Martin, R. M., Rino, J., Carvalho, C., Kirchhausen, T., & Carmo-Fonseca, M. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.08.013 · Cited by 173 · see citing works
Recursive splicing in long vertebrate genes
Sibley, C. R., Emmett, W., Blázquez, L., Faro, A., Haberman, N., Briese, M., Trabzuni, D., Ryten, M., Weale, M. E., Hardy, J., et al. (2015) · Nature · doi:10.1038/nature14466 · Cited by 165 · see citing works
Analysis of the stimulatory effect of splicing on mRNA production and utilization in mammalian cells
Lu, S., & Cullen, B. R. (2003) · RNA · doi:10.1261/rna.5260303 · Cited by 163 · see citing works
Terminal Exon Definition Occurs Cotranscriptionally and Promotes Termination of RNA Polymerase II
Dye, M. J., & Proudfoot, N. J. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80464-5 · Cited by 159 · see citing works
Miccio, A., Cesari, R., Lotti, F., Rossi, C., Sanvito, F., Ponzoni, M., Routledge, S. J. E., Chow, C.-M., Antoniou, M. N., & Ferrari, G. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711666105 · Cited by 154 · see citing works
Grosso, A. R., Leite, A. P., Carvalho, S., Matos, M. R., Martins, F. B., Vítor, A. C., Desterro, J. M., Carmo-Fonseca, M., & de Almeida, S. F. (2015) · eLife · doi:10.7554/elife.09214 · Cited by 152 · see citing works
“Nought May Endure but Mutability”: Spliceosome Dynamics and the Regulation of Splicing
Smith, D. J., Query, C. C., & Konarska, M. M. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.04.013 · Cited by 149 · see citing works
Nojima, T., Rebelo, K., Gomes, T., Grosso, A. R., Proudfoot, N. J., & Carmo‐Fonseca, M. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.09.004 · Cited by 146 · see citing works
From Structure to Systems: High-Resolution, Quantitative Genetic Analysis of RNA Polymerase II
Braberg, H., Jin, H., Moehle, E. A., Chan, Y. A., Wang, S., Shales, M., Benschop, J. J., Morris, J. H., Qiu, C., Hu, F., et al. (2013) · Cell · doi:10.1016/j.cell.2013.07.033 · Cited by 143 · see citing works
Pause locally, splice globally
Oesterreich, F. C., Bieberstein, N. I., & Neugebauer, K. M. (2011) · Trends in Cell Biology · doi:10.1016/j.tcb.2011.03.002 · Cited by 131 · see citing works
Self-citationComparative analysis reveals genomic features of stress-induced transcriptional readthrough
Vilborg, A., Sabath, N., Wiesel, Y., Nathans, J., Levy-Adam, F., Yario, T. A., Steitz, J. A., & Shalgi, R. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1711120114 · Cited by 131 · see citing works
Sheridan, R. M., Fong, N., D’Alessandro, A., & Bentley, D. L. (2019) · Molecular Cell · doi:10.1016/j.molcel.2018.10.031 · Cited by 123 · see citing works
Testa, S. M., Disney, M. D., Turner, D. H., & Kierzek, R. (1999) · Biochemistry · doi:10.1021/bi991187d · Cited by 122 · see citing works
Fica, S. M., Oubridge, C., Wilkinson, M. E., Newman, A. J., & Nagai, K. (2019) · Science · doi:10.1126/science.aaw5569 · Cited by 118 · see citing works
Wuarin, J., & Schibler, U. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.11.7219-7225.1994 · Cited by 117 · see citing works
So, B. R., Di, C., Cai, Z., Venters, C. C., Guo, J., Oh, J., Arai, C., & Dreyfuss, G. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.08.007 · Cited by 116 · see citing works
The fission yeast MTREC complex targets CUTs and unspliced pre-mRNAs to the nuclear exosome
Zhou, Y., Zhu, J., Schermann, G., Ohle, C., Bendrin, K., Sugioka-Sugiyama, R., Sugiyama, T., & Fischer, T. (2015) · Nature Communications · doi:10.1038/ncomms8050 · Cited by 113 · see citing works
Mechanistic insights into mRNA 3′-end processing
Kumar, A., Clerici, M., Muckenfuss, L. M., Passmore, L. A., & Jínek, M. (2019) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2019.08.001 · Cited by 110 · see citing works
Transcription rate strongly affects splicing fidelity and cotranscriptionality in budding yeast
Aslanzadeh, V., Huang, Y., Sanguinetti, G., & Beggs, J. D. (2018) · Genome Research · doi:10.1101/gr.225615.117 · Cited by 109 · see citing works
Long-read sequencing of nascent RNA reveals coupling among RNA processing eventsPreprint
Herzel, L., Straube, K., & Neugebauer, K. M. (2018) · Genome Research · doi:10.1101/gr.232025.117 · Cited by 107 · see citing works
Self-citationCooke, C., Hans, H. H., & Alwine, J. C. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.7.4971 · Cited by 93 · see citing works
Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation
Schor, I. E., Fiszbein, A., Petrillo, E., & Kornblihtt, A. R. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.167 · Cited by 90 · see citing works
Antoniou, M. N. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.3.721 · Cited by 90 · see citing works
A Splicing-Dependent Transcriptional Checkpoint Associated with Prespliceosome Formation
Chathoth, K. T., Barrass, J. D., Webb, S., & Beggs, J. D. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.01.017 · Cited by 84 · see citing works
Spliceosome assembly is coupled to RNA polymerase II dynamics at the 3′ end of human genes
Martins, S., Rino, J., Carvalho, T., Carvalho, C., Yoshida, M., Klose, J. M., de Almeida, S. F., & Carmo‐Fonseca, M. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2124 · Cited by 80 · see citing works
Determinants of RNA metabolism in the Schizosaccharomyces pombe genome
Eser, P., Wachutka, L., Maier, K. C., Demel, C., Boroni, M., Iyer, S., Cramer, P., & Gagneur, J. (2016) · Molecular Systems Biology · doi:10.15252/msb.20156526 · Cited by 80 · see citing works
Guo, L., Adams, R. L., Wan, H., Huston, N. C., Potapova, O., Olson, S., Gallardo, C. M., Graveley, B. R., Torbett, B. E., & Pyle, A. M. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.03.022 · Cited by 78 · see citing works
Nascent RNA and the Coordination of Splicing with TranscriptionPreprint
Neugebauer, K. M. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a032227 · Cited by 77 · see citing works
Self-citationPosition-dependent inhibition of the cleavage step of pre-mRNA 3′-end processing by U1 snRNP
Vagner, S., Rüegsegger, U., Gunderson, S., KELLER, W., & Mattaj, I. W. (2000) · RNA · doi:10.1017/s1355838200991854 · Cited by 76 · see citing works
Microfluidic isoform sequencing shows widespread splicing coordination in the human transcriptome
Tilgner, H., Jahanbani, F., Gupta, I., Collier, P., Wei, E., Rasmussen, M., & Snyder, M. (2018) · Genome Research · doi:10.1101/gr.230516.117 · Cited by 71 · see citing works
Widespread intra-dependencies in the removal of introns from human transcripts
Kim, S. W., Taggart, A. J., Heintzelman, C., Cygan, K. J., Hull, C. G., Wang, J., Shrestha, B., & Fairbrother, W. G. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx661 · Cited by 61 · see citing works
Muniz, L., Deb, M. K., Aguirrebengoa, M., Lazorthes, S., Trouche, D., & Nicolas, E. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.11.006 · Cited by 56 · see citing works
Alexander, R. D., Barrass, J. D., Dichtl, B. S., Koš, M., Obtułowicz, T., Robert, M.-C., Koper, M., Karkusiewicz, I., Mariconti, L., Tollervey, D. W., et al. (2010) · RNA · doi:10.1261/rna.2162610 · Cited by 53 · see citing works
Co-transcriptional splicing and the CTD code
Custódio, N., & Carmo‐Fonseca, M. (2016) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2016.1230086 · Cited by 50 · see citing works
A Detailed Protocol for Subcellular RNA Sequencing (subRNA‐seq)
Mayer, A., & Churchman, L. S. (2017) · Current Protocols in Molecular Biology · doi:10.1002/cpmb.44 · Cited by 48 · see citing works
Induction of Erythroid-Specific Expression in Murine Erythroleukemia (MEL) Cell Lines
Antoniou, M. N. (2003) · Humana Press eBooks · doi:10.1385/0-89603-178-0:421 · Cited by 47 · see citing works
Pai, A. A., & Luca, F. (2018) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1503 · Cited by 47 · see citing works
RNA structure in splicing: An evolutionary perspective
Lin, C., Taggart, A. J., & Fairbrother, W. G. (2016) · RNA Biology · doi:10.1080/15476286.2016.1208893 · Cited by 44 · see citing works
Alpert, T., Straube, K., Oesterreich, F. C., Herzel, L., & Neugebauer, K. M. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108324 · Cited by 39 · see citing works
Self-citationSpliceosome 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
Humanized β-Thalassemia Mouse Model Containing the Common IVSI-110 Splicing Mutation
Vadolas, J., Nefedov, M. D., Wardan, H., Mansooriderakshan, S., Voullaire, L. E., Jamsai, D., Williamson, R., & Ioannou, P. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m512931200 · Cited by 35 · see citing works
The Cellular EJC Interactome Reveals Higher-Order mRNP Structure and an EJC-SR Protein Nexus
Singh, G., Küçükural, A., Cenik, C., Leszyk, J., Shaffer, S. A., Weng, Z., & Moore, M. J. (2012) · Cell · doi:10.1016/j.cell.2012.10.032 · Cited by 34 · see citing works
How do messenger RNA splicing alterations drive myelodysplasia?
Joshi, P. M., Halene, S., & Abdel-Wahab, O. I. (2017) · Blood · doi:10.1182/blood-2017-02-692715 · Cited by 32 · see citing works
Splicing-coupled 3′ end formation requires a terminal splice acceptor site, but not intron excision
Davidson, L., & West, S. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt446 · Cited by 31 · see citing works
Transcriptome-wide Interrogation of the Functional Intronome by Spliceosome Profiling
Chen, W., Moore, J. E., Özadam, H., Shulha, H. P., Rhind, N., Weng, Z., & Moore, M. J. (2018) · Cell · doi:10.1016/j.cell.2018.03.062 · Cited by 29 · see citing works
Numerous recursive sites contribute to accuracy of splicing in long introns in flies
Pai, A. A., Paggi, J. M., Yan, P., Adelman, K., & Burge, C. B. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007588 · Cited by 26 · see citing works
Self-citationMilligan, L., Sayou, C., Tuck, A., Auchynnikava, T., Reid, J. E., Alexander, R., Alves, F. D. L., Allshire, R., Spanos, C., Rappsilber, J., et al. (2017) · eLife · doi:10.7554/elife.27082 · Cited by 23 · see citing works
Castillo-Guzman, D., Hartono, S. R., Frederick, M. H., Sanz, L. A., Sereiva, T., & Chedin, F. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.08.130583 · Cited by 20 · see citing works
Patsali, P., Papasavva, P. L., Stephanou, C., Christou, S., Sitarou, M., Antoniou, M. N., Lederer, C. W., & Kleanthous, M. (2018) · Haematologica · doi:10.3324/haematol.2018.189357 · Cited by 17 · see citing works
A potential mechanism underlying U1 snRNP inhibition of the cleavage step of mRNA 3’ processing
Deng, Y., Shi, J., Ran, Y., Xiang, A. P., & Yao, C. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.06.092 · Cited by 12 · see citing works
Preparation of Mammalian Nascent RNA for Long Read Sequencing
Reimer, K. A., & Neugebauer, K. M. (2020) · Current Protocols in Molecular Biology · doi:10.1002/cpmb.128 · Cited by 12 · see citing works
Self-citationBlood Relatives: Splicing Mechanisms underlying Erythropoiesis in Health and Disease
Reimer, K. A., & Neugebauer, K. M. (2018) · F1000Research · doi:10.12688/f1000research.15442.1 · Cited by 9 · see citing works
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Mapping information-rich genotype-phenotype landscapes with genome-scale Perturb-seq
Replogle, J. M., Saunders, R. A., Pogson, A. N., Hussmann, J. A., Lenail, A., Guna, A., Mascibroda, L., Wagner, E. J., Adelman, K., Lithwick-Yanai, G., et al. (2022) · Cell · doi:10.1016/j.cell.2022.05.013 · Cited by 751 · see citing works
Self-citationMechanisms of lncRNA biogenesis as revealed by nascent transcriptomics
Nojima, T., & Proudfoot, N. J. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00447-6 · Cited by 424 · see citing works
Transcription factors interact with RNA to regulate genes
Oksuz, O., Henninger, J. E., Warneford-Thomson, R., Zheng, M. M., Erb, H., Vancura, A., Overholt, K. J., Hawken, S. W., Banani, S. F., Lauman, R., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.06.012 · Cited by 275 · see citing works
Regulation of pre-mRNA splicing: roles in physiology and disease, and therapeutic prospects
Rogalska, M. E., Vivori, C., & Valcárcel, J. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00556-8 · Cited by 269 · see citing works
Genome organization around nuclear speckles drives mRNA splicing efficiency
Bhat, P., Chow, A. Y., Emert, B. L., Ettlin, O., Quinodoz, S. A., Strehle, M. M., Takei, Y., Burr, A., Goronzy, I. N., Chen, A. W., et al. (2024) · Nature · doi:10.1038/s41586-024-07429-6 · Cited by 182 · see citing works
Mutant NPM1 Directly Regulates Oncogenic Transcription in Acute Myeloid Leukemia
Uckelmann, H. J., Haarer, E. L., Takeda, R., Wong, E. M. C., Hatton, C., Marinaccio, C., Perner, F., Rajput, M., Antonissen, N. J. C., Wen, Y., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-0366 · Cited by 135 · see citing works
Stein, C. B., Field, A. R., Mimoso, C. A., Zhao, C., Huang, K.-L., Wagner, E. J., & Adelman, K. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.10.004 · Cited by 116 · see citing works
Self-citationSingle-nuclei isoform RNA sequencing unlocks barcoded exon connectivity in frozen brain tissue
Hardwick, S. A., Hu, W., Joglekar, A., Fan, L., Collier, P. G., Foord, C., Balacco, J., Lanjewar, S., Sampson, M. M., Koopmans, F., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-022-01231-3 · Cited by 119 · see citing works
Transcriptomics in the era of long-read sequencing
Monzó, C., Liu, T.-Y., & Conesa, A. (2025) · Nature reviews genetics · doi:10.1038/s41576-025-00828-z · Cited by 110 · see citing works
POINT technology illuminates the processing of polymerase-associated intact nascent transcripts
Sousa‐Luís, R., Dujardin, G., Zukher, I., Kimurâ, H., Weldon, C., Carmo‐Fonseca, M., Proudfoot, N. J., & Nojima, T. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.02.034 · Cited by 94 · see citing works
3′-End Processing of Eukaryotic mRNA: Machinery, Regulation, and Impact on Gene Expression
Boreikaitė, V., & Passmore, L. A. (2023) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052521-012445 · Cited by 95 · see citing works
Sites of Transcription Initiation Drive mRNA Isoform Selection
Alfonso-Gonzalez, C., Legnini, I., Holec, S., Arrigoni, L., Ozbulut, H. C., Mateos, F., Koppstein, D., Rybak‐Wolf, A., Bönisch, U., Rajewsky, N., et al. (2022) · Cell · doi:10.1016/j.cell.2023.04.012 · Cited by 95 · see citing works
Co-transcriptional gene regulation in eukaryotes and prokaryotes
Shine, M., Gordon, J. M., Schärfen, L., Zigáčková, D., Herzel, L., & Neugebauer, K. M. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00706-2 · Cited by 95 · see citing works
Self-citationU1 snRNP increases RNA Pol II elongation rate to enable synthesis of long genes
Mimoso, C. A., & Adelman, K. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.03.002 · Cited by 92 · see citing works
Self-citationPre-mRNA splicing and its cotranscriptional connections
Shenasa, H., & Bentley, D. L. (2023) · Trends in Genetics · doi:10.1016/j.tig.2023.04.008 · Cited by 84 · see citing works
The regulation and function of post-transcriptional RNA splicing
Choquet, K., Patop, I. L., & Churchman, L. S. (2025) · Nature Reviews Genetics · doi:10.1038/s41576-025-00836-z · Cited by 71 · see citing works
HIF regulates multiple translated endogenous retroviruses: Implications for cancer immunotherapy
Jiang, Q., Braun, D. A., Clauser, K. R., Ramesh, V., Shirole, N. H., Duke-Cohan, J. E., Nabilsi, N., Kramer, N. J., Forman, C., Lippincott, I. E., et al. (2025) · Cell · doi:10.1016/j.cell.2025.01.046 · Cited by 68 · see citing works
Ietswaart, R., Smalec, B. M., Xu, A., Choquet, K., McShane, E., Jowhar, Z. M., Guegler, C. K., Baxter-Koenigs, A. R., West, E. R., Fu, B. X. H., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.06.008 · Cited by 83 · see citing works
A ubiquitous disordered protein interaction module orchestrates transcription elongation
Čermáková, K., Demeulemeester, J., Lux, V., Nedomova, M., Goldman, S. R., Smith, E. A., Srb, P., Hexnerova, R., Fábry, M., Mádlíková, M., et al. (2021) · Science · doi:10.1126/science.abe2913 · Cited by 67 · see citing works
Self-citationOlsen, S., Godfrey, L. J., Healy, J., Choi, Y., Kai, Y., Hatton, C., Perner, F., Haarer, E., Nabet, B., Yuan, G.-C., et al. (2022) · Molecules and Cells · doi:10.1016/j.molcel.2022.02.013 · Cited by 58 · see citing works
HSFs drive transcription of distinct genes and enhancers during oxidative stress and heat shock
Himanen, S. V., Puustinen, M. C., Silva, A. J. D., Vihervaara, A., & Sistonen, L. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac493 · Cited by 54 · see citing works
Profiling the epigenome using long-read sequencing
Liu, T., & Conesa, A. (2025) · Nature Genetics · doi:10.1038/s41588-024-02038-5 · Cited by 57 · see citing works
Transcription Regulation Through Nascent RNA Folding
Schärfen, L., & Neugebauer, K. M. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.166975 · Cited by 54 · see citing works
Self-citationAsada, K., Kaneko, S., Takasawa, K., Machino, H., Takahashi, S., Shinkai, N., Shimoyama, R., Komatsu, M., & Hamamoto, R. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.666937 · Cited by 54 · see citing works
Long, Y., Jia, J., Mo, W., Jin, X., & Zhai, J. (2021) · Nature Protocols · doi:10.1038/s41596-021-00581-7 · Cited by 51 · see citing works
Zimmer, J. T., Rosa-Mercado, N. A., Canzio, D., STEITZ, J. A., & Simon, M. D. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.08.019 · Cited by 48 · see citing works
Zeng, Y., Fair, B. J., Zeng, H., Krishnamohan, A., Hou, Y., Hall, J. M., Ruthenburg, A. J., Li, Y., & Staley, J. P. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.11.004 · Cited by 51 · see citing works
Vlaming, H., Mimoso, C. A., Field, A. R., Martin, B. J. E., & Adelman, K. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00785-9 · Cited by 49 · see citing works
Self-citationControl of mammalian gene expression by modulation of polyA signal cleavage at 5′ UTR
Luo, L., Jea, J. D.-Y., Wang, Y., Chao, P.-W., & Yen, L. (2024) · Nature Biotechnology · doi:10.1038/s41587-023-01989-0 · Cited by 50 · see citing works
Introns: the “dark matter” of the eukaryotic genome
Girardini, K. N., Olthof, A. M., & Kanadia, R. (2023) · Frontiers in Genetics · doi:10.3389/fgene.2023.1150212 · Cited by 46 · see citing works
Who let the DoGs out? – biogenesis of stress-induced readthrough transcripts
Rosa-Mercado, N. A., & STEITZ, J. A. (2021) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2021.08.003 · Cited by 44 · see citing works
Co-transcriptional genome surveillance by HUSH is coupled to termination machinery
Spencley, A. L., Bar, S., Swigut, T., Flynn, R. A., Lee, C. H., Chen, L., Bassik, M. C., & Wysocka, J. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.04.014 · Cited by 46 · see citing works
Caldas, P., Luz, M., Baseggio, S., Andrade, R., Sobral, D., & Grosso, A. R. (2024) · Communications Biology · doi:10.1038/s42003-024-05779-5 · Cited by 45 · see citing works
Emerging and re-emerging themes in co-transcriptional pre-mRNA splicing
Carrocci, T. J., & Neugebauer, K. M. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.08.036 · Cited by 44 · see citing works
Self-citationRapid unleashing of macrophage efferocytic capacity via transcriptional pause release
Tufan, T., Cömertpay, G., Villani, A., Nelson, G. M., Terekhova, M., Kelley, S. M., Zakharov, P. N., Ellison, R. M., Shpynov, O., Raymond, M. H., et al. (2024) · Nature · doi:10.1038/s41586-024-07172-y · Cited by 41 · see citing works
From computational models of the splicing code to regulatory mechanisms and therapeutic implications
Capitanchik, C., Wilkins, O. G., Wagner, N., Gagneur, J., & Ule, J. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00774-2 · Cited by 42 · see citing works
Zhang, Z., Bae, B., Dredge, W. H., & Miura, P. (2023) · Nature Communications · doi:10.1038/s41467-023-41207-8 · Cited by 40 · see citing works
Boddu, P. C., Gupta, A. K., Roy, R., Avalos, B. D. L. P., Olazabal‐Herrero, A., Neuenkirchen, N., Zimmer, J. T., Chandhok, N. S., King, D. P., Nannya, Y., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.02.032 · Cited by 39 · see citing works
Self-citationChoquet, K., Baxter‐Koenigs, A. R., Dülk, S.-L., Smalec, B. M., Rouskin, S., & Churchman, L. S. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01035-2 · Cited by 39 · see citing works
Birth of a poly(A) tail: mechanisms and control of mRNA polyadenylation
Rodríguez‐Molina, J. B., & Turtola, M. (2022) · FEBS Open Bio · doi:10.1002/2211-5463.13528 · Cited by 38 · see citing works
The control of polycomb repressive complexes by long noncoding RNAs
Trotman, J. B., Braceros, K. C. A., Cherney, R. E., Murvin, M. M., & Calabrese, J. M. (2021) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1657 · Cited by 37 · see citing works
Biophysical modeling with variational autoencoders for bimodal, single-cell RNA sequencing data
Carilli, M., Gorin, G., Choi, Y., Chari, T., & Pachter, L. S. (2024) · Nature Methods · doi:10.1038/s41592-024-02365-9 · Cited by 33 · see citing works
Rixosomal RNA degradation contributes to silencing of Polycomb target genes
Zhou, H., Stein, C. B., Shafiq, T. A., Shipkovenska, G. G., Kalocsay, M., Paulo, J. A., Zhang, J., Luo, Z., Gygi, S. P., Adelman, K., et al. (2022) · Nature · doi:10.1038/s41586-022-04598-0 · Cited by 36 · see citing works
Self-citationPTBP1-activated co-transcriptional splicing controls epigenetic status of pluripotent stem cells
Iannone, C., Kainov, Y. A., Zhuravskaya, A., Hamid, F., Nojima, T., & Makeyev, E. V. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.12.014 · Cited by 33 · see citing works
Cryo-EM snapshots of the human spliceosome reveal structural adaptions for splicing regulation
Fica, S. M. (2020) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2020.06.018 · Cited by 34 · see citing works
Regulation of bacterial gene expression by non-coding RNA: It is all about time!
Chauvier, A., & Walter, N. G. (2024) · Cell chemical biology · doi:10.1016/j.chembiol.2023.12.011 · Cited by 31 · see citing works
Leader, Y., Lev-Maor, G., Sorek, M., Shayevitch, R., Hussein, M., Hameiri, O., Tammer, L., Zonszain, J., Keydar, I., Hollander, D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24774-6 · Cited by 32 · see citing works
Mo, W., Liu, B., Zhang, H., Jin, X., Lu, D., Yu, Y., Liu, Y., Jia, J., Long, Y., Deng, X. M., et al. (2021) · Genome biology · doi:10.1186/s13059-021-02543-4 · Cited by 30 · see citing works
Nuclear mRNA decay: regulatory networks that control gene expression
Rambout, X., & Maquat, L. E. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00712-2 · Cited by 29 · see citing works
Cotranscriptional splicing efficiencies differ within genes and between cell types
Bedi, K., Magnuson, B., Narayanan, I. V., Paulsen, M. T., Wilson, T. E., & Ljungman, M. E. (2021) · RNA · doi:10.1261/rna.078662.120 · Cited by 28 · see citing works
Morgan, M. A., Shiekhattar, R., Shilatifard, A., & Lauberth, S. M. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.04.008 · Cited by 30 · see citing works
RNA helicase-dependent gene looping impacts messenger RNA processing
Terrone, S., Valat, J., Fontrodona, N., Giraud, G., Claude, J., Combe, E., Lapendry, A., Polvèche, H., Ameur, L. B., Duvermy, A., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac717 · Cited by 25 · see citing works
CTCF blocks antisense transcription initiation at divergent promoters
Luan, J. Y., Vermunt, M. W., Syrett, C. M., Coté, A., Tome, J. M., Zhang, H., Huang, A., Luppino, J. M., Keller, C. A., Giardine, B. M., et al. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00855-y · Cited by 29 · see citing works
Kaye, E. G., Basavaraju, K., Nelson, G. M., Zomer, H. D., Roy, D., Joseph, I. I., Rajabi‐Toustani, R., Qiao, H., Adelman, K., & Reddi, P. P. (2024) · Nature Communications · doi:10.1038/s41467-024-45177-3 · Cited by 28 · see citing works
Self-citationCo-depletion of NIPBL and WAPL balance cohesin activity to correct gene misexpression
Luppino, J. M., Field, A. R., Nguyen, S. C., Park, D. S., Shah, P. P., Abdill, R. J., Lan, Y., Yunker, R., Jain, R., Adelman, K., et al. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010528 · Cited by 31 · see citing works
Self-citationInherited blood cancer predisposition through altered transcription elongation
Zhao, J., Cato, L. D., Arora, U. P., Bao, E. L., Bryant, S. C., Williams, N., Jia, Y., Goldman, S. R., Nangalia, J., Erb, M. A., et al. (2024) · Cell · doi:10.1016/j.cell.2023.12.016 · Cited by 25 · see citing works
miR-430 regulates zygotic mRNA during zebrafish embryogenesis
Amaral, D. B., Egidy, R., Perera, A. G., & Bazzini, A. (2024) · Genome biology · doi:10.1186/s13059-024-03197-8 · Cited by 24 · see citing works
Challenges in identifying mRNA transcript starts and ends from long-read sequencing dataPreprint
Calvo-Roitberg, E., Daniels, R. F., & Pai, A. A. (2024) · Genome Research · doi:10.1101/gr.279559.124 · Cited by 24 · see citing works
Regulation of the Alternative Neural Transcriptome by ELAV/Hu RNA Binding Proteins
Lü, W., & Lai, E. C. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.848626 · Cited by 23 · see citing works
Regulation of gene expression by alternative polyadenylation in health and disease
Tian, B., Yu, S., & Zhang, Q. (2026) · Nature Reviews Genetics · doi:10.1038/s41576-025-00928-w · Cited by 23 · see citing works
Parker, M. T., Knop, K., Barton, G. J., & Simpson, G. G. (2021) · Genome biology · doi:10.1186/s13059-021-02296-0 · Cited by 22 · see citing works
Castillo-Guzman, D., Hartono, S. R., Frederick, M. H., Sanz, L. A., Sereiva, T., & Chedin, F. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.08.130583 · Cited by 20 · see citing works
Regulation of alternative splicing and polyadenylation in neurons
Lee, S., Aubee, J. I., & Lai, E. C. (2023) · Life Science Alliance · doi:10.26508/lsa.202302000 · Cited by 21 · see citing works
Modulation of mRNA 3′-End Processing and Transcription Termination in Virus-Infected Cells
Vijayakumar, A., Park, A., & STEITZ, J. A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.828665 · Cited by 20 · see citing works
Zhang, X., Xu, J., Hu, J., Zhang, S., Hao, Y., Zhang, D., Qian, H., Wang, D., & Fu, X. (2024) · Nature Communications · doi:10.1038/s41467-024-50298-w · Cited by 19 · see citing works
Coupling of co-transcriptional splicing and 3’ end Pol II pausing during termination in Arabidopsis
Zhou, S., Zhao, F., Zhu, D., Zhang, Q., Dai, Z., & Wu, Z. (2023) · Genome biology · doi:10.1186/s13059-023-03050-4 · Cited by 18 · see citing works
Elements at the 5′ end of Xist harbor SPEN-independent transcriptional antiterminator activity
Trotman, J. B., Lee, D. M., Cherney, R. E., Kim, S. O., Inoue, K., Schertzer, M. D., Bischoff, S. R., Cowley, D. O., & Calabrese, J. M. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa789 · Cited by 18 · see citing works
Co-transcriptional splicing efficiency is a gene-specific feature that can be regulated by TGFβ
Sánchez-Escabias, E., Guerrero-Martinez, J. A., & Reyes, J. C. (2022) · Communications Biology · doi:10.1038/s42003-022-03224-z · Cited by 18 · see citing works
Transcription and splicing dynamics during early Drosophila development
Prudêncio, P., Savisaar, R., Rebelo, K., Martinho, R. G., & Carmo‐Fonseca, M. (2021) · RNA · doi:10.1261/rna.078933.121 · Cited by 18 · see citing works
Post-transcriptional splicing can occur in a slow-moving zone around the genePreprint
Coté, A., O’Farrell, A., Dardani, I. P., Dunagin, M. C., Coté, C., Wan, Y., Bayatpour, S., Drexler, H. L., Alexander, K. A., Chen, F., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.06.028092 · Cited by 18 · see citing works
The quantitative impact of 3′UTRs on gene expression
West, J. D., Smith, H. J., Vu, L. T., Fogarty, E. A., Matreyek, K. A., Fowler, D. M., & Grimson, A. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf568 · Cited by 17 · see citing works
Widespread occurrence of hybrid internal-terminal exons in human transcriptomes
Fiszbein, A., McGurk, M. P., Calvo-Roitberg, E., Kim, G., Burge, C. B., & Pai, A. A. (2022) · Science Advances · doi:10.1126/sciadv.abk1752 · Cited by 17 · see citing works
Danckwardt, S., Trégouët, D., & Castoldi, E. (2023) · Cardiovascular Research · doi:10.1093/cvr/cvad046 · Cited by 17 · see citing works
CDK11, a splicing-associated kinase regulating gene expression
Hluchý, M., & Blažek, D. (2024) · Trends in Cell Biology · doi:10.1016/j.tcb.2024.08.004 · Cited by 16 · see citing works
Measuring mRNA Decay with Roadblock‐qPCR
Watson, M. J., & Thoreen, C. C. (2022) · Current Protocols · doi:10.1002/cpz1.344 · Cited by 16 · see citing works
TP63 fusions drive multicomplex enhancer rewiring, lymphomagenesis, and EZH2 dependence
Wu, G., Yoshida, N., Liu, J., Zhang, X., Xiong, Y., Heavican, T. B., Mandato, E., Liu, H., Nelson, G. M., Yang, L., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.adi7244 · Cited by 16 · see citing works
Self-citationHuman histone H1 variants impact splicing outcome by controlling RNA polymerase II elongation
Pascal, C., Zonszain, J., Hameiri, O., Gargi-Levi, C., Lev-Maor, G., Tammer, L., Levy, T., Tarabeih, A., Roy, V. R., Ben-Salmon, S., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.10.003 · Cited by 17 · see citing works
Timing is everything: advances in quantifying splicing kinetics
Merens, H. E., Choquet, K., Baxter‐Koenigs, A. R., & Churchman, L. S. (2024) · Trends in Cell Biology · doi:10.1016/j.tcb.2024.03.007 · Cited by 16 · see citing works
Long non-coding RNAs and splicing
Staněk, D. (2021) · Essays in Biochemistry · doi:10.1042/ebc20200087 · Cited by 16 · see citing works
Gallardo, C. M., de Diego, A. S., Martínez‐A, C., & van Wely, K. H. M. (2021) · Transcription · doi:10.1080/21541264.2021.1959244 · Cited by 15 · see citing works
Gildea, M. A., Dwyer, Z. W., & Pleiss, J. A. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.06.020 · Cited by 15 · see citing works
Erickson, E. C., You, I., Perry, G. E., Dugourd, A. J. F., Donovan, K. A., Crafter, C., Johannes, J. W., Williamson, S. C., Moss, J. I., R�os, S., et al. (2024) · Science Signaling · doi:10.1126/scisignal.adf2670 · Cited by 15 · see citing works
Townley, B. A., Buerer, L., Tsao, N., Bacolla, A., Mansoori, F., Rusanov, T., Clark, N. E., Goodarzi, N., Schmidt, N., Srivatsan, S. N., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.06.011 · Cited by 15 · see citing works
PGC-1α senses the CBC of pre-mRNA to dictate the fate of promoter-proximally paused RNAPII
Rambout, X., Cho, H., Blanc, R., Lyu, Q., Miano, J. M., Chakkalakal, J. V., Nelson, G. M., Yalamanchili, H. K., Adelman, K., & Maquat, L. E. (2023) · Molecular Cell · doi:10.1016/j.molcel.2022.12.022 · Cited by 14 · see citing works
Self-citationPost-transcriptional splicing can occur in a slow-moving zone around the gene
Coté, A., O’Farrell, A., Dardani, I. P., Dunagin, M. C., Coté, C., Wan, Y., Bayatpour, S., Drexler, H. L., Alexander, K. A., Chen, F., et al. (2023) · eLife · doi:10.7554/elife.91357 · Cited by 14 · see citing works
Post-transcriptional splicing can occur in a slow-moving zone around the gene
Coté, A., O’Farrell, A., Dardani, I. P., Dunagin, M. C., Coté, C., Wan, Y., Bayatpour, S., Drexler, H. L., Alexander, K. A., Chen, F., et al. (2024) · eLife · doi:10.7554/elife.91357.3 · Cited by 14 · see citing works
Post-transcriptional regulation of erythropoiesis
Li, Y., Zhang, H., Hu, B., Wang, P., Wang, W., & Liu, J. (2023) · Blood Science · doi:10.1097/bs9.0000000000000159 · Cited by 12 · see citing works
CEBPA repression by MECOM blocks differentiation to drive aggressive leukemias
Fleming, T. J., Antoszewski, M., Lambo, S., Gundry, M. C., Piussi, R., Wahlster, L., Shah, S. B., Reed, F. E., Dong, K. D., Paulo, J. A., et al. (2025) · Blood · doi:10.1182/blood.2025028954 · Cited by 11 · see citing works
Self-citationElucidating the coordination of RNA processing using short-read and long-read RNA-sequencing methods
Alfonso-Gonzalez, C., & Hilgers, V. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-025-00895-4 · Cited by 13 · see citing works
Chen, C. C., Han, J., Chinn, C. A., Rounds, J. S., Li, X., Nikan, M., Myszka, M., Tong, L., Passalacqua, L. F. M., Bredy, T. W., et al. (2024) · eLife · doi:10.7554/elife.90116 · Cited by 10 · see citing works
Co-transcriptional splicing facilitates transcription of gigantic genes
Fingerhut, J. M., Lannes, R., Whitfield, T. W., Thiru, P., & Yamashita, Y. M. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1011241 · Cited by 10 · see citing works
Schärfen, L., Zigáčková, D., Reimer, K. A., Stark, M. R., Slat, V., Francoeur, N. J., Wells, M. L., Zhou, L., Blackshear, P. J., Neugebauer, K. M., et al. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2021.818697 · Cited by 10 · see citing works
Self-citationChen, L., Roake, C. M., Maccallini, P., Bavasso, F., Dehghannasiri, R., Santonicola, P., Mendoza-Ferreira, N., Scatolini, L., Rizzuti, L., Esposito, A., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac659 · Cited by 10 · see citing works
Requirement for Cyclin D1 Underlies Cell-Autonomous HIF2 Dependence in Kidney Cancer
Shirole, N. H., Kesar, D., Lee, Y., Goodale, A. B., Syamala, S., Kukreja, S., Li, R., Qiu, X., Yu, W., Goldman, S. R., et al. (2025) · Cancer Discovery · doi:10.1158/2159-8290.cd-24-1378 · Cited by 9 · see citing works
Self-citationThe RNA revolution in medicine: from gene regulation to clinical therapeutics
Jeong, J., & Jeong-Yu, S. (2025) · Animal Cells and Systems · doi:10.1080/19768354.2025.2548253 · Cited by 9 · see citing works
Regulation of mature mRNA levels by RNA processing efficiency
Henfrey, C., Murphy, S., & Tellier, M. (2022) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqad059 · Cited by 8 · see citing works
Lau, M. S., Hu, Z., Zhao, X., Tan, Y. S., Liu, J., Huang, H. Y., Yeo, C. J., Leong, H. F., Grinchuk, O. V., Chan, J. K., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42078-9 · Cited by 8 · see citing works
Genome-wide characterization of nascent RNA processing in plants
Qin, Y., Long, Y., & Zhai, J. (2022) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2022.102294 · Cited by 8 · see citing works
Podszywalow‐Bartnicka, P., Shine, M., Lin, J., & Neugebauer, K. M. (2026) · Science Advances · doi:10.1126/sciadv.aea2475 · Cited by 7 · see citing works
Self-citationKrug, B., Hu, B., Chen, H., Negrón-Lomas, C., Chen, X., Mouatani, A. E., Gretarsson, K. H., Ptack, A., Deshmukh, S., Kabir, N., et al. (2026) · Nature Genetics · doi:10.1038/s41588-026-02586-y · Cited by 9 · see citing works
- Authors
- Reimer, K. A., Mimoso, C. A., Adelman, K., & Neugebauer, K. M.
- Affiliations
- Yale University (US)
- Harvard University (US)
- Corresponding author
- Neugebauer, Karla M.
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2021-03
- Volume
- 81
- Issue
- 5
- Pages
- 998-1012.e7
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC8038867
- OpenAlex
- W3121080183
- Cited by
- 180
- References
- 102
- Citations by year
- 2026: 21 · 2025: 26 · 2024: 41 · 2023: 31 · 2022: 34 · 2021: 22 · 2020: 5
- FWCI
- 10.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
- Keywords
- co-transcriptional splicing, 3' end cleavage, erythropoiesis, pre-mRNA processing, transcription elongation, RNA polymerase II, 3' splice site, splicing intermediates, intron retention, splicing efficiency, thalassemia, beta-globin, cryptic splice site, nascent RNA
- MeSH terms
- Animals, Base Sequence, Cell Differentiation, Erythropoiesis, Exons, Humans, Introns, Leukocytes, Mutation, RNA Polymerase II, RNA Splicing, beta-Thalassemia, Spliceosomes, RNA Splice Sites, Erythroid Cells, Cell Line, Tumor, Mice, beta-Globins, RNA Cleavage, Transcription Elongation, Genetic
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