Cited by 252RNA Research and SplicingDNA Repair MechanismsGenomics and Chromatin Dynamics

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The core spliceosome as target and effector of non-canonical ATM signalling

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Tresini, Maria, Warmerdam, Daniël O., Kolovos, Petros, Snijder, Loes, Vrouwe, Mischa G., Demmers, Jeroen A. A., van IJcken, Wilfred F. J., Grosveld, Frank G., Medema, René H., Hoeijmakers, Jan H. J., Mullenders, Leon H. F., Vermeulen, Wim, Marteijn, Jurgen A.·2015·Nature

DOI 10.1038/nature14512PMC PMC4501432

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Abstract

In response to DNA damage, tissue homoeostasis is ensured by protein networks promoting DNA repair, cell cycle arrest or apoptosis. DNA damage response signalling pathways coordinate these processes, partly by propagating gene-expression-modulating signals. DNA damage influences not only the abundance of messenger RNAs, but also their coding information through alternative splicing. Here we show that transcription-blocking DNA lesions promote chromatin displacement of late-stage spliceosomes and initiate a positive feedback loop centred on the signalling kinase ATM. We propose that initial spliceosome displacement and subsequent R-loop formation is triggered by pausing of RNA polymerase at DNA lesions. In turn, R-loops activate ATM, which signals to impede spliceosome organization further and augment ultraviolet-irradiation-triggered alternative splicing at the genome-wide level. Our findings define R-loop-dependent ATM activation by transcription-blocking lesions as an important event in the DNA damage response of non-replicating cells, and highlight a key role for spliceosome displacement in this process.

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1 retracted

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Cox, J., & Mann, M. (2008) · Nature Biotechnology · doi:10.1038/nbt.1511 · Cited by 14,855
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,682
The DNA Damage Response: Making It Safe to Play with Knives
Ciccia, A., & Elledge, S. J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.019 · Cited by 4,368
DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation
Bakkenist, C. J., & Kastan, M. B. (2003) · Nature · doi:10.1038/nature01368 · Cited by 3,466
ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage
Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R., Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y., et al. (2007) · Science · doi:10.1126/science.1140321 · Cited by 3,075
DNA damage, aging, and Cancer
Hoeijmakers, J. H. J. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804615 · Cited by 2,239
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Shiloh, Y., & Ziv, Y. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3546 · Cited by 1,649
ATM Activation by DNA Double-Strand Breaks Through the Mre11-Rad50-Nbs1 Complex
Lee, J.-H., & Paull, T. T. (2005) · Science · doi:10.1126/science.1108297 · Cited by 1,424
Linkage of ATM to Cell Cycle Regulation by the Chk2 Protein Kinase
Matsuoka, S. (1998) · Science · doi:10.1126/science.282.5395.1893 · Cited by 1,322

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Walker, C., & El‐Khamisy, S. F. (2018) · Brain · doi:10.1093/brain/awy076 · Cited by 40
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Chakraborty, A., Tapryal, N., Venkova, T., Mitra, J., Vasquez, V., Sarker, A. H., Duarte‐Silva, S., Huai, W., Ashizawa, T., Ghosh, G., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1917280117 · Cited by 40
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hPso4/hPrp19: a critical component of DNA repair and DNA damage checkpoint complexes
Mahajan, K. N. (2015) · Oncogene · doi:10.1038/onc.2015.321 · Cited by 34

Authors: Tresini, M., Warmerdam, D. O., Kolovos, P., Snijder, L., Vrouwe, M. G., Demmers, J. A. A., van IJcken, W. F. J., Grosveld, F. G., Medema, R. H., Hoeijmakers, J. H. J., Mullenders, L. H. F., Vermeulen, W., & Marteijn, J. A.
Affiliations: Erasmus MC (NL)
The Netherlands Cancer Institute (NL)
Leiden University Medical Center (NL)
Corresponding author: Tresini, Maria
Vermeulen, Wim
Marteijn, Jurgen A.
ORCID: Tresini, Maria
Warmerdam, Daniël O.
Kolovos, Petros
Demmers, Jeroen A. A.
Grosveld, Frank G.
Medema, René H.
Hoeijmakers, Jan H. J.
Vermeulen, Wim
Marteijn, Jurgen A.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2015-06-24
Volume: 523
Issue: 7558
Pages: 53-58
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature14512
PMC: PMC4501432
OpenAlex: W1823908009
Cited by: 252
References: 45
Citations by year: 2026: 8 · 2025: 13 · 2024: 22 · 2023: 21 · 2022: 22 · 2021: 20 · 2020: 24 · 2019: 25 · 2018: 27 · 2017: 31 · 2016: 25 · 2015: 14
FWCI: 14.03
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
PubMed Central (acceptedVersion)
Pure Amsterdam UMC (submittedVersion, cc-by)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Leiden Repository (Leiden University) (submittedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
RePub (Erasmus University Rotterdam) (submittedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion)
Funders: ZonMw (912.12.132, 912.08.031, 854.11.002)
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (935.11.042, 823.02.013, 854.11.002, 912.12.132, 912.08.031)
National Institute on Aging (P01AG017242)
FP7 Ideas: European Research Council (340988, 233424)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: ATM kinase, alternative splicing, DNA damage response, R-loops, U2 snRNP, U5 snRNP, UV irradiation, RNA polymerase pausing, feed-forward loop, nascent RNA
MeSH terms: Cell Line, Chromatin, DNA Damage, Enzyme Activation, Humans, DNA-Directed RNA Polymerases, Ultraviolet Rays, Signal Transduction, Spliceosomes, Alternative Splicing, Ataxia Telangiectasia Mutated Proteins

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The core spliceosome as target and effector of non-canonical ATM signalling

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