CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing
Open accessAbstract
Alternative splicing of pre-messenger RNA is a key feature of transcriptome expansion in eukaryotic cells, yet its regulation is poorly understood. Spliceosome assembly occurs co-transcriptionally, raising the possibility that DNA structure may directly influence alternative splicing. Supporting such an association, recent reports have identified distinct histone methylation patterns, elevated nucleosome occupancy and enriched DNA methylation at exons relative to introns. Moreover, the rate of transcription elongation has been linked to alternative splicing. Here we provide the first evidence that a DNA-binding protein, CCCTC-binding factor (CTCF), can promote inclusion of weak upstream exons by mediating local RNA polymerase II pausing both in a mammalian model system for alternative splicing, CD45, and genome-wide. We further show that CTCF binding to CD45 exon 5 is inhibited by DNA methylation, leading to reciprocal effects on exon 5 inclusion. These findings provide a mechanistic basis for developmental regulation of splicing outcome through heritable epigenetic marks.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The methylation status around spliced exons could affect their inclusion level.
“suggesting that the methylation status surrounding the spliced exons could affect the inclusion level of these exons.”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [112]
CTCF binding to the exon or intron depends on DNA methylation.
“Importantly, the binding of CTCF to the exon or intron was dependent on DNA methylation”
From Transcription factors as readers and effectors of DNA methylation (2016) · cites this paper as [112]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
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
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845 · see citing works
The ENCODE Project Consortium (2007) · Nature · doi:10.1038/nature05874 · Cited by 5,223 · see citing works
Alternative isoform regulation in human tissue transcriptomes
Wang, E. T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S. F., Schroth, G. P., & Burge, C. B. (2008) · Nature · doi:10.1038/nature07509 · Cited by 5,181 · see citing works
Self-citationPan, Q., Shai, O., Lee, L. J., Frey, B. J., & Blencowe, B. J. (2008) · Nature Genetics · doi:10.1038/ng.259 · Cited by 3,951 · see citing works
CTCF: Master Weaver of the Genome
Phillips‐Cremins, J. E., & Corces, V. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.001 · Cited by 1,540 · see citing works
Analysis and design of RNA sequencing experiments for identifying isoform regulation
Katz, Y., Wang, E. T., Airoldi, E. M., & Burge, C. B. (2010) · Nature Methods · doi:10.1038/nmeth.1528 · Cited by 1,353 · see citing works
Understanding alternative splicing: towards a cellular code
Matlin, A. J., Clark, F., & Smith, C. W. J. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1645 · Cited by 1,299 · see citing works
Regulation of Alternative Splicing by Histone Modifications
Luco, R. F., Pan, Q., Tominaga, K., Blencowe, B. J., Pereira‐Smith, O. M., & Misteli, T. (2010) · Science · doi:10.1126/science.1184208 · Cited by 1,099 · see citing works
Analysis of the Vertebrate Insulator Protein CTCF-Binding Sites in the Human Genome
Kim, T. H., Abdullaev, Z., Smith, A. D., Ching, K. A., Loukinov, D. I., Green, R. D., Zhang, M. Q., Lobanenkov, V. V., & Ren, B. (2007) · Cell · doi:10.1016/j.cell.2006.12.048 · Cited by 1,022 · see citing works
CD45: A Critical Regulator of Signaling Thresholds in Immune Cells
Hermiston, M. L., Xu, Z., & Weiss, A. (2003) · Annual Review of Immunology · doi:10.1146/annurev.immunol.21.120601.140946 · Cited by 950 · see citing works
An Abundance of Ubiquitously Expressed Genes Revealed by Tissue Transcriptome Sequence Data
Ramsköld, D., Wang, E. T., Burge, C. B., & Sandberg, R. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000598 · Cited by 820 · see citing works
Self-citationAlternative pre-mRNA splicing regulation in cancer: pathways and programs unhingedPreprint
David, C. J., & Manley, J. L. (2010) · Genes & Development · doi:10.1101/gad.1973010 · Cited by 815 · see citing works
Epigenetics in Alternative Pre-mRNA Splicing
Luco, R. F., Alló, M., Schor, I. E., Kornblihtt, A. R., & Misteli, T. (2011) · Cell · doi:10.1016/j.cell.2010.11.056 · Cited by 783 · see citing works
Progression through the RNA Polymerase II CTD Cycle
Buratowski, S. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.10.019 · Cited by 777 · see citing works
Trowbridge, I. S., & Thomas, M. L. (1994) · Annual Review of Immunology · doi:10.1146/annurev.iy.12.040194.000505 · Cited by 746 · see citing works
The Honey Bee Epigenomes: Differential Methylation of Brain DNA in Queens and Workers
Lyko, F., Foret, S., Kucharski, R., Wolf, S., Falckenhayn, C., & Maleszka, R. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000506 · Cited by 727 · see citing works
Relationship between nucleosome positioning and DNA methylation
Chodavarapu, R. K., Feng, S., Bernatavichute, Y. V., Chen, P., Stroud, H., Yu, Y., Hetzel, J., Kuo, F., Kim, J., Cokus, S. J., et al. (2010) · Nature · doi:10.1038/nature09147 · Cited by 696 · 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
Differential chromatin marking of introns and expressed exons by H3K36me3
Kolasinska-Zwierz, P., Down, T. A., Latorre, I. J., Liu, T., Liu, X. S., & Ahringer, J. (2009) · Nature Genetics · doi:10.1038/ng.322 · Cited by 671 · see citing works
Chromatin organization marks exon-intron structure
Schwartz, S., Meshorer, E., & Ast, G. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1659 · Cited by 638 · see citing works
Aberrant Epigenetic Landscape in Cancer: How Cellular Identity Goes Awry
Berdasco, M., & Esteller, M. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.10.005 · Cited by 623 · see citing works
Filippova, G. N., Fagerlie, S. R., Klenova, E. M., Myers, C. D., Dehner, Y., Goodwin, G. H., Neiman, P. E., Collins, S. J., & Lobanenkov, V. V. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.6.2802 · Cited by 543 · see citing works
Alternative splicing and disease
Tazi, J., Bakkour, N., & Stamm, S. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.09.017 · Cited by 541 · see citing works
Genome-wide identification of<i>in vivo</i>protein-DNA binding sites from ChIP-Seq data
Jothi, R., Cuddapah, S., Barski, A., Cui, K., & Zhao, K. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn488 · Cited by 539 · see citing works
A Practical Approach to Microarray Data Analysis
Wall, M. E., Rechtsteiner, A., & Rocha, L. M. (2003) · Kluwer Academic Publishers eBooks · doi:10.1007/b101875 · Cited by 531 · see citing works
Nucleosome positioning as a determinant of exon recognition
Tilgner, H., Nikolaou, C., Althammer, S., Sammeth, M., Beato, M., Valcárcel, J., & Guigó, R. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1658 · Cited by 446 · see citing works
Biased chromatin signatures around polyadenylation sites and exons
Nielsen, C. B., Padgett, R. A., Spies, N., & Burge, C. B. (2009) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 390 · 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
Methylated DNA Immunoprecipitation (MeDIP)
Mohn, F., Weber, M., Schübeler, D., & Roloff, T. C. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-522-0_5 · Cited by 239 · see citing works
Hodges, E. C., Smith, A. D., Kendall, J., Xuan, Z., Ravi, K., Rooks, M. G., Zhang, M. Q., Ye, K. Q., Bhattacharjee, A., Brizuela, L., et al. (2009) · Genome Research · doi:10.1101/gr.095190.109 · Cited by 236 · see citing works
Jelinic, P., & Shaw, P. H. (2006) · The Journal of Pathology · doi:10.1002/path.2116 · Cited by 231 · see citing works
Building specificity with nonspecific RNA-binding proteins
Singh, R., & Valcárcel, J. (2005) · Nature Structural & Molecular Biology · doi:10.1038/nsmb961 · Cited by 222 · see citing works
Regulation of CD45 Alternative Splicing by Heterogeneous Ribonucleoprotein, hnRNPLL
Oberdoerffer, S., Moita, L. F., Neems, D. S., Freitas, R. P., Hacohen, N., & Rao, A. (2008) · Science · doi:10.1126/science.1157610 · Cited by 205 · see citing works
Self-citationCoupling Transcription and Alternative Splicing
Kornblihtt, A. R. (2007) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-77374-2_11 · Cited by 168 · see citing works
Kireeva, M. L., Nedialkov, Y. A., Cremona, G. H., Purtov, Y. A., Lubkowska, L., Malagón, F., Burton, Z. F., Strathern, J. N., & Kashlev, M. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.04.017 · Cited by 163 · see citing works
Self-citationPre-mRNA splicing: where and when in the nucleus
Han, J., Ji, X., Wang, D., & Fu, X. (2011) · Trends in Cell Biology · doi:10.1016/j.tcb.2011.03.003 · Cited by 163 · see citing works
A wave of nascent transcription on activated human genes
Wada, Y., Ohta, Y., Xu, M., Tsutsumi, S., Minami, T., Inoue, K., Komura, D., Kitakami, J.-I., Oshida, N., Papantonis, A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902573106 · Cited by 152 · see citing works
Critical DNA Binding Interactions of the Insulator Protein CTCF
Renda, M., Baglivo, I., Burgess-Beusse, B. L., Esposito, S., Fattorusso, R., Felsenfeld, G., & Pedone, P. V. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706213200 · Cited by 152 · see citing works
Reciprocal intronic and exonic histone modification regions in humans
Huff, J. T., Plocik, A. M., Guthrie, C., & Yamamoto, K. R. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1924 · Cited by 128 · see citing works
Transcription Elongation through DNA Arrest Sites
Awrey, D. E., Weilbaecher, R. G., Hemming, S. A., et al. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.23.14747 · Cited by 113 · see citing works
SVDMAN—singular value decomposition analysis of microarray data
Wall, M. E., Dyck, P. A., & Brettin, T. S. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.6.566 · Cited by 99 · see citing works
Context-Dependent Regulatory Mechanism of the Splicing Factor hnRNP L
Motta-Mena, L. B., Heyd, F., & Lynch, K. W. (2010) · Molecular Cell · doi:10.1016/j.molcel.2009.12.027 · Cited by 95 · see citing works
OHLSSON, R. I., Bartkuhn, M., & Renkawitz, R. (2010) · Chromosoma · doi:10.1007/s00412-010-0262-0 · Cited by 94 · see citing works
Topp, J. D., Jackson, J., Melton, A. A., & Lynch, K. W. (2008) · RNA · doi:10.1261/rna.1212008 · Cited by 90 · see citing works
Engineering of elongation complexes of bacterial and yeast RNA polymerases.
Komissarova, N., Kireeva, M., Becker, J., Sidorenkov, I., & Kashlev, M. (2003) · Methods in Enzymology · doi:10.1016/s0076-6879(03)71017-9 · Cited by 82 · see citing works
Self-citationTong, A., Nguyen, J., & Lynch, K. W. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508123200 · Cited by 65 · see citing works
Methylated DNA Immunoprecipitation
Thu, K. L., Vucic, E. A., Kennett, J. Y., Heryet, C., Brown, C. J., Lam, W. L., & Wilson, I. M. (2009) · Journal of Visualized Experiments · doi:10.3791/935 · Cited by 51 · see citing works
Chromatin and Alternative SplicingPreprint
Alló, M., Schor, I. E., Muñoz, M. J., de la Mata, M., Agirre, E., Valcárcel, J., Eyras, E., & Kornblihtt, A. R. (2010) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2010.75.023 · Cited by 48 · see citing works
Kireeva, M. L., Lubkowska, L., Komissarova, N. V., et al. (2003) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(03)70012-3 · Cited by 47 · see citing works
CD45RB expression defines two interconvertible subsets of human CD4+ T cells with memory function
Horgan, K. J., Tanaka, Y., Luce, G. E. G., et al. (1994) · European Journal of Immunology · doi:10.1002/eji.1830240536 · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Functions of DNA methylation: islands, start sites, gene bodies and beyond
Jones, P. A. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3230 · Cited by 6,061 · see citing works
The biogenesis, biology and characterization of circular RNAs
Kristensen, L. S., Andersen, M. S., Stagsted, L. V. W., Ebbesen, K. K., Hansen, T. B., & Kjems, J. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0158-7 · Cited by 4,823 · see citing works
DNA methylation: roles in mammalian development
Smith, Z. D., & Meissner, A. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3354 · Cited by 3,045 · see citing works
Function and information content of DNA methylation
Schübeler, D. (2015) · Nature · doi:10.1038/nature14192 · Cited by 2,060 · see citing works
Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells
Ramsköld, D., Luo, S., Wang, Y.-C., Li, R., Deng, Q., Faridani, O. R., Daniels, G. A., Khrebtukova, I., Loring, J. F., Laurent, L. C., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2282 · Cited by 1,609 · see citing works
Self-citationCoupling 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
RNA splicing is a primary link between genetic variation and disease
Li, Y. I., van de Geijn, B., Raj, A., Knowles, D. A., Petti, A. A., Golan, D., Gilad, Y., & Pritchard, J. K. (2016) · Science · doi:10.1126/science.aad9417 · Cited by 660 · see citing works
Transcription factors as readers and effectors of DNA methylation
Zhu, H., Wang, G., & Qian, J. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.83 · Cited by 649 · see citing works
Widespread plasticity in CTCF occupancy linked to DNA methylation
Wang, H., Maurano, M. T., Qu, H., Varley, K. E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R., et al. (2012) · Genome Research · doi:10.1101/gr.136101.111 · Cited by 588 · see citing works
“…patterns are largely invariant between cell types (Kim et al. 2007; Cuddapah et al. 2008; Heintzman et al. 2009), though diverse regulatory mechanisms at individual loci have been described (Lefevre et al. 2008; Sekimata et al. 2009; Witcher and Emerson 2009; Lai et al. 2010; Shukla et al. 2011).”
Jonkers, I., Kwak, H., & Lis, J. T. (2014) · eLife · doi:10.7554/elife.02407 · Cited by 581 · see citing works
Maunakea, A. K., Chepelev, I., Cui, K., & Zhao, K. (2013) · Cell Research · doi:10.1038/cr.2013.110 · Cited by 552 · see citing works
Dayeh, T., Volkov, P., Salö, S., Hall, E., Nilsson, E., Olsson, A. H., Kirkpatrick, C. L., Wollheim, C. B., Eliasson, L., Rönn, T., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004160 · Cited by 523 · see citing works
CpG and non-CpG methylation in epigenetic gene regulation and brain function
Jang, H., Shin, W., Lee, J., & Do, J. (2017) · Genes · doi:10.3390/genes8060148 · Cited by 427 · see citing works
Dynamic integration of splicing within gene regulatory pathways
Braunschweig, U., Gueroussov, S., Plocik, A. M., Graveley, B. R., & Blencowe, B. J. (2013) · Cell · doi:10.1016/j.cell.2013.02.034 · Cited by 406 · see citing works
DNA methylation changes in plasticity genes accompany the formation and maintenance of memory
Halder, R., Hennion, M., Vidal, R. O., Shomroni, O., Rahman, R.-U., Rajput, A., Centeno, T. P., van Bebber, F., Capece, V., Vizcaino, J. C. G., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4194 · Cited by 358 · 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
Cellular and epigenetic drivers of stem cell ageing
Ermolaeva, M., Neri, F., Ori, A., & Rudolph, K. L. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0020-3 · Cited by 272 · see citing works
Dayeh, T. A., Olsson, A. H., Volkov, P., Almgren, P., Rönn, T., & Ling, C. (2013) · Diabetologia · doi:10.1007/s00125-012-2815-7 · Cited by 199 · see citing works
DNA methylation in social insects: how epigenetics can control behavior and longevity
Yan, H., Bonasio, R., Simola, D. F., Liebig, J., Berger, S. L., & Reinberg, D. (2015) · Annual Review of Entomology · doi:10.1146/annurev-ento-010814-020803 · Cited by 183 · see citing works
Huang, H., Zhu, Q., Jussila, A., Han, Y., Bintu, B., Kern, C., Conte, M., Zhang, Y., Bianco, S., Chiariello, A. M., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00863-6 · Cited by 187 · see citing works
Sharples, A. P., Stewart, C. E., & Seaborne, R. A. (2016) · Aging Cell · doi:10.1111/acel.12486 · Cited by 180 · see citing works
Alternative splicing: decoding an expansive regulatory layer
Irimia, M., & Blencowe, B. J. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.03.005 · Cited by 177 · see citing works
Epigenetic alterations in depression and antidepressant treatment
Menke, A., & Binder, E. B. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.3/amenke · Cited by 161 · see citing works
Epigenetic dysregulation of SHANK3 in brain tissues from individuals with autism spectrum disorders
Zhu, L., Wang, X., Li, X.-L., Towers, A., Cao, X., Wang, P., Bowman, R., Yang, H., Goldstein, J., Li, Y.-J., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddt547 · Cited by 147 · see citing works
van den Hoogenhof (2016) · doi:10.1161/circresaha.115.307872 · Cited by 134 · see citing works
Characterizing the genetic basis of methylome diversity in histologically normal human lung tissue
Shi, J., Marconett, C. N., Duan, J., Hyland, P. L., Li, P., Wang, Z., Wheeler, W., Zhou, B., Campan, M., Lee, D. S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4365 · Cited by 137 · see citing works
17q21 asthma-risk variants switch CTCF binding and regulate IL-2 production by T cells
Schmiedel, B. J., Seumois, G., Samaniego-Castruita, D., Cayford, J., Schulten, V., Chavez, L., Ay, F., Sette, A., Peters, B., & Vijayanand, P. (2016) · Nature Communications · doi:10.1038/ncomms13426 · Cited by 127 · see citing works
Pause & go: from the discovery of RNA polymerase pausing to its functional implications
Mayer, A., Landry, H. M., & Churchman, L. S. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.03.002 · Cited by 125 · see citing works
Schweikhard, V., Meng, C., Murakami, K., Kaplan, C. D., Kornberg, R. D., & Block, S. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1405181111 · Cited by 92 · see citing works
Wan, J., Oliver, V. F., Zhu, H., Zack, D. J., Qian, J., & Merbs, S. L. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt652 · Cited by 49 · see citing works
Yu, D.-H., Ware, C., Waterland, R. A., Zhang, J., Chen, M.-H., Gadkari, M., Kunde-Ramamoorthy, G., Nosavanh, L. M., & Shen, L. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01124-12 · Cited by 48 · see citing works
A Whole Methylome CpG-SNP Association Study of Psychosis in Blood and Brain Tissue
van den Oord, E. J. C. G., Clark, S. L., Xie, L. Y., Shabalin, A. A., Dozmorov, M. G., Kumar, G., Swedish Schizophrenia Consortium, Vladimirov, V. I., Magnusson, P. K. E., & Aberg, K. A. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv182 · Cited by 47 · see citing works
Li-Tempel, T., Larra, M. F., Sandt, E., Mériaux, S. B., Schote, A. B., Schächinger, H., Muller, C. P., & Turner, J. D. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0180-y · Cited by 46 · see citing works
Mammalian cells acquire epigenetic hallmarks of human cancer during immortalization
Tommasi, S., Zheng, A., Weninger, A., Bates, S. E., Li, X. A., Wu, X., Hollstein, M., & Besaratinia, A. (2013) · Nucleic Acids Research · doi:10.1093/nar/gks1051 · Cited by 45 · see citing works
Decoding the role of TET family dioxygenases in lineage specification
Wu, X., Li, G., & Xie, R. (2018) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0228-7 · Cited by 43 · see citing works
Banerjee, A. R., Kim, Y. J., & Kim, T. H. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1018 · Cited by 39 · see citing works
Khurana, I., Kaspi, A., Ziemann, M., Block, T., Connor, T., Spolding, B., Cooper, A., Zimmet, P., El-Osta, A., & Walder, K. (2016) · International Journal of Obesity · doi:10.1038/ijo.2016.64 · Cited by 11 · see citing works
- Authors
- Shukla, S., Kavak, E., Gregory, M., Imashimizu, M., Shutinoski, B., Kashlev, M., Oberdoerffer, P., Sandberg, R., & Oberdoerffer, S.
- Affiliations
- National Cancer Institute (US)
- Frederick National Laboratory for Cancer Research (US)
- Karolinska Institutet (SE)
- Corresponding author
- Oberdoerffer, Shalini
- ORCID
- Venue
- Nature
- Published
- 2011-11
- Volume
- 479
- Issue
- 7371
- Pages
- 74-79
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7398428
- OpenAlex
- W2092992881
- Cited by
- 973
- References
- 54
- Citations by year
- 2026: 28 · 2025: 37 · 2024: 46 · 2023: 39 · 2022: 48 · 2021: 78 · 2020: 51 · 2019: 66 · 2018: 63 · 2017: 61 · 2016: 64 · 2015: 104 · 2014: 103 · 2013: 100 · 2012: 79
- FWCI
- 37.10
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Vetenskapsrådet
- National Institutes of Health (1ziabc011636-01)
- National Cancer Institute (ZIABC011293)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- CTCF, RNA polymerase II pausing, DNA methylation, alternative splicing, co-transcriptional splicing, CD45, exon inclusion, histone methylation, nucleosome occupancy, transcription elongation, spliceosome assembly
- MeSH terms
- CCCTC-Binding Factor, Animals, Cell Line, Cells, Cultured, Exons, Humans, Protein Binding, Repressor Proteins, RNA Polymerase II, RNA, Messenger, Saccharomyces cerevisiae, Transcription, Genetic, Genome, Human, Alternative Splicing, Leukocyte Common Antigens, DNA Methylation, RNA Splice Sites, Epigenesis, Genetic, 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 ›
Are you an author, or do you see a problem with this page? Request a review