A CSB-PAF1C axis restores processive transcription elongation after DNA damage repair
Open accessPreprint — published as 10.1038/s41467-021-21520-w · Paper page
Abstract
The coordinated transcription of genes involves the regulated release of RNA polymerase II (RNAPII) from promoter-proximal sites into active elongation. DNA lesions in transcribed strands block elongation and induce a strong transcriptional arrest. The transcription-coupled repair (TCR) pathway efficiently removes transcription-blocking DNA lesions, but this is not sufficient to resume transcription. Through proteomics screens, we find that the TCR-specific CSB protein loads the evolutionary conserved PAF1 complex (PAF1C) onto RNAPII in promoter-proximal regions in response to DNA damage. PAF1C is dispensable for TCR-mediated repair, but is essential for recovery of RNA synthesis after UV irradiation, suggesting an uncoupling between DNA repair and transcription recovery. Moreover, we find that PAF1C promotes RNAPII pause release in promoter-proximal regions and subsequently acts as a processivity factor that stimulates transcription elongation throughout genes. Our findings expose the molecular basis for a non-canonical PAF1C-dependent pathway that restores transcription throughout the human genome after genotoxic stress.
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Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · 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
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382 · see citing works
The Perseus computational platform for comprehensive analysis of (prote)omics data
Tyanova, S., Temu, T., Sinitcyn, P. G., Carlson, A., Hein, M. Y., Geiger, T., Mann, M., & Cox, J. (2016) · Nature Methods · doi:10.1038/nmeth.3901 · Cited by 7,977 · see citing works
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · see citing works
Pérez-Riverol, Y., Csordas, A., Bai, J.-W., Bernal-Llinares, M., Hewapathirana, S., Kundu, D. J., Inuganti, A., Griss, J., Mayer, G., Eisenacher, M., et al. (2018) · Nucleic Acids Res. · doi:10.1093/nar/gky1106 · Cited by 6,216 · see citing works
Aligning sequence reads, clone sequences and assembly con*gs with BWA-MEMPreprint
Li, H. (2014) · arXiv (Cornell University) · doi:10.6084/m9.figshare.963153.v1 · Cited by 5,150 · see citing works
The MaxQuant computational platform for mass spectrometry-based shotgun proteomics
Tyanova, S., Temu, T., & Cox, J. (2016) · Nature Protocols · doi:10.1038/nprot.2016.136 · Cited by 4,691 · see citing works
Rappsilber, J., Mann, M., & Ishihama, Y. (2007) · Nature Protocols · doi:10.1038/nprot.2007.261 · Cited by 4,641 · see citing works
Understanding nucleotide excision repair and its roles in cancer and ageing
Marteijn, J. A., Lans, H., Vermeulen, W., & Hoeijmakers, J. H. J. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3822 · Cited by 1,192 · see citing works
Self-citationWada, T., Takagi, T., Yamaguchi, Y., Ferdous, A., Imai, T., Hirose, S., Sugimoto, S., Yano, K., Hartzog, G. A., Winston, F., et al. (1998) · Genes & Development · doi:10.1101/gad.12.3.343 · Cited by 750 · see citing works
Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J.-I., Saijo, M., Drapkin, R., Kisselev, A. F., Tanaka, K., & Nakatani, Y. (2003) · Cell · doi:10.1016/s0092-8674(03)00316-7 · Cited by 739 · see citing works
Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S. S., Shilatifard, A., & Reinberg, D. (2006) · Cell · doi:10.1016/j.cell.2006.04.029 · Cited by 708 · see citing works
Krogan, N. J., Dover, J., Wood, A., Schneider, J., Heidt, J. W., Boateng, M. A., Dean, K., Ryan, O. W., Golshani, A., Johnston, M., et al. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00091-1 · Cited by 706 · see citing works
Rapid protein depletion in human cells by auxin-inducible degron tagging with short homology donors
Natsume, T., Kiyomitsu, T., Saga, Y., & Kanemaki, M. T. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.001 · Cited by 673 · see citing works
Transcription regulation by the Mediator complex
Soutourina, J. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.115 · Cited by 591 · see citing works
DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy
Lehmann, A. (2003) · Biochimie · doi:10.1016/j.biochi.2003.09.010 · Cited by 496 · see citing works
Born to run: control of transcription elongation by RNA polymerase II
Chen, F. X., Smith, E. R., & Shilatifard, A. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0010-5 · Cited by 447 · see citing works
Structure of activated transcription complex Pol II–DSIF–PAF–SPT6
Vos, S. M., Farnung, L., Boehning, M., Wigge, C., Linden, A., Urlaub, H., & Cramer, P. (2018) · Nature · doi:10.1038/s41586-018-0440-4 · Cited by 432 · see citing works
Mayne, L. V., & Lehmann, A. R. (1982) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(82)90047-1 · Cited by 420 · see citing works
Structural basis of transcription initiation by RNA polymerase II
Sainsbury, S., Bernecky, C., & Cramer, P. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3952 · Cited by 397 · see citing works
Structure of paused transcription complex Pol II–DSIF–NELF
Vos, S. M., Farnung, L., Urlaub, H., & Cramer, P. (2018) · Nature · doi:10.1038/s41586-018-0442-2 · Cited by 378 · see citing works
Citterio, E., van den Boom, V., Schnitzler, G. R., Kanaar, R., Bonte, E. J., Kingston, R. E., Hoeijmakers, J. H. J., & Vermeulen, W. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.20.7643-7653.2000 · Cited by 371 · see citing works
Donahue, B. A., Yin, S., Taylor, J., Reines, D., & Hanawalt, P. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.18.8502 · Cited by 358 · see citing works
Blockage of RNA polymerase as a possible trigger for u.v. light-induced apoptosis.
Ljungman, M. E., & Zhang, F. (1996) · PubMed · Cited by 330 · see citing works
Self-citationCockayne syndrome group B protein enhances elongation by RNA polymerase II
Selby, C. P., & Sancar, A. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.21.11205 · Cited by 307 · see citing works
Adam, S., Polo, S. E., & Almouzni, G. (2013) · Cell · doi:10.1016/j.cell.2013.08.029 · Cited by 290 · see citing works
UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair
Schwertman, P., Lagarou, A., Dekkers, D. H. W., Raams, A., van der Hoek, A. C., Laffeber, C., Hoeijmakers, J. H. J., Demmers, J. A. A., Fousteri, M., Vermeulen, W., et al. (2012) · Nature Genetics · doi:10.1038/ng.2230 · Cited by 279 · see citing works
Self-citationFlavopiridol (L86 8275; NSC 649890), a new kinase inhibitor for tumor therapy
Sedlacek, H., Czech, J., Naik, R., Kaur, G., Worland, P., Losiewicz, M., Parker, B., Carlson, B., Smith, A., Senderowicz, A., et al. (1996) · International Journal of Oncology · doi:10.3892/ijo.9.6.1143 · Cited by 275 · see citing works
Kim, J., Guermah, M., & Roeder, R. G. (2010) · Cell · doi:10.1016/j.cell.2009.12.050 · Cited by 273 · see citing works
CPD Damage Recognition by Transcribing RNA Polymerase II
Brueckner, F., Hennecke, U., Carell, T., & Cramer, P. (2007) · Science · doi:10.1126/science.1135400 · Cited by 256 · see citing works
PAF1, a Molecular Regulator of Promoter-Proximal Pausing by RNA Polymerase II
Chen, F., Woodfin, A. R., Gardini, A., Rickels, R. A., Marshall, S. A., Smith, E. R., Shiekhattar, R., & Shilatifard, A. (2015) · Cell · doi:10.1016/j.cell.2015.07.042 · Cited by 253 · see citing works
Distribution and Repair of Bipyrimidine Photoproducts in Solar UV-irradiated Mammalian Cells
Perdiz, D., Gróf, P., Mezzina, M., Nikaido, O., Moustacchi, E., & Sage, E. (2000) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)61437-7 · Cited by 248 · see citing works
DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2APreprint
Bergink, S., Salomons, F. A., Hoogstraten, D., Groothuis, T. A., de Waard, H., Wu, J., Li, Y., Citterio, E., Houtsmuller, A. B., Neefjes, J., et al. (2006) · Genes & Development · doi:10.1101/gad.373706 · Cited by 247 · see citing works
Yu, M., Yang, W., Ni, T., Tang, Z., Nakadai, T., Zhu, J., & Roeder, R. G. (2015) · Science · doi:10.1126/science.aad2338 · Cited by 241 · see citing works
Mutation update for the CSB / ERCC6 and CSA / ERCC8 genes involved in Cockayne syndrome
Laugel, V., Dalloz, C., Durand, M., Sauvanaud, F., Kristensen, U., Vincent, M., Pasquier, L., Odent, S., Cormier‐Daire, V., Gener, B., et al. (2009) · Human Mutation · doi:10.1002/humu.21154 · Cited by 238 · see citing works
The human PAF complex coordinates transcription with events downstream of RNA synthesisPreprint
Zhu, B., Mandal, S. S., Pham, A.-D., Zheng, Y., Erdjument‐Bromage, H., Batra, S. K., Tempst, P., & Reinberg, D. (2005) · Genes & Development · doi:10.1101/gad.1292105 · Cited by 235 · see citing works
Ubiquitination of DNA Damage-Stalled RNAPII Promotes Transcription-Coupled Repair
Nakazawa, Y., Hara, Y., Oka, Y., Komine, O., van den Heuvel, D., Guo, C., Daigaku, Y., Isono, M., He, Y., Shimada, M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.02.010 · Cited by 229 · see citing works
Self-citationSarker, A. H., Tsutakawa, S. E., Kostek, S. A., Ng, C., Shin, D. S., Peris, M., Campeau, E., Tainer, J. A., Nogales, E., & Cooper, P. K. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.09.022 · Cited by 224 · see citing works
Nakazawa, Y., Sasaki, K., Mitsutake, N., Matsuse, M., Shimada, M., Nardò, T., Takahashi, Y., Ohyama, K., Ito, K., Mishima, H., et al. (2012) · Nature Genetics · doi:10.1038/ng.2229 · Cited by 213 · see citing works
Saponaro, M., Kantidakis, T., Mitter, R., Kelly, G. P., Heron, M., Williams, H., Söding, J., Stewart, A., & Svejstrup, J. Q. (2014) · Cell · doi:10.1016/j.cell.2014.03.048 · Cited by 207 · see citing works
Rockx, D., Mason, R. S., van Hoffen, A., Barton, M. C., Citterio, E., Bregman, D. B., van Zeeland, A. A., Vrieling, H., & Mullenders, L. H. F. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.180169797 · Cited by 203 · see citing works
Local UV‐induced DNA damage in cell nuclei results in local transcription inhibition
Moné, M. J., Volker, M., Nikaido, O., Mullenders, L. H. F., van Zeeland, A. A., Verschure, P. J., Manders, E. M. M., & DRIEL, R. V. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve224 · Cited by 202 · see citing works
Structural basis for the initiation of eukaryotic transcription-coupled DNA repair
Xu, J., Lahiri, I., Wang, W., Wier, A. D., Cianfrocco, M. A., Chong, J. P. C., Hare, A. A., Dervan, P. B., DiMaio, F., Leschziner, A. E., et al. (2017) · Nature · doi:10.1038/nature24658 · Cited by 202 · see citing works
Williamson, L. M., Saponaro, M., Boeing, S., East, P., Mitter, R., Kantidakis, T., Kelly, G. P., Lobley, A., Walker, J., Spencer‐Dene, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.01.019 · Cited by 197 · see citing works
Use of Bru-Seq and BruChase-Seq for genome-wide assessment of the synthesis and stability of RNA
Paulsen, M. T., Veloso, A., Prasad, J., Bedi, K., Ljungman, E. A., Magnuson, B., Wilson, T. E., & Ljungman, M. E. (2013) · Methods · doi:10.1016/j.ymeth.2013.08.015 · Cited by 194 · see citing works
Self-citationThe cooperative action of CSB, CSA, and UVSSA target TFIIH to DNA damage-stalled RNA polymerase II
van der Weegen, Y., Golan-Berman, H., Mevissen, T. E. T., Apelt, K., González‐Prieto, R., Goedhart, J., Heilbrun, E. E., Vertegaal, A. C. O., van den Heuvel, D., Walter, J. C., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15903-8 · Cited by 177 · see citing works
Self-citationJaspers, N. G. J., Raams, A., Kelner, M. J., Ng, J. M. Y., Yamashita, Y. M., Takeda, S., McMorris, T. C., & Hoeijmakers, J. H. J. (2002) · DNA repair · doi:10.1016/s1568-7864(02)00166-0 · Cited by 165 · see citing works
Cockayne syndrome B protein regulates the transcriptional program after UV irradiation
Proietti‐De‐Santis, L., Drané, P., & Egly, J. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601071 · Cited by 163 · see citing works
Structural basis of TFIIH activation for nucleotide excision repair
Kokic, G., Chernev, A., Tegunov, D., Dienemann, C., Urlaub, H., & Cramer, P. (2019) · Nature Communications · doi:10.1038/s41467-019-10745-5 · Cited by 163 · see citing works
L1Base 2: more retrotransposition-active LINE-1s, more mammalian genomes
Penzkofer, T., Jäger, M., Figlerowicz, M., Badge, R. M., Mundlos, S., Robinson, P. N., & Żemojtel, T. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw925 · Cited by 158 · see citing works
Enhanced Chromatin Dynamics by FACT Promotes Transcriptional Restart after UV-Induced DNA Damage
Dinant, C., Ampatziadis-Michailidis, G., Lans, H., Tresini, M., Lagarou, A., Grosbart, M., Theil, A. F., van Cappellen, W. A., Kimurâ, H., Bártek, J., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.08.007 · Cited by 145 · see citing works
Self-citationPAF1 regulation of promoter-proximal pause release via enhancer activation
Chen, F., Xie, P., Collings, C. K., Cao, K., Aoi, Y., Marshall, S. A., Rendleman, E. J., Ugarenko, M., Ozark, P. A., Zhang, A., et al. (2017) · Science · doi:10.1126/science.aan3269 · Cited by 134 · see citing works
Paf1C regulates RNA polymerase II progression by modulating elongation rate
Hou, L., Wang, Y., Liu, Y., Zhang, N., Shamovsky, I., Nudler, E., Tian, B., & Dynlacht, B. D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904324116 · Cited by 129 · see citing works
Mechanistic Interpretation of Promoter-Proximal Peaks and RNAPII Density Maps
Ehrensberger, A. H., Kelly, G. P., & Svejstrup, J. Q. (2013) · Cell · doi:10.1016/j.cell.2013.07.032 · Cited by 125 · see citing works
Chen, F., Gao, X., & Shilatifard, A. (2015) · Genes & Development · doi:10.1101/gad.246173.114 · Cited by 124 · see citing works
Albert, T., Rigault, C., Eickhoff, J., Baumgart, K., Antrecht, C., Klebl, B., Mittler, G., & Meisterernst, M. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12408 · Cited by 116 · see citing works
Spruijt, C. G., Luijsterburg, M. S., Menafra, R., Lindeboom, R. G. H., Jansen, P. W. T. C., Edupuganti, R. R., Baltissen, M. P. A., Wiegant, W. W., Voelker-Albert, M., Matarese, F., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.037 · Cited by 111 · see citing works
Self-citationCaron, P., Pankotai, T., Wiegant, W. W., Tollenaere, M. A. X., Furst, A., Bonhomme, C., Helfricht, A., de Groot, A., Pastink, A., Vertegaal, A. C. O., et al. (2019) · Genes & Development · doi:10.1101/gad.321943.118 · Cited by 110 · see citing works
Self-citationThe STUbL RNF4 regulates protein group SUMOylation by targeting the SUMO conjugation machinery
Kumar, R., González‐Prieto, R., Xiao, Z., Vries, M. V., & Vertegaal, A. C. O. (2017) · Nature Communications · doi:10.1038/s41467-017-01900-x · Cited by 110 · see citing works
Self-citationDysregulation of gene expression as a cause of Cockayne syndrome neurological disease
Wang, Y., Chakravarty, P., Ranes, M., Kelly, G. P., Brooks, P. J., Neilan, E. G., Stewart, A., Schiavo, G., & Svejstrup, J. Q. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1412569111 · Cited by 109 · see citing works
Epanchintsev, A., Costanzo, F., Rauschendorf, M., Caputo, M., Ye, T., Donnio, L., Proietti‐De‐Santis, L., Coin, F., Laugel, V., & Egly, J. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.11.009 · Cited by 101 · see citing works
P-TEFb Activation by RBM7 Shapes a Pro-survival Transcriptional Response to Genotoxic Stress
Bugai, A., Quaresma, A. J. C., Friedel, C. C., Lenasi, T., Düster, R., Sibley, C. R., Fujinaga, K., Kukanja, P., Hennig, T., Blasius, M., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.01.033 · Cited by 90 · see citing works
de Andrade-Lima, L. C., Veloso, A., Paulsen, M. T., Menck, C. F. M., & Ljungman, M. E. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv148 · Cited by 88 · see citing works
Self-citationp38-MK2 signaling axis regulates RNA metabolism after UV-light-induced DNA damage
Borisova, M. E., Voigt, A., Tollenaere, M. A. X., Sahu, S. K., Juretschke, T., Kreim, N., Mailand, N., Choudhary, C., Bekker‐Jensen, S., Akutsu, M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03417-3 · Cited by 82 · see citing works
Histone Methyltransferase DOT1L Drives Recovery of Gene Expression after a Genotoxic Attack
Oksenych, V., Zhovmer, A. S., Ziani, S., Mari, P., Eberová, J., Nardò, T., Stefanini, M., Giglia‐Mari, G., Egly, J., & Coin, F. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003611 · Cited by 78 · see citing works
Fitz, J., Neumann, T., & Pavri, R. (2018) · The EMBO Journal · doi:10.15252/embj.201797965 · Cited by 74 · see citing works
Chiou, Y., Hu, J., Sancar, A., & Selby, C. P. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000971 · Cited by 71 · see citing works
Fei, J., & Chen, J. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.398131 · Cited by 70 · see citing works
Structural insights into Paf1 complex assembly and histone binding
Chu, X., Qin, X., Xu, H., Li, L., Wang, Z., Li, F., Xie, X., Zhou, H., Shen, Y., & Long, J. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt819 · Cited by 69 · see citing works
Kristensen, U., Epanchintsev, A., Rauschendorf, M., Laugel, V., Stevnsner, T., Bohr, V. A., Coin, F., & Egly, J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220071110 · Cited by 61 · see citing works
H3K4me2 regulates the recovery of protein biosynthesis and homeostasis following DNA damage
Wang, S., Meyer, D. H., & Schumacher, B. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-00513-1 · Cited by 49 · see citing works
Cucinotta, C. E., Hildreth, A. E., McShane, B. M., Shirra, M. K., & Arndt, K. M. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz549 · Cited by 33 · see citing works
Wienholz, F., Vermeulen, W., & Marteijn, J. A. F. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1360 · Cited by 30 · see citing works
Self-citationCDK9 inhibition strategy defines distinct sets of target genes
Garriga, J., & Graña, X. (2014) · BMC Research Notes · doi:10.1186/1756-0500-7-301 · Cited by 26 · see citing works
Donnio, L., Lagarou, A., Sueur, G., Mari, P., & Giglia‐Mari, G. (2019) · Molecular and Cellular Biology · doi:10.1128/mcb.00225-18 · Cited by 8 · see citing works
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2 of the 78 references couldn’t be matched to a known paper.
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Structure of complete Pol II–DSIF–PAF–SPT6 transcription complex reveals RTF1 allosteric activation
Vos, S. M., Farnung, L., Linden, A., Urlaub, H., & Cramer, P. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0437-1 · Cited by 160 · see citing works
Structural basis of human transcription–DNA repair coupling
Kokić, G., Wagner, F., Chernev, A., Urlaub, H., & Cramer, P. (2021) · Nature · doi:10.1038/s41586-021-03906-4 · Cited by 137 · see citing works
Moreno, N. N., Olthof, A. M., & Svejstrup, J. Q. (2023) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052621-091205 · Cited by 115 · see citing works
Coordinated regulation of RNA polymerase II pausing and elongation progression by PAF1
Wang, Z., Song, A., Xu, H., Hu, S., Tao, B., Peng, L., Wang, J., Li, J., Yu, J., Wang, L., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm5504 · Cited by 62 · see citing works
Transcription-coupled DNA–protein crosslink repair by CSB and CRL4CSA-mediated degradation
van Sluis, M., Yu, Q. S., van der Woude, M., Gonzalo-Hansen, C., Dealy, S., Janssens, R. C., Somsen, H. B., Ramadhin, A. R., Dekkers, D. H. W., Wienecke, H. L., et al. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01394-y · Cited by 55 · see citing works
Self-citationJia, N., Guo, C., Nakazawa, Y., van den Heuvel, D., Luijsterburg, M. S., & Ogi, T. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103192 · Cited by 50 · see citing works
Self-citationSTK19 facilitates the clearance of lesion-stalled RNAPII during transcription-coupled DNA repair
(2024) · doi:10.1016/j.cell.2024.10.018 · Cited by 44 · see citing works
Self-citationReprogramming transcription after DNA damage: recognition, response, repair, and restart
Lu, H., Yang, M., & Zhou, Q. (2022) · Trends in Cell Biology · doi:10.1016/j.tcb.2022.11.010 · Cited by 40 · see citing works
Xu, J., Wang, W., Xu, L., Chen, J., Chong, J. P. C., Oh, J., Leschziner, A. E., Fu, X., & Wang, D. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2013379117 · Cited by 39 · see citing works
Bouvier, D., Ferrand, J., Chevallier, O., Paulsen, M. T., Ljungman, M. E., & Polo, S. E. (2021) · Nature Communications · doi:10.1038/s41467-021-24153-1 · Cited by 36 · see citing works
Self-citationElevated glucose increases genomic instability by inhibiting nucleotide excision repair
Ciminera, A. K., Shuck, S. C., & Termini, J. S. (2021) · Life Science Alliance · doi:10.26508/lsa.202101159 · Cited by 33 · see citing works
Transcription-coupled DNA double-strand break repair
Guha, S., & Bhaumik, S. R. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103211 · Cited by 32 · see citing works
Tan, Y., Gao, M., Huang, Y., Zhan, D., Wu, S., An, J., Zhang, X., & Hu, J. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae787 · Cited by 31 · see citing works
Ellison, M. A., Namjilsuren, S., Shirra, M. K., Blacksmith, M. S., Schusteff, R. A., Kerr, E. M., Fang, F., Xiang, Y., Shi, Y., & Arndt, K. M. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad180 · Cited by 26 · see citing works
Li, C., Guo, Y., Wang, L., & Yan, S. (2023) · The EMBO Journal · doi:10.15252/embj.2022112756 · Cited by 22 · see citing works
Spyropoulou, Z., Papaspyropoulos, A., Lаgopati, N., Myrianthopoulos, V., Georgakilas, A. G., Fousteri, M. I., Kotsinas, A., & Gorgoulis, V. G. (2021) · Cells · doi:10.3390/cells10040866 · Cited by 21 · see citing works
van den Heuvel, D., Kim, M., Wondergem, A. P., van der Meer, P. J., Witkamp, M., Lambregtse, F., Kim, H.-S., Kan, F., Apelt, K., Kragten, A., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2208860120 · Cited by 21 · see citing works
Self-citationJoecker, B., Baczewski, A., Gamble, J. K., Pla, J. J., Saraiva, A., & Morello, A. (2021) · New Journal of Physics · doi:10.1088/1367-2630/ac0abf · Cited by 20 · see citing works
The small CRL4CSA ubiquitin ligase component DDA1 regulates transcription-coupled repair dynamics
Llerena Schiffmacher, D. A., Lee, S.-H., Kliza, K. W., Theil, A. F., Akita, M., Helfricht, A., Bezstarosti, K., Gonzalo-Hansen, C., van Attikum, H., Verlaan-de Vries, M., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50584-7 · Cited by 19 · see citing works
Self-citationSwiatlowska, P., & Iskratsch, T. (2021) · Biophysical Reviews · doi:10.1007/s12551-021-00837-2 · Cited by 19 · see citing works
Sulfur ion irradiation experiments simulating space weathering of Solar System body surfaces
Ruf, A., Bouquet, A., Schmitt‐Kopplin, P., Boduch, P., Mousis, O. J., & Danger, G. (2021) · Astronomy and Astrophysics · doi:10.1051/0004-6361/202141190 · Cited by 18 · see citing works
Tiwari, V., Kulikowicz, T., Wilson, D. M., & Bohr, V. A. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab458 · Cited by 18 · see citing works
Elevated PAF1-RAD52 axis confers chemoresistance to human cancers
Rauth, S., Ganguly, K., Atri, P., Parte, S. C., Nimmakayala, R. K., Varadharaj, V., Nallasamy, P., Vengoji, R., Ogunleye, A. O., Lakshmanan, I., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112043 · Cited by 17 · see citing works
The molecular basis of human transcription-coupled DNA repair
van der Meer, P. J., & Luijsterburg, M. S. (2025) · Nature Cell Biology · doi:10.1038/s41556-025-01715-9 · Cited by 17 · see citing works
Self-citationAudrey, A., Kok, Y. P., Yu, S., de Haan, L., van de Kooij, B., van den Tempel, N., Chen, M., de Boer, H. R., van der Vegt, B., & van Vugt, M. A. T. M. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114116 · Cited by 15 · see citing works
Mechanisms of transcription-coupled repair and DNA damage surveillance in health and disease
van Sluis, M., Gonzalo-Hansen, C., Li, Q., Lans, H., Wang, D., & Marteijn, J. A. F. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-025-00915-3 · Cited by 21 · see citing works
Self-citationCS proteins and ubiquitination: orchestrating DNA repair with transcription and cell division
Costanzo, F., Paccosi, E., Proietti‐De‐Santis, L., & Egly, J. (2024) · Trends in Cell Biology · doi:10.1016/j.tcb.2024.06.002 · Cited by 14 · see citing works
DNA Damage-Induced RNAPII Degradation and Its Consequences in Gene Expression
Muñoz, J. C., Beckerman, I., Choudhary, R., Bouvier, L. A., & Muñoz, M. J. (2022) · Genes · doi:10.3390/genes13111951 · Cited by 12 · see citing works
Huang, Y., Gu, L., & Li, G. (2023) · Cell Discovery · doi:10.1038/s41421-023-00601-8 · Cited by 11 · see citing works
Keep calm and reboot – how cells restart transcription after DNA damage and DNA repair
Donnio, L., & Giglia‐Mari, G. (2024) · FEBS Letters · doi:10.1002/1873-3468.14964 · Cited by 11 · see citing works
The Paf1 complex is required for RNA polymerase II removal in response to DNA damage
Chen, F., Liu, B., Zhou, H., & Long, J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2207332119 · Cited by 11 · see citing works
Pal, S., & Biswas, D. (2023) · Gene · doi:10.1016/j.gene.2023.147571 · Cited by 11 · see citing works
Nucleolar Pol II interactome reveals TBPL1, PAF1, and Pol I at intergenic rDNA drive rRNA biogenesis
Khosraviani, N., Yerlici, V. T., St‐Germain, J. R., Hou, Y. Y., Cao, S. B., Ghali, C., Bokros, M., Krishnan, R., Hakem, R., Lee, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54002-w · Cited by 11 · see citing works
New roles for elongation factors in RNA polymerase II ubiquitylation and degradation
Reese, J. C. (2023) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2023.194956 · Cited by 10 · see citing works
Different elongation factors distinctly modulate RNA polymerase II transcription in Arabidopsis
Obermeyer, S., Schrettenbrunner, L., Stöckl, R., Schwartz, U., & Grasser, K. D. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad825 · Cited by 8 · see citing works
A genome-wide screen identifies SCAI as a modulator of the UV-induced replicative stress response
Lemay, J.-F., St-Hilaire, E., Ronato, D. A., Gao, Y., Bélanger, F., Gezzar-Dandashi, S., Ishimwe, A. B. K., Sawchyn, C., Lévesque, D., McQuaid, M. E., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001543 · Cited by 9 · see citing works
Live cell transcription-coupled nucleotide excision repair dynamics revisited
Schiffmacher, D. A. L., Kliza, K. W., Theil, A. F., Kremers, G., Demmers, J., Ogi, T., Vermeulen, M., Vermeulen, W., & Pines, A. (2023) · DNA repair · doi:10.1016/j.dnarep.2023.103566 · Cited by 8 · see citing works
Self-citationNusG–Spt5 Transcription Factors: Universal, Dynamic Modulators of Gene Expression
Mooney, R. A., Zhu, J., Saba, J., & Landick, R. C. (2024) · Journal of Molecular Biology · doi:10.1016/j.jmb.2024.168814 · Cited by 8 · see citing works
Transcription‐coupled repair: tangled up in convoluted repair
Schiffmacher, D. A. L., Pai, Y. J., Pines, A., & Vermeulen, W. (2025) · FEBS Journal · doi:10.1111/febs.70104 · Cited by 9 · see citing works
Cellular fractionation reveals transcriptome responses of human fibroblasts to UV-C irradiation
Liu, J., Wu, Z., He, J. H., & Wang, Y. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-04634-x · Cited by 8 · see citing works
Widening spinal injury research to consider all supraspinal cell types: Why we must and how we can
Blackmore, M. G., Batsel, E., & Tsoulfas, P. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113862 · Cited by 8 · see citing works
Ubiquitin-proteasome system regulation of a key gene regulatory factor, Paf1C
Barman, P., Ferdoush, J., Kaja, A., Chakraborty, P., Uprety, B., Bhaumik, R., Bhaumik, R., & Bhaumik, S. R. (2023) · Gene · doi:10.1016/j.gene.2023.148004 · Cited by 7 · see citing works
González-Vinceiro, L., Espejo-Serrano, C., Soler-Oliva, M. E., Soto-Hidalgo, E., Mateos‐Martín, M. L., Rico, D., González‐Aguilera, C., & González‐Prieto, R. (2025) · Science Advances · doi:10.1126/sciadv.ady4151 · Cited by 6 · see citing works
Self-citationRobu, M., Shah, R. G., van den Heuvel, D., Coulombe, Y., Bazin, M., van der Woude, M., Kragten, A., Lans, H., Pascal, J. M., Masson, J., et al. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf1303 · Cited by 6 · see citing works
Self-citationWang, X., Xue, Y., Li, L., Song, J., Jia, L., Xu, L. L., Fan, M., Lu, L., Su, W., Han, J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59578-5 · Cited by 5 · see citing works
Transcription and genome integrity
Ljungman, M. E. (2022) · DNA repair · doi:10.1016/j.dnarep.2022.103373 · Cited by 5 · see citing works
Self-citationHu, H., Zhang, Y., Yu, Y., Liu, D., Dong, Z., & Chen, G. (2025) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2025.140129 · Cited by 4 · see citing works
Integrator subunit INTS12 links ribotoxic stress to transcription-coupled nucleotide excision repair
Li, Z., Li, R., Yang, M., Huang, Y., Yang, J., Zhu, Q., Shao, Y., Zhao, W., Fu, H., Xiao, Y.-X., et al. (2026) · Nature Structural & Molecular Biology · doi:10.1038/s41594-026-01766-y · Cited by 4 · see citing works
The Archer and the Prey: The Duality of PAF1C in Antiviral Immunity
Kenaston, M. W., & Shah, P. S. (2023) · Viruses · doi:10.3390/v15051032 · Cited by 3 · see citing works
Decoding DNA repair regulation across human lifespan variability
Tang, Y., Zhang, D., Wang, K., Mao, Z., & Chen, Y. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102833 · Cited by 3 · see citing works
PAF1C restores transcription after DNA damage independently of promoting histone mark deposition
van Schie, J. J. M., de Groot, B. A. F. J., van den Heuvel, D., & Luijsterburg, M. S. (2026) · EMBO Reports · doi:10.1038/s44319-026-00761-0 · Cited by 2 · see citing works
Self-citationPAF1c depletion confers chemoresistance to topoisomerase inhibitors
Li, D., Zhu, C., Wang, T., 陈奇辉, & Chen, Q. (2026) · Cell Insight · doi:10.1016/j.cellin.2026.100332 · Cited by 2 · see citing works
Transcriptomic profiling implicates PAF1 in both active and repressive immune regulatory networks
Kenaston, M. W., Pham, O., Petit, M. J., & Shah, P. S. (2022) · BMC Genomics · doi:10.1186/s12864-022-09013-6 · Cited by 2 · see citing works
Wang, X., Zheng, R., Сергеевна, Д. М., Wang, L., Shen, Y., & Lin, Z. (2024) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b2300712 · Cited by 2 · see citing works
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 · see citing works
Self-citationLiakos, A., Ntakou‐Zamplara, K. Z., Angelova, N., Konstantopoulos, D., Synacheri, A., Spyropoulou, Z., Tsarmaklis, I. A., Korrou‐Karava, D., Nikolopoulos, G., Lavigne, M. D., et al. (2024) · Aging Cell · doi:10.1111/acel.14341 · Cited by 1 · see citing works
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 · see citing works
Spt6 directly interacts with Cdc73 and is required for Paf1C recruitment to active genesPreprint
Ellison, M. A., Blacksmith, M. S., Namjilsuren, S., Shirra, M. K., Schusteff, R. A., Kerr, E. M., Fang, F., Xiang, Y., Shi, Y., & Arndt, K. M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.04.490663 · Cited by 1 · see citing works
Reply to van Schie et al.: ARK2N in TCR: Across in vivo and in vitro studies
Luo, Y., Li, J., & Wang, J. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2426163122 · Cited by 1 · see citing works
González-Vinceiro, L., Espejo-Serrano, C., Soler-Oliva, M. E., Mateos‐Martín, M. L., Rico, D., González‐Aguilera, C., & González‐Prieto, R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.27.650851 · Cited by 1 · see citing works
Self-citationLemay, J.-F., St-Hilaire, E., Gezzar-Dandashi, S., McQuaid, M. E., Ronato, D. A., Gao, Y., Bélanger, F., Sawchyn, C., Ishimwe, A. B. K., Mallette, F. A., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.17.476707
Mooney, R. A., Zhu, J., Saba, J., & Landick, R. C. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4882915
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-citationThe NSL complex promotes neural development by preventing R-loop induced replication stressPreprint
Lingeman, J., van den Heuvel, D., van den Berg, J., Singh, J. K., van Hooijdonk, R., Wiegant, W. W., Boer, D. E. C., Lo, C. S. Y., Παναγόπουλος, Α., González‐Prieto, R., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.22.671281
Self-citationA chemical-genetic interaction between PAF1 and ENL/AF9 YEATS inhibition
Barta, P. A., Garnar-Wortzel, L., Bishop, T. R., Hayward, R. E., Hargis, L. M., Shaum, J. B., Kwok, H.-S., Liau, B. B., Cravatt, B. F., & Erb, M. A. (2025) · bioRxiv · doi:10.1039/d5cb00233h
Zhang, J., Xiang, X., Nie, X., Li, J., & Gui, R. (2025) · Open Research (University of Surrey) · doi:10.1002/viw.20250149
RNA degradation by DIS3 is a necessary step in the resolution of backtracked transcription complexes
Enervald, E., Jain, S., Tarbier, M., Sinha, I., Jain, A., Banerjee, P., Planells, J., McHugh, T., & Visa, N. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117886
Transcription in check at DNA double-strand breaks
Pradel, L., Marnef, A., & Legube, G. (2026) · Trends in Genetics · doi:10.1016/j.tig.2026.06.004
Li, D., Wang, X., Luo, H., Tu, H., Hao, L., Lei, I., Hu, R., Zheng, P., Shi, Y., Sun, J., et al. (2026) · Oncogene · doi:10.1038/s41388-026-03978-4
- Authors
- van den Heuvel, D., Spruijt, C. G., González-Prieto, R., Kragten, A., Paulsen, M. T., Zhou, D., Wu, H., Apelt, K., van der Weegen, Y., Yang, K., Dijk, M., Daxinger, L., Marteijn, J. A., Vertegaal, A. C. O., Ljungman, M., Vermeulen, M., & Luijsterburg, M. S.
- Affiliations
- Radboud University Nijmegen (NL)
- Leiden University Medical Center (NL)
- University of Michigan (US)
- Oncode Institute (NL)
- Corresponding author
- Luijsterburg, Martijn S.
- ORCID
- Venue
- Nature Communications
- Publisher
- openRxiv
- Published
- 2020-01-05
- Volume
- 12
- Issue
- 1
- Pages
- 1342-1342
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC7910549
- OpenAlex
- W3131547871
- Cited by
- 69
- References
- 78
- Citations by year
- 2026: 6 · 2025: 16 · 2024: 12 · 2023: 12 · 2022: 10 · 2021: 11 · 2020: 2
- FWCI
- 3.53
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (acceptedVersion, cc-by)
- Leiden Repository (Leiden University) (submittedVersion, cc-by)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- Universiteit Leiden
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (ALW.016.161.320, VI.C.182.025, 016.161.320)
- KWF Kankerbestrijding (11367)
- Leids Universitair Medisch Centrum
- Oncode Institute
- National Institute of General Medical Sciences (T32GM070449)
- FP7 Ideas: European Research Council (310913)
- 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 › Chromatin Remodeling and Cancer
- Keywords
- CSB, Paf1 complex, RNA polymerase II, transcription elongation, transcription-coupled repair, DNA damage, UV irradiation, promoter-proximal pausing, processivity factor, genotoxic stress, transcriptional arrest
- MeSH terms
- Poly-ADP-Ribose Binding Proteins, Cell Nucleus, DNA, DNA Damage, DNA Repair, DNA Helicases, Humans, RNA Polymerase II, Transcription Factors, Transcription, Genetic, Ultraviolet Rays, DNA Repair Enzymes, Protein Interaction Maps
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