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ELOF1 is a transcription-coupled DNA repair factor that directs RNA polymerase II ubiquitylation
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Abstract
Cells employ transcription-coupled repair (TCR) to eliminate transcription-blocking DNA lesions. DNA damage-induced binding of the TCR-specific repair factor CSB to RNA polymerase II (RNAPII) triggers RNAPII ubiquitylation of a single lysine (K1268) by the CRL4 CSA ubiquitin ligase. How CRL4 CSA is specifically directed towards K1268 is unknown. Here, we identify ELOF1 as the missing link that facilitates RNAPII ubiquitylation, a key signal for the assembly of downstream repair factors. This function requires its constitutive interaction with RNAPII close to K1268, revealing ELOF1 as a specificity factor that binds and positions CRL4 CSA for optimal RNAPII ubiquitylation. Drug-genetic interaction screening also revealed a CSB-independent pathway in which ELOF1 prevents R-loops in active genes and protects cells against DNA replication stress. Our study offers key insights into the molecular mechanisms of TCR and provides a genetic framework of the interplay between transcriptional stress responses and DNA replication.
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“Notably, ELOF1, a recently identified transcription elongation factor that plays an important role in transcription-coupled nucleotide-excision repair47, and LEO1, a subunit of the polymerase-associated factor 1 (Paf1) complex RNA polymerase that is required for RNA polymerase II removal in response to DNA damage, were identified48,49.”
From Large-scale CRISPR screening in primary human 3D gastric organoids enables comprehensive dissection of gene-drug interactions (2025) · cites this paper as [47]
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Self-citationPolymerase face-off: emerging concepts in transcription-replication coordination
Uruci, S., Lalonde, M., Luijsterburg, M. S., & Hamperl, S. (2026) · EMBO Reports · doi:10.1038/s44319-026-00800-w · Cited by 2
Self-citationGaillard, H., Ciudad, T., Aguilera, A., & Wellinger, R. E. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1011300 · Cited by 3
Evidence that ARK2N is not a core factor in transcription-coupled DNA repair
van Schie, J. J. M., Brussee, S. J., & Luijsterburg, M. S. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2425178122 · Cited by 2
Self-citationStabilization of AFF1 by PARylation ensures transcriptional restart after DNA damage
Zhu, F., Fu, H., Zhu, W., Li, C., Yang, M., Feng, Z., Shao, Y., Li, Z., Guo, Y., Huang, M., et al. (2025) · Nature Chemical Biology · doi:10.1038/s41589-025-02045-5 · Cited by 2
van der Woude, M., Thijssen, K. L., Sabatella, M., Marteijn, J. A. F., Vermeulen, W., & Lans, H. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.21.644538 · Cited by 2
Stalling of elongating Pol II triggers Ser7 phosphorylation in trans to drive transcription recoveryPreprint
Shlamovitz, I., Bao, Y., Toteva, T., Crisp, A., Ye, S., Wingett, S., Cacioppo, R., Edmondson, A., Castiblanco, D., Boemo, M. A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.04.692291 · Cited by 2
ELOF1 is a core component of the promoter-proximal paused RNA polymerase II complexPreprint
Nunez, R. J. V., Bressin, A., Shao, Z., Mayer, A., & Vos, S. M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.26.728003 · Cited by 2
Transcription-coupled repair: protecting genome across generations
Pani, B., & Nudler, E. (2025) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2025.102385 · Cited by 1
Pantazi, V., Smith, P., Páhi, Z. G., Katona, M., Pap, Á., Darula, Z., Fischer, R., Vendrell, I., Kessler, B. M., van Vugt, M. A. T. M., et al. (2026) · Nucleic Acids Research · doi:10.1093/nar/gkag347 · Cited by 1
The Role of TFIIH Complex in Nucleotide Excision RepairPreprint
Hoag, A., Duan, M., & Mao, P. (2023) · doi:10.22541/au.168173465.59820001/v1 · Cited by 1
Gaillard, H., Ciudad, T., Aguilera, A., & Wellinger, R. E. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.13.593813 · Cited by 1
Ubiquitylation of RNA Polymerase II Controls Early Stages of the Transcription CyclePreprint
Cacioppo, R., Gillis, A., Shlamovitz, I., Zeller, A., Castiblanco, D., Crisp, A., Haworth, B., Arabiotorre, A., Abyaneh, P., Bao, Y., et al. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4826625
Finding novel vulnerabilities of hypomorphic BRCA1 allelesPreprint
Schreuder, A., de Lint, K., Gois, M. M., Kampen, R. A., Alonso, M. S. M., Nootenboom, I., Garzero, V., Wolthuis, R. M. F., & Noordermeer, S. M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.24.595688
Self-citationMorse, R. H. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-814809-9.00009-3
RNA Polymerase II subunits overexpressions induce genome instability and deregulate transcriptionPreprint
Sadurnì, M. M., Jones, M. L., Pavlou, L., Radi, M., Kompocholi, S., Passaretti, P., Gambus, A., Gregersen, L. H., & Saponaro, M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.20.622938
Bypass of Blocking Lesions by RNAPII Impairs the Transcriptional DNA Damage ResponsePreprint
Bañuelos, C. P., Caeiro, L. D., Cingaram, P. R., Beckedorff, F., Morey, L., Cortes, D. B., Shiekhattar, R., & Verdún, R. E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.28.651040
van Schie, J. J. M., de Groot, B. A. F. J., & Luijsterburg, M. S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.23.666359
Self-citationA Splicing Variant in XPA Results in Delayed Onset of Clinical Features of Xeroderma Pigmentosum
van den Heuvel, A., Wondergem, A. P., Kim, M., Breet, I., Kim, H. S., Fawcett, H., Fassihi, H., Lehmann, A. R., Schärer, O. D., & Luijsterburg, M. S. (2025) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2025.08.047
Self-citationde Groot, B. A. F. J., van der Meer, P. J., van den Heuvel, D., & Luijsterburg, M. S. (2025) · STAR Protocols · doi:10.1016/j.xpro.2025.104213
Self-citation
Metadata
- Authors
- van der Weegen, Y., de Lint, K., van den Heuvel, D., Nakazawa, Y., Mevissen, T. E. T., van Schie, J. J. M., San Martin Alonso, M., Boer, D. E. C., González-Prieto, R., Narayanan, I. V., Klaassen, N. H. M., Wondergem, A. P., Roohollahi, K., Dorsman, J. C., Hara, Y., Vertegaal, A. C. O., de Lange, J., Walter, J. C., Noordermeer, S. M., Ljungman, M., Ogi, T., Wolthuis, R. M. F., & Luijsterburg, M. S.
- Affiliations
- Leiden University Medical Center (NL)
- Amsterdam University Medical Centers (NL)
- Research Institute of Environmental Medicine, Nagoya University (JP)
- Howard Hughes Medical Institute (US)
- University of Michigan (US)
- Corresponding author
- Wolthuis, Rob M. F.
- Luijsterburg, Martijn S.
- ORCID
- van der Weegen, Yana
- de Lint, Klaas
- van den Heuvel, Diana
- Nakazawa, Yuka
- Mevissen, Tycho E. T.
- van Schie, Janne J. M.
- Boer, Daphne E. C.
- González-Prieto, Román
- Narayanan, Ishwarya V.
- Klaassen, Noud H. M.
- Wondergem, Annelotte P.
- Dorsman, Josephine C.
- Hara, Yuichiro
- Vertegaal, Alfred C. O.
- de Lange, Job
- Walter, Johannes C.
- Noordermeer, Sylvie M.
- Ljungman, Mats
- Ogi, Tomoo
- Wolthuis, Rob M. F.
- Luijsterburg, Martijn S.
- Venue
- Nature Cell Biology
- Published
- 2021-06
- Volume
- 23
- Issue
- 6
- Pages
- 595-607
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC8890769
- OpenAlex
- W3170184056
- Cited by
- 114
- References
- 64
- Citations by year
- 2026: 22 · 2025: 29 · 2024: 27 · 2023: 17 · 2022: 11 · 2021: 8
- FWCI
- 4.94
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature Cell Biology (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Leiden Repository (Leiden University) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion, cc-by)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Amsterdam University Medical Centers
- Universiteit Leiden
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (ALW.016.161.320, 016.161.320, VI.Vidi.192.039, OCENW.KLEIN.090)
- Leids Universitair Medisch Centrum
- Japan Society for the Promotion of Science (18H03372, 20H00629, 21H02399, 21K19844)
- National Heart, Lung, and Blood Institute (R01HL098316)
- National Human Genome Research Institute (UM1HG009382)
- National Cancer Institute (R01CA213214)
- Topics
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- transcription-coupled repair, CSB, transcription elongation, R-loops, replication stress, transcriptional stress response, DNA damage response
- MeSH terms
- Poly-ADP-Ribose Binding Proteins, DNA Damage, DNA Repair, DNA Helicases, Humans, Protein Binding, RNA Polymerase II, Transcription Factors, Peptide Elongation Factor 1, Ubiquitin-Protein Ligases, DNA Repair Enzymes, Cell Line, Tumor, Receptors, Interleukin-17, Protein Interaction Domains and Motifs, Ubiquitination, Transcription Elongation, Genetic, CRISPR-Cas Systems
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