Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation
Open accessAbstract
Alternative splicing contributes to cell type-specific transcriptomes. Here, we show that changes in intragenic chromatin marks affect NCAM (neural cell adhesion molecule) exon 18 (E18) alternative splicing during neuronal differentiation. An increase in the repressive marks H3K9me2 and H3K27me3 along the gene body correlated with inhibition of polymerase II elongation in the E18 region, but without significantly affecting total mRNA levels. Treatment with the general DNA methylation inhibitor 5-azacytidine and BIX 01294, a specific inhibitor of H3K9 dimethylation, inhibited the differentiation-induced E18 inclusion, pointing to a role for repressive marks in sustaining NCAM splicing patterns typical of mature neurons. We demonstrate that intragenic deployment of repressive chromatin marks, induced by intronic small interfering RNAs targeting NCAM intron 18, promotes E18 inclusion in undifferentiated N2a cells, confirming the chromatin changes observed upon differentiation to be sufficient to induce alternative splicing. Combined with previous evidence that neuronal depolarization causes H3K9 acetylation and subsequent E18 skipping, our results show how two alternative epigenetic marks regulate NCAM alternative splicing and E18 levels in different cellular contexts.
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Local changes of histone modifications such as acetylation or methylation and RNA Pol II speed occur on alternative spliced exons during cell response to depolarization and differentiation.
“Along the same lines, local changes of histone modifications such as acetylation or methylation and RNA Pol II speed occur on alternative spliced exons during cell response to depolarization and differentiation (Schor et al, 2009; Schor et al, 2013; Sharma et al, 2014).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Schor et al, 2013
The Introduction and Discussion link neuronal depolarization and differentiation to changes in NCAM histone marks, RNA polymerase II elongation, and alternative splicing of exon E18. However, the Discussion says the histone-mark changes during differentiation are spread across the gene body, not specifically located at E18; the elongation change is more localized. Thus the claim overstates how precisely the histone changes occur at the alternative exon. (LLM, conf=0.86)
Experimental — accuracy not yet measuredRNA Pol II speed can vary on individual genes or downstream of genes in response to different stimuli.
“Moreover, we and others have shown that RNA Pol II speed can vary on individual genes or downstream of genes in response to different stimuli (Schor et al, 2009; Schor et al, 2013; Sharma et al, 2014; Muniz et al, 2017).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Schor et al, 2013
RNA Pol II velocity changes around alternatively spliced exons in specific genes, in response to cell depolarization and cellular differentiation.
“Second, RNA Pol II velocity changes around alternatively spliced exons in specific genes, in response to cell depolarization and cellular differentiation (Schor et al, 2009; Schor et al, 2013; Sharma et al, 2014).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Schor et al, 2013
Changes in RNA Pol II velocity measured in response to cell depolarization and cell differentiation regulate alternative splicing and thus RNA identity.
“Indeed, changes in RNA Pol II velocity measured in response to cell depolarization and cell differentiation regulate alternative splicing and thus RNA identity (Schor et al, 2009; Schor et al, 2013; Sharma et al, 2014).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Schor et al, 2013
An increase in H3K9 di-methylation and H3K27 tri-methylation correlates with a slow-down of RNA Pol II transcription.
“Similarly, H3K9 hyperacetylation correlates with a change in the ratio of distal versus proximal pre‐mRNA levels suggesting a local increase in RNA Pol II speed (Schor et al, 2009), whereas an increase in H3K9 di‐methylation and H3K27 tri‐methylation correlates with a slow‐down of RNA Pol II transcription (Schor et al, 2013).”
From RNA polymerase II speed: a key player in controlling and adapting transcriptome composition (2021) · cites this paper as Schor et al, 2013
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Chromatin and Alternative SplicingPreprint
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BackgroundRNA polymerase II speed: a key player in controlling and adapting transcriptome composition
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“…correlates with a change in the ratio of distal versus proximal pre-mRNA levels suggesting a local increase in RNA Pol II speed (Schor et al , 2009), whereas an increase in H3K9 di-methylation and H3K27 tri-methylation correlates with a slow-down of RNA Pol II transcription (Schor et al , 2013).”
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“All these features prompted us to investigate whether SYNE2 E107 inclusion is regulated in an AGO1-dependent manner, in particular, through the TGS-AS mechanism (3, 23).”
BackgroundResultInfluentialSelf-citationTET‐catalyzed oxidation of intragenic 5‐methylcytosine regulates CTCF‐dependent alternative splicing
Marina, R. J., Sturgill, D. M., Bailly, M. A., Thénoz, M., Varma, G., Prigge, M. F., Nanan, K. K., Shukla, S., Haque, N., & Oberdoerffer, S. (2015) · The EMBO Journal · doi:10.15252/embj.201593235 · Cited by 102 · see citing works
“…structure have revealed global alterations in splicing patterns, thus broadening the pre-mRNA splicing “code” to include intragenic chromatin structure (Schor et al, 2009, 2013; Luco et al, 2010; Hnilicova et al, 2011; Saint-Andre et al, 2011; Ameyar-Zazoua et al, 2012; Patrick et al, 2015).”
BackgroundSplicing at the phase-separated nuclear speckle interface: a model
Liao, S. E., & Regev, O. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1209 · Cited by 98 · see citing works
Fuchs, G., Hollander, D., Voichek, Y., Ast, G., & Oren, M. (2014) · Genome Research · doi:10.1101/gr.176487.114 · Cited by 102 · see citing works
“Pol II has been shown to pause or slow down upstream of exons, presumably underlying a regulatory effect of elongation rate on cotranscriptional splicing (de la Mata et al. 2003; Schor et al. 2009, 2013; Ip et al. 2011; Luco et al. 2011; Kwak et al. 2013).”
BackgroundSites 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
Alternative Splicing of G9a Regulates Neuronal Differentiation
Fiszbein, A., Giono, L. E., Quaglino, A., Berardino, B. G., Sigaut, L., von Bilderling, C., Schor, I. E., Steinberg, J. H. E., Rossi, M., Pietrasanta, L. I., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.063 · Cited by 88 · see citing works
Self-citationAlternative splicing in EMT and TGF-β signaling during cancer progression
Zhang, Y. E., & Stuelten, C. H. (2024) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2024.04.001 · Cited by 95 · see citing works
Alternative splicing switches: Important players in cell differentiation
Fiszbein, A., & Kornblihtt, A. R. (2017) · BioEssays · doi:10.1002/bies.201600157 · Cited by 85 · see citing works
“Inaddition, our lab furtheranalyzed the regulationofNCAM AS by chromatin structure during neuronal differentiation [80].”
MethodSelf-citationNascent 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
“…alternative splicing are dependent on Pol II elongation rates, which are slowed or accelerated on ultraviolet (UV) damage, chromatin modification, and direct mutation of Pol II (Munoz et al. 2009; Luco et al. 2011; Hnilicova et al. 2013; Schor et al. 2013; Dujardin et al. 2014; Fong et al. 2014).”
BackgroundDNA Methylation within Transcribed Regions
To, T. K., Saze, H., & Kakutani, T. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.00543 · Cited by 75 · see citing works
“Interestingly, artificially established repressive marks driven by small interfering RNAs can cause an increase in DNA methylation and ectopic inclusion of noncanonical exons (Schor et al., 2013).”
BackgroundMarasco, L. E., Dujardin, G., Sousa‐Luís, R., Liu, Y. H., Stigliano, J. N., Nomakuchi, T. T., Proudfoot, N. J., Krainer, A. R., & Kornblihtt, A. R. (2022) · Cell · doi:10.1016/j.cell.2022.04.031 · Cited by 71 · see citing works
Self-citationWang, H. V., & Chekanova, J. A. (2016) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1340 · Cited by 67 · see citing works
“Recent work in Drosophila and humans has reported examples of regulation of AS through smRNAs.(37,40,150,151) Human siRNAs can regulate AS by mediating the formation of facultative heterochromatin, increasing repressive histone modifications H3K9me2 and H3K27me3.”
BackgroundBoeckx, C. A., & Benítez‐Burraco, A. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01324 · Cited by 65 · see citing works
L1-CAM and N-CAM: From Adhesion Proteins to Pharmacological Targets
Colombo, F., & Meldolesi, J. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.08.004 · Cited by 62 · see citing works
How Are Short Exons Flanked by Long Introns Defined and Committed to Splicing?
Hollander, D., Naftelberg, S., Lev-Maor, G., Kornblihtt, A. R., & Ast, G. (2016) · Trends in Genetics · doi:10.1016/j.tig.2016.07.003 · Cited by 59 · see citing works
Self-citationRNA processing in skeletal muscle biology and disease
Hinkle, E. R., Wiedner, H. J., Black, A. J., & Giudice, J. (2018) · Transcription · doi:10.1080/21541264.2018.1558677 · Cited by 61 · see citing works
“Creating a more permissive chromatin environment via treatment with an HDAC inhibitor increased exon skipping whereas enrichment of repressive marks around exon 18 promoted its inclusion [121,122].”
BackgroundCalcium-mediated histone modifications regulate alternative splicing in cardiomyocytes
Sharma, A., Nguyen, H., Geng, C., Hinman, M. N., Luo, G., & Lou, H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408964111 · Cited by 59 · see citing works
He, R., & Kidder, B. L. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx251 · Cited by 54 · see citing works
Neuronal activity-regulated alternative mRNA splicing
Hermey, G., Blüthgen, N., & Kuhl, D. (2017) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2017.06.002 · Cited by 50 · see citing works
Salton, M., Voss, T. C., & Misteli, T. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1226 · Cited by 50 · see citing works
“Previous work has linked H3K9me3 to AS of CD44 (59) and NCAM (61).”
BackgroundMoehle, E. A., Braberg, H., Krogan, N. J., & Guthrie, C. (2014) · RNA Biology · doi:10.4161/rna.28646 · Cited by 46 · see citing works
“318 RnA Biology Volume 11 issue 4 exciting example of this from human neuronal culture shows a direct link between chromatin modification and alternative splicing, via an effect on RNAPII elongation rate.(67) As additional factors that influence splicing efficiency are defined, and assays to better characterize the ti…”
Matveeva, E. A., Al-Tinawi, Q. M. H., Rouchka, E. C., & Fondufe‐Mittendorf, Y. N. (2019) · Epigenetics & Chromatin · doi:10.1186/s13072-019-0261-1 · Cited by 47 · see citing works
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“As histone modifications can impact alternative splicing, we believe that an SNRPG -driven histone-based system might help elucidate details regarding the collection of alternative splicing arrays in cells and tissues 48-50 , which may be the direction of our future studies.”
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
Alternative Splicing and Transcription Elongation in Plants
Herz, M. A. G., & Kornblihtt, A. R. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00309 · Cited by 42 · see citing works
Self-citationSoto, E. J. L., & Lipscombe, D. (2020) · eLife · doi:10.7554/elife.54879 · Cited by 40 · see citing works
“CTCF has been suggested to enhance exon recognition by slowing the elongation rate of Pol II (Shukla et al., 2011) and this co-transcription-splicing mechanism proposed to account for the influ- ence of epigenetic modifications on pre mRNA splicing in neurons (Ding et al., 2017; Schor et al., 2013).”
BackgroundLinking transcription, RNA polymerase II elongation and alternative splicing
Giono, L. E., & Kornblihtt, A. R. (2020) · Biochemical Journal · doi:10.1042/bcj20200475 · Cited by 39 · see citing works
Self-citationRegulation of alternative splicing by p300-mediated acetylation of splicing factors
Siam, A., Baker, M., Amit, L., Regev, G. M., Rabner, A., Najar, R. A., Bentata, M., Dahan, S., Cohen, K., Araten, S., et al. (2019) · RNA · doi:10.1261/rna.069856.118 · Cited by 35 · see citing works
“…is by directly affecting nucleosome occupancy; specifically, histone acetylation results in the eviction of ORF nucleosomes during transcription elongation consequently promoting RNAPII fast kinetics (Church and Fleming 2017) and exon exclusion (Schor et al. 2009, 2013; Du š ková et al. 2014).”
A saga of cancer epigenetics: linking epigenetics to alternative splicing
Narayanan, S. P., Singh, S., & Shukla, S. (2017) · Biochemical Journal · doi:10.1042/bcj20161047 · Cited by 34 · see citing works
Epigenetic control of skeletal muscle atrophy
Liang, W., Xu, F., Li, L., Peng, C., Sun, H., Qiu, J., & Sun, J. (2024) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-024-00618-1 · Cited by 32 · see citing works
Epigenetic Neuropharmacology: Drugs Affecting the Epigenome in the Brain
Tóth, M. (2020) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-030220-022920 · Cited by 32 · see citing works
Alternative RNA splicing in tumour heterogeneity, plasticity and therapy
Pohl, S., & Myant, K. (2022) · Disease Models & Mechanisms · doi:10.1242/dmm.049233 · Cited by 31 · see citing works
“Furthermore, RNA polymerase elongation rates and therefore pre-mRNA splicing can be regulated by intergenic histone modifications, including histone H3K9 acetylation (Schor et al., 2009) and H3K9 methylation (Schor et al., 2013).”
KDM3A regulates alternative splicing of cell-cycle genes following DNA damage
Baker, M., Petasny, M., Taqatqa, N., Bentata, M., Kay, G., Engal, E., Nevo, Y., Siam, A., Dahan, S., & Salton, M. (2021) · RNA · doi:10.1261/rna.078796.121 · Cited by 26 · see citing works
“…promoterregionshasbeenshowntocause gene silencing, the same modification in the intragenic region of genes was shown to alter alternative splicing (Schor et al. 2013; Salton et al. 2014; Agirre et al. 2015; Lev Maor et al. 2015; Bieberstein et al. 2016; Fiszbein and Kornblihtt 2016; Fiszbein et…”
Li, X., Baker‐Andresen, D., Zhao, Q., Marshall, V. M., & Bredy, T. W. (2014) · Genes Brain & Behavior · doi:10.1111/gbb.12150 · Cited by 25 · see citing works
“To date, investigation of neuronal DNA methylation has been restricted to candidate loci (Labonte et al. 2012; Matrisciano et al. 2013; Nishioka et al. 2013; Schor et al. 2013), reduced representations of the genome (Guo et al.”
BackgroundPre-mRNA Splicing in the Nuclear LandscapePreprint
Carrocci, T. J., & Neugebauer, K. M. (2019) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2019.84.040402 · Cited by 25 · see citing works
“It is also well known that RNA polymerase II (Pol II) speed influences alternative splicing and intron retention in all examined species (Schor et al. 2009, 2013; Aslanzadeh et al. 2018; Saldi et al. 2018; Godoy Herz et al. 2019).”
BackgroundBeyond transcription: compelling open questions in plant RNA biology
Manavella, P. A., Herz, M. A. G., Kornblihtt, A. R., Sorenson, R. S., Sieburth, L., Nakaminami, K., Seki, M., Ding, Y., Sun, Q., Kang, H., et al. (2022) · The Plant Cell · doi:10.1093/plcell/koac346 · Cited by 25 · see citing works
Self-citationTALE-directed local modulation of H3K9 methylation shapes exon recognition
Bieberstein, N. I., Kozáková, E., Huranová, M., Thakur, P. K., Krchňáková, Z., Krausová, M., Oesterreich, F. C., & Staněk, D. (2016) · Scientific Reports · doi:10.1038/srep29961 · Cited by 22 · see citing works
“1 21,33 ), we speculated this histone modification may help to recognize exons in general.”
Epigenetics at the base of alternative splicing changes that promote colorectal cancer
Kornblihtt, A. R. (2017) · Journal of Clinical Investigation · doi:10.1172/jci96497 · Cited by 18 · see citing works
“Intragenic histone modifications, including H2B monoubiquitylation (10), H3K9 acetylation and methylation (11, 12), and H3K4 trimethylation (13), that affect nucleosome organization have been shown to correlate with changes in elongation.”
BackgroundSelf-citationShenker, N. S., Flower, K. J., Wilhelm-Benartzi, C. S., Dai, W., Bell, E., Gore, E. J., El-Bahrawy, M. A., Weaver, G., Brown, R. E., & Flanagan, J. M. (2015) · BMC Cancer · doi:10.1186/s12885-015-1335-5 · Cited by 17 · see citing works
“Several mechanisms by which IGM may be functionally important have been proposed, including the prevention of transcription from alternative start sites in the gene body, chromatin regulation, the inhibition of transposable elements, and the control of alternative splicing [29,30].”
BackgroundMyogenic Differential Methylation: Diverse Associations with Chromatin Structure
Chandra, S., Baribault, C., Lacey, M. R., & Ehrlich, M. (2014) · Biology · doi:10.3390/biology3020426 · Cited by 16 · see citing works
“Evidence is accumulating that changes in DNA methylation also help direct alternative splicing [15].”
BackgroundAlterations of presynaptic proteins in autism spectrum disorder
Yeo, X. Y., Lim, Y. T., Chae, W. R., Park, C., Park, H., & Jung, S. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1062878 · Cited by 15 · see citing works
“As LAR-RPTPs were required for the synaptogenic function of presynaptic neurexin (Han et al., 2020) and postsynaptic Slitand Trk-like proteins (Slitrks) (Yim et al., 2013), presynaptic Liprin can modulate synapse specification.”
BackgroundAltered Morphologies and Functions of the Olfactory Bulb and Hippocampus Induced by miR-30c
Sun, T., Li, T., Davies, H., Li, W., Yang, J., Li, S., & Ling, S. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00207 · Cited by 15 · see citing works
“Neuro2A is a mouse-neural-crest-derived cell line, endued with nearly all the attributes of neurons and it has been extensively used as neuron substitute in study of neuronal proliferation and differentiation (Schor et al., 2013; Fiszbein et al., 2016).”
BackgroundAcker, H. H. V., Acker, Z. P. V., Versteven, M., Ponsaerts, P., Pende, D., Berneman, Z. N., Anguille, S., Tendeloo, V. F. V., & Smits, E. (2019) · Cancers · doi:10.3390/cancers11071029 · Cited by 15 · see citing works
“Interestingly, epigenetic modulation has been reported to result in alternative splicing of NCAM [32].”
BackgroundLeung, C. S., Rosenzweig, S. J., Yoon, B., Marinelli, N. A., Hollingsworth, E. W., Maguire, A. M., Cowen, M. H., Schmidt, M., Imitola, J., Uzun, E. D. G., et al. (2023) · Human Molecular Genetics · doi:10.1093/hmg/ddad002 · Cited by 15 · see citing works
Effect of histone modifications on hMLH1 alternative splicing in gastric cancer
Zhao, J., Li, X., Shi, B., Wang, F., Xu, Z., Meng, H., Su, Y., Wang, J., Xiao, N., He, Q., et al. (2017) · Tumor Biology · doi:10.1177/1010428317697546 · 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
Long range chromatin organization
Acuña, L. I. G., & Kornblihtt, A. R. (2014) · Transcription · doi:10.4161/trns.28726 · Cited by 14 · see citing works
Self-citationZhang, L., Gordiyenko, Y., Morgan, T., Franco, C., Tufegdžić Vidaković, A., & Zhang, S. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01586-6 · Cited by 12 · see citing works
“Our structures reveal that the brake helix of RECQL5 competes with the UVSSA C-terminal hinged helix for the same binding site next to the K1268 loop (Fig.”
Effects of airborne particulate matter on alternative pre-mRNA splicing in colon cancer cells
Buggiano, V., Petrillo, E., Alló, M., Lafaille, C., Redal, M. A., Alghamdi, M. A., Khoder, M. I., SHAMY, M. Y., Muñoz, M. J., & Kornblihtt, A. R. (2015) · Environmental Research · doi:10.1016/j.envres.2015.04.001 · Cited by 11 · see citing works
“…if BMP4 splicing was regulated instead by changes in transcriptional elongation, as previously reported for several ASEs (de la Mata et al., 2003; Schor et al., 2009, 2013; Alló et al., 2009; Ameyar-Zazoua et al. 2012; Dujardin et al., 2014) whose splicing is coupled to RNA polymerase II (Pol…”
BackgroundSelf-citationMatveeva, E. A., Dhahri, H., & Fondufe‐Mittendorf, Y. N. (2022) · Cells · doi:10.3390/cells11203202 · Cited by 10 · see citing works
Borght, A. V., Duysinx, M., Broers, J. L. V., et al. (2018) · Translational Lung Cancer Research · doi:10.21037/tlcr.2018.03.03 · Cited by 9 · see citing works
“(15) identified epigenetic modulation resulting in alternative splicing of NCAM and expression of E18 in neuroblastoma cells.”
BackgroundRapid and Efficient Co-Transcriptional Splicing Enhances Mammalian Gene Expression
Reimer, K. A. (2020) · doi:10.26226/morressier.5ebd45acffea6f735881ae83 · Cited by 10 · see citing works
“For example, altering the rate of RNA polymerase II (Pol II) elongation has been shown to affect the outcome of splicing; when Pol II transcribes more slowly than usual, widespread changes in alternative splicing occur (Aslanzadeh et al., 2018; Braberg et al., 2013; Carrillo Oesterreich et al., 2016; de la Mata et al.…”
BackgroundFiszbein, A., Schor, I. E., & Kornblihtt, A. R. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800781-5.00011-6 · Cited by 7 · see citing works
Self-citation‘Mediator‐ing’ messenger RNA processing
Huang, Y., Xiao, Y., & Wang, G. (2014) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1273 · Cited by 7 · see citing works
Animal Models of Transgenerational Epigenetic Effects
Rosenfeld, C. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405944-3.00011-8 · Cited by 7 · see citing works
Pan, D., Long, L., Li, C., Zhou, Y., Liu, Q., Zhao, Z., Zhao, H., Lin, W., Zheng, Z.-Y., Liu, P., et al. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107414 · Cited by 6 · see citing works
“…and cis -acting elements, epigenetic modi fi cations (N6-adenylate methylation (38), RNA editing (39), DNA methylation, and histone modi fi cation (40, 41)), and RNA structure (intron length and RNA stem-loop structure (42 – 44), pseu-douridine modi fi cation (45), and GC content of genes (46, 47)).”
BackgroundTargeting proteins to RNA transcription and processing sites within the nucleus
Sánchez-Hernández, N., Prieto‐Sánchez, S., Moreno‐Castro, C., Muñoz-Cobo, J. P., Yousfi, Y. E., Boyero-Corral, S., Suñé-Pou, M., Hernández-Munaín, C., & Suñé, C. (2017) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2017.06.001 · Cited by 6 · see citing works
Ortega, M. T., Bivens, N. J., Jogahara, T., Kuroiwa, A., Givan, S. A., & Rosenfeld, C. S. (2019) · BMC Genomics · doi:10.1186/s12864-019-5426-6 · Cited by 6 · see citing works
RNA Transcript Diversity in Neuromuscular Research
Lim, W. F., & Rinaldi, C. (2023) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-221601 · Cited by 7 · see citing works
Interplay Between Chromatin and Splicing
Fiszbein, A., Herz, M. A. G., Acuña, L. I. G., & Kornblihtt, A. R. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803395-1.00008-3 · Cited by 4 · see citing works
Self-citationEvolution and stress response potential of the plant splicing factor U1C
Jia, Z., Wang, J., Meng, X., Yang, X., Tian, Y., Wang, B., Chen, M., Yang, J., Das, D., & Cao, Y. (2024) · Scientific Reports · doi:10.1038/s41598-024-68190-4 · Cited by 3 · see citing works
Revisiting Evidence for Epigenetic Control of Alternative SplicingPreprint
Manz, Q., & List, M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.30.610315 · Cited by 2 · see citing works
Crosstalk between chromatin state and ATM signalling in DNA damage-induced transcription stress
Salas‐Armenteros, I., Klunder, M., Vermeulen, W., & Tresini, M. (2025) · The EMBO Journal · doi:10.1038/s44318-025-00537-7 · Cited by 1 · see citing works
“Despite sporadic evidence from independent published studies that would support a link between ATM signaling and H3S10P (often with conflicting findings) a direct relationship between ATM signaling, MSK1 function and phosphorylation of H3(S10) has only been demonstrated in our current study.”
Viegas, J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421075111 · Cited by 1 · see citing works
Prenatal Exposure to Maternal Cigarette Smoking, Addiction, and the Offspring Brain
Paus, T., & Pausová, Z. (2015) · Palgrave Macmillan UK eBooks · doi:10.1057/9781137362650_14 · Cited by 1 · see citing works
Townley, B. A., Buerer, L., Bacolla, A., Rusanov, T., Schmidt, N., Srivatsan, S. N., Clark, N. E., Mansoori, F., Sample, R. A., Brickner, J. R., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.03.515106 · Cited by 1 · see citing works
“examining elongation rate in response to UV damage, chromatin state, and Pol II mutation have found that abnormal elongation rates caused by altered Pol II function reduced splicing efficiency and resulted in aberrant alternative splicing patterns (Dujardin et al., 2014; Fong et al., 2014; Hnilicova et al., 2013; Luco…”
BackgroundStigliano, J. N., Haberfeld, E., Marasco, L. E., Fiszbein, A., Proudfoot, N. J., & Kornblihtt, A. R. (2026) · Molecular Cell · doi:10.1101/2025.10.10.681673 · Cited by 1 · see citing works
“Moreover, intragenic deployment of specific histone marks can inhibit or promote RNAPII elongation by affecting chromatin compaction, which consequently affects alternative splicing.”
Self-citationAssessing the relationship between chromatin and splicing factors in alternative splicing
Kremsky, I. (2015) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
Crosstalk between chromatin state and ATM signalling in DNA damage-induced transcription stress.Preprint
Tresini, M., Salas‐Armenteros, I., Klunder, M., & Vermeulen, W. (2024) · Research Square · doi:10.21203/rs.3.rs-3831414/v1
Riccardi, F., Romano, G., Licastro, D., & Pagani, F. (2024) · PLoS ONE · doi:10.1371/journal.pone.0298965
Krick, K. S., Maroni, M. J., Korb, E., Lynch, K. W., & Heller, E. A. (2025) · Genome Research · doi:10.1101/gr.280082.124 · Cited by 1 · see citing works
“H3K36me3 redistributes over KCl-dependent alternative exons in response to KCl Previous work by ourselves and others demonstrate the impact of chromatin modifications on alternative splicing (Schor et al. 2009, 2013; Luco et al. 2010; Ding et al. 2017; Hu et al. 2017, 2020).”
Real time imaging of transcription reveals new features of cellular and viral promoters
Kozulic-Pirher, A. (2018) · theses.fr (ABES) · doi:10.70675/0099e36bz620ez43d7z9b47z2789ed360d73
- Authors
- Schor, I. E., Fiszbein, A., Petrillo, E., & Kornblihtt, A. R.
- Affiliations
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- Corresponding author
- Kornblihtt, Alberto R
- Venue
- The EMBO Journal
- Published
- 2013-07-26
- Volume
- 32
- Issue
- 16
- Pages
- 2264-2274
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC3746202
- OpenAlex
- W2106478804
- Cited by
- 90
- References
- 64
- Citations by year
- 2025: 4 · 2024: 9 · 2023: 3 · 2022: 8 · 2021: 3 · 2020: 6 · 2019: 10 · 2018: 4 · 2017: 8 · 2016: 7 · 2015: 12 · 2014: 15 · 2013: 1
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Conicet (submittedVersion, cc-by-nc-sa)
- Funders
- Howard Hughes Medical Institute
- Consejo Nacional de Investigaciones Científicas y Técnicas
- Universidad de Buenos Aires (CONICET)
- 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
- CD56, alternative splicing, neuronal differentiation, H3K9me2, H3K27me3, DNA methylation, azacitidine, BIX-01294, RNA polymerase II elongation, siRNA, N2a cells
- MeSH terms
- Animals, Azacitidine, Azepines, Cell Differentiation, Chromatin, Exons, Neurons, Quinazolines, Alternative Splicing, Sequence Analysis, DNA, DNA Primers, Neural Cell Adhesion Molecules, DNA Methylation, Reverse Transcriptase Polymerase Chain Reaction, RNA, Small Interfering, Epigenesis, Genetic, Cell Line, Tumor, Chromatin Immunoprecipitation, Mice, Real-Time Polymerase Chain Reaction
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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