ATR/Chk1 pathway is essential for resumption of DNA synthesis and cell survival in UV-irradiated XP variant cells
Abstract
DNA polymerase eta (poleta) performs translesion synthesis past ultraviolet (UV) photoproducts and is deficient in cancer-prone xeroderma pigmentosum variant (XP-V) syndrome. The slight sensitivity of XP-V cells to UV is dramatically enhanced by low concentrations of caffeine. So far, the biological explanation for this feature remains elusive. Using DNA combing, we showed that translesion synthesis defect leads to a strong reduction in the number of active replication forks and a high proportion of stalled forks in human cells, which contrasts with budding yeast. Moreover, extensive regions of single-strand DNA are formed during replication in irradiated XP-V cells, leading to an over-activation of ATR/Chk1 pathway after low UVC doses. Addition of a low concentration of caffeine post-irradiation, although inefficient to restore S-phase progression, significantly decreases Chk1 activation and abrogates DNA synthesis in XP-V cells. While inhibition of Chk1 activity by UCN-01 prevents UVC-induced S-phase delay in wild-type cells, it aggravates replication defect in XP-V cells by increasing fork stalling. Consequently, UCN-01 sensitizes XP-V cells to UVC as caffeine does. Our findings indicate that poleta acts at stalled forks to resume their progression, preventing the requirement for efficient replication checkpoint after low UVC doses. In the absence of poleta, Chk1 kinase becomes essential for replication resumption by alternative pathways, via fork stabilization.
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Polη ensures accurate replication of TT-CPDs, and its bypass may act at stalled replication forks and through post-replicative gap-filling.
“It is well established that Pol ensures accurate replication of TT-CPDs [21,22] and this bypass may act at the stalled replication fork [23,24] but also through a post-replicative gapfilling pathway [15,25].”
From Gap-filling and bypass at the replication fork are both active mechanisms for tolerance of low-dose ultraviolet-induced DNA damage in the human genome (2014) · cites this paper as [23]
UVC-induced γH2AX in Polη-deficient cells is associated with ssDNA generated by uncoupling of replicative DNA polymerase and helicase at stalled forks.
“UVC-induced ␥H2AX in Pol-deficient cells has also been previously associated with the generation of single-stranded DNA (ssDNA) caused by the uncoupling between the replicative DNA polymerase and the helicase at stalled replication forks [23,40,48]”
From Gap-filling and bypass at the replication fork are both active mechanisms for tolerance of low-dose ultraviolet-induced DNA damage in the human genome (2014) · cites this paper as [23]
Cites
Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes
Zou, L., & Elledge, S. J. (2003) · Science · doi:10.1126/science.1083430 · Cited by 2,693 · see citing works
ATR: an essential regulator of genome integrity
Cimprich, K. A., & Cortez, D. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2450 · Cited by 1,798 · see citing works
(1999) · PubMed · Cited by 1,030 · see citing works
The Y-Family of DNA Polymerases
Ohmori, H., Friedberg, E. C., Fuchs, R. P., Goodman, M. F., Hanaoka, F., Hinkle, D. C., Kunkel, T. A., Lawrence, C. W., Livneh, Z., Nohmi, T., et al. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00278-7 · Cited by 882 · see citing works
Interaction of Human DNA Polymerase η with Monoubiquitinated PCNA
Kannouche, P. L., Wing, J., & Lehmann, A. R. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00259-x · Cited by 845 · see citing works
Self-citationRapid Destruction of Human Cdc25A in Response to DNA Damage
Mailand, N., Falck, J., Lukas, C., Syljuåsen, R. G., Welcker, M., Bartek, J., & Lukas, J. (2000) · Science · doi:10.1126/science.288.5470.1425 · Cited by 787 · see citing works
Byun, T. S., Pacek, M., Yee, M.-C., Walter, J. C., & Cimprich, K. A. (2005) · Genes & Development · doi:10.1101/gad.1301205 · Cited by 767 · see citing works
<i>hRAD30</i> Mutations in the Variant Form of Xeroderma Pigmentosum
Johnson, R. E., Kondratick, C. M., Prakash, S., & Prakash, L. (1999) · Science · doi:10.1126/science.285.5425.263 · Cited by 732 · see citing works
The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair
Sørensen, C. S., Hansen, L. T., Dziegielewski, J., Syljuåsen, R. G., Lundin, C., Bartek, J., & Helleday, T. (2005) · Nature Cell Biology · doi:10.1038/ncb1212 · Cited by 666 · see citing works
Lehman, A. R., Kirk-Bell, S., Arlett, C. F., Paterson, M. C., Lohman, P. H., de Weerd-Kastelein, E. A., & Bootsma, D. (1975) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.72.1.219 · Cited by 614 · see citing works
Lopes, M., Foiani, M., & Sogo, J. M. (2006) · Molecular Cell · doi:10.1016/j.molcel.2005.11.015 · Cited by 563 · see citing works
Mechanisms of accurate translesion synthesis by human DNA polymerase η
Masutani, C., Kusumoto, R., Iwai, S., & Hanaoka, F. (2000) · The EMBO Journal · doi:10.1093/emboj/19.12.3100 · Cited by 504 · see citing works
Trading Places: How Do DNA Polymerases Switch during Translesion DNA Synthesis?
Friedberg, E. C., Lehmann, A. R., & Fuchs, R. P. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.03.032 · Cited by 376 · see citing works
Raderschall, E., Golub, E. I., & Haaf, T. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.1921 · Cited by 350 · see citing works
(2000) · PubMed · Cited by 314 · see citing works
Ünsal-Kaçmaz, K., Chastain, P. D., Qu, P.-P., Minoo, P., Cordeiro-Stone, M., Sancar, A., & Kaufmann, W. K. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02190-06 · Cited by 240 · see citing works
The structural determinants of checkpoint activation
MacDougall, C. A., Byun, T. S., Van, C., Yee, M.-C., & Cimprich, K. A. (2007) · Genes & Development · doi:10.1101/gad.1522607 · Cited by 240 · see citing works
Edmunds, C. E., Simpson, L. J., & Sale, J. E. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.03.024 · Cited by 239 · see citing works
Chk1 regulates the density of active replication origins during the vertebrate S phase
Maya‐Mendoza, A., Petermann, E., Gillespie, D. A., Caldecott, K. W., & Jackson, D. A. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601714 · Cited by 236 · see citing works
Conti, C., Saccà, B., Herrick, J., Lalou, C., Pommier, Y. G., & Bensimon, A. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-08-0689 · Cited by 236 · see citing works
Visualization of Altered Replication Dynamics after DNA Damage in Human Cells
Merrick, C. J., Jackson, D. A., & Diffley, J. F. X. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400022200 · Cited by 228 · see citing works
Trenz, K., Smith, E., Smith, S. J., & Costanzo, V. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601045 · Cited by 219 · see citing works
Limoli, C. L., Giedzinski, E., Bonner, W. M., & Cleaver, J. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.231611798 · Cited by 210 · see citing works
Phosphorylation of the Bloom's Syndrome Helicase and Its Role in Recovery from S-Phase Arrest
Davies, S. L., North, P. S., Dart, D. A., Lakin, N. D., & Hickson, I. D. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.3.1279-1291.2004 · Cited by 208 · see citing works
Structural Basis for Chk1 Inhibition by UCN-01
Zhao, B., Bower, M. J., McDevitt, P. J., Zhao, H., Davis, S. T., Johanson, K., Green, S. M., Concha, N. O., & Zhou, B. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m201233200 · Cited by 206 · see citing works
DNA damage tolerance: when it's OK to make mistakes
Chang, D. J., & Cimprich, K. A. (2009) · Nature Chemical Biology · doi:10.1038/nchembio.139 · Cited by 203 · see citing works
Petermann, E., Maya‐Mendoza, A., Zachos, G., Gillespie, D. A., Jackson, D. A., & Caldecott, K. W. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.8.3319-3326.2006 · Cited by 181 · see citing works
The enigmatic effects of caffeine in cell cycle and cancer
Bode, A. M., & Dong, Z. (2006) · Cancer Letters · doi:10.1016/j.canlet.2006.03.032 · Cited by 177 · see citing works
Dimitrova, D. S., & Gilbert, D. M. (2000) · Nature Cell Biology · doi:10.1038/35036309 · Cited by 160 · see citing works
Control of Replication Origin Density and Firing Time in Xenopus Egg Extracts
Marheineke, K., & Hyrien, O. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m401574200 · Cited by 152 · see citing works
Self-citationPhosphorylation activates Chk1 and is required for checkpoint-mediated cell cycle arrest
Capasso, H., Palermo, C., Wan, S., Rao, H., John, U. P., O’Connell, M. J., & Walworth, N. C. (2002) · Journal of Cell Science · doi:10.1242/jcs.00133 · Cited by 147 · see citing works
Arlett, C. F., Harcourt, S. A., & Broughton, B. C. (1975) · Mutation Research · doi:10.1016/0027-5107(75)90209-2 · Cited by 140 · see citing works
Role of DNA Polymerase η in the UV Mutation Spectrum in Human Cells
Stary, A., Kannouche, P. L., Lehmann, A. R., & Sarasin, A. R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211838200 · Cited by 127 · see citing works
Self-citationPichierri, P., Rosselli, F., & Franchitto, A. (2003) · Oncogene · doi:10.1038/sj.onc.1206169 · Cited by 125 · see citing works
Replication Fork Bypass of a Pyrimidine Dimer Blocking Leading Strand DNA Synthesis
Cordeiro‐Stone, M., Zaritskaya, L., Price, L. K., & Kaufmann, W. K. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.21.13945 · Cited by 123 · see citing works
Ziv, O., Geacintov, N. E., Nakajima, S., Yasui, A., & Livneh, Z. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812548106 · Cited by 123 · see citing works
Kaufmann, W. K., & Cleaver, J. E. (1981) · Journal of Molecular Biology · doi:10.1016/0022-2836(81)90297-7 · Cited by 121 · see citing works
Chk1 and Claspin potentiate PCNA ubiquitination
Yang, X. H., Shiotani, B., Classon, M., & Zou, L. (2008) · Genes & Development · doi:10.1101/gad.1632808 · Cited by 111 · see citing works
Cordeiro‐Stone, M., Makhov, A. M., Zaritskaya, L., & Griffith, J. D. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1999.2847 · Cited by 102 · see citing works
Block, W. D. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh508 · Cited by 90 · see citing works
Bomgarden, R. D., Lupardus, P. J., Soni, D. V., Yee, M., Ford, J. M., & Cimprich, K. A. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601123 · Cited by 87 · see citing works
Rao, V. A., Conti, C., Guirouilh‐Barbat, J., Nakamura, A., Miao, Z., Davies, S., Saccà, B., Hickson, I. D., Bensimon, A., & Pommier, Y. G. (2007) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-07-0028 · Cited by 86 · see citing works
Olson, E. E., Nievera, C. J., Lee, A. Y., Chen, L., & Wu, X. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702162200 · Cited by 81 · see citing works
Rudé, J. M., & Friedberg, E. C. (1977) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(77)80047-x · Cited by 80 · see citing works
Labit, H., Goldar, A., Guilbaud, G., Douarche, C., Hyrien, O., & Marheineke, K. (2008) · BioTechniques · doi:10.2144/000113002 · Cited by 65 · see citing works
Self-citationSingle DNA molecule analysis: Applications of molecular combing
Lebofsky, R. (2003) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/1.4.385 · Cited by 61 · see citing works
Pagès, V., Santa Maria, S. R., Prakash, L., & Prakash, S. (2009) · Genes & Development · doi:10.1101/gad.1793409 · Cited by 55 · see citing works
Checkpoint Regulation of Replication Dynamics in UV-Irradiated Human Cells
Chastain, P. D., Heffernan, T. P., Nevis, K. R., Li, L., Kaufmann, W. K., Kaufman, D. G., & Cordeiro‐Stone, M. (2006) · Cell Cycle · doi:10.4161/cc.5.18.3236 · Cited by 52 · see citing works
DNA damage responses protect xeroderma pigmentosum variant from UVC-induced clastogenesis
Cordeiro‐Stone, M., Frank, A. R., Bryant, M. F., Oguejiofor, I., Hatch, S. B., McDaniel, L. D., & Kaufmann, W. K. (2002) · Carcinogenesis · doi:10.1093/carcin/23.6.959 · Cited by 33 · see citing works
UV-induced RPA phosphorylation is increased in the absence of DNA polymerase η and requires DNA-PK
Cruet-Hennequart, S., Coyne, S., Glynn, M. T., Oakley, G. G., & Carty, M. P. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.01.008 · Cited by 28 · see citing works
Alternative recombination pathways in UV-irradiated XP variant cells
Limoli, C. L., Giedzinski, E., & Cleaver, J. E. (2005) · Oncogene · doi:10.1038/sj.onc.1208515 · Cited by 26 · see citing works
Bullock, S. K., Kaufmann, W. K., & Cordeiro‐Stone, M. (2001) · Carcinogenesis · doi:10.1093/carcin/22.2.233 · Cited by 17 · see citing works
Matsudaira, Y., & YAMASAKI, T. (1975) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(75)90291-2 · Cited by 4 · see citing works
Flagged first, then by citations
1 of the 54 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
PrimPol Bypasses UV Photoproducts during Eukaryotic Chromosomal DNA Replication
Bianchi, J., Rudd, S. G., Jóźwiakowski, S. K., Bailey, L. J., Soura, V., Taylor, E. M., Stevanović, I., Green, A., Stracker, T. H., Lindsay, H. D., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.035 · Cited by 294 · see citing works
The causes of replication stress and their consequences on genome stability and cell fate
Magdalou, I., López, B. S., Pasero, P., & Lambert, S. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.04.035 · Cited by 157 · see citing works
Guilbaud, G., Rappailles, A., Baker, A., Chen, C.-L., Arnéodo, A., Goldar, A., d’Aubenton-Carafa, Y., Thermes, C., Audit, B., & Hyrien, O. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002322 · Cited by 148 · see citing works
Self-citationUV stalled replication forks restart by re-priming in human fibroblasts
Elvers, I., Johansson, F., Groth, P., Erixon, K., & Helleday, T. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr420 · Cited by 120 · see citing works
Mutations in DONSON disrupt replication fork stability and cause microcephalic dwarfism
Reynolds, J. J., Bicknell, L. S., Carroll, P., Higgs, M. R., Shaheen, R., Murray, J., Papadopoulos, D. K., Leitch, A., Murina, O., Tarnauskaitė, Ž., et al. (2017) · Nature Genetics · doi:10.1038/ng.3790 · Cited by 119 · see citing works
To skip or not to skip: choosing repriming to tolerate DNA damage
Quinet, A., Tirman, S., Cybulla, E., Meroni, A., & Vindigni, A. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.01.012 · Cited by 109 · see citing works
γH2Ax: Biomarker of Damage or Functional Participant in DNA Repair “All that Glitters Is not Gold!”
Cleaver, J. E. (2011) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2011.00995.x · Cited by 112 · see citing works
Analysis of DNA replication profiles in budding yeast and mammalian cells using DNA combing
Bianco, J. N., Poli, J., Saksouk, J., Bacal, J., Silva, M. J., Yoshida, K., Lin, Y., Tourrière, H., Lengronne, A., & Pasero, P. (2012) · Methods · doi:10.1016/j.ymeth.2012.04.007 · Cited by 111 · see citing works
Moiseeva, T. N., Hood, B. L., Schamus, S., O’Connor, M. J., Conrads, T. P., & Bakkenist, C. J. (2017) · Nature Communications · doi:10.1038/s41467-017-01401-x · Cited by 99 · see citing works
TRAIP promotes DNA damage response during genome replication and is mutated in primordial dwarfism
Harley, M. E., Murina, O., Leitch, A., Higgs, M. R., Bicknell, L. S., Yigit, G., Blackford, A. N., Zlatanou, A., Mackenzie, K. J., Reddy, K., et al. (2015) · Nature Genetics · doi:10.1038/ng.3451 · Cited by 92 · see citing works
Translesion synthesis mechanisms depend on the nature of DNA damage in UV-irradiated human cells
Quinet, A., Martins, D. J., Vessoni, A. T., Biard, D., Sarasin, A., Stary, A., & Menck, C. F. M. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw280 · Cited by 76 · see citing works
Spartan/C1orf124 is important to prevent UV-induced mutagenesis
Machida, Y., Kim, M. S., & Machida, Y. (2012) · Cell Cycle · doi:10.4161/cc.21694 · Cited by 77 · see citing works
Roles of trans-lesion synthesis (TLS) DNA polymerases in tumorigenesis and cancer therapy
Anand, J. R., Chiou, L. F., Sciandra, C. A., Zhang, X., Hong, J., Wu, D., Zhou, P., & Vaziri, C. (2023) · NAR Cancer · doi:10.1093/narcan/zcad005 · Cited by 73 · see citing works
Despras, E., Sittewelle, M., Pouvelle, C., Delrieu, N., Cordonnier, A. M., & Kannouche, P. L. (2016) · Nature Communications · doi:10.1038/ncomms13326 · Cited by 74 · see citing works
Self-citationQuinet, A., Vessoni, A. T., Rocha, C. R. R., Gottifredi, V., Biard, D., Sarasin, A., Menck, C. F. M., & Stary, A. (2014) · DNA Repair · doi:10.1016/j.dnarep.2013.12.005 · Cited by 70 · see citing works
The fork and the kinase: A DNA replication tale from a CHK1 perspective
Besteiro, M. A. G., & Gottifredi, V. (2014) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2014.10.003 · Cited by 71 · see citing works
The 6-4 Photoproduct Is the Trigger of UV-Induced Replication Blockage and ATR Activation
Hung, K.-F., Sidorova, J. M., Nghiem, P., & Kawasumi, M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1917196117 · Cited by 64 · see citing works
Bailey, L. J., Bianchi, J., & Doherty, A. J. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz056 · Cited by 60 · see citing works
Lerner, L. K., Francisco, G., Soltys, D. T., Rocha, C. R. R., Quinet, A., Vessoni, A. T., Castro, L. P., David, T. I. P., Bustos, S. O., Strauss, B. E., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1196 · Cited by 53 · see citing works
“In agreement with previous reports (34,35), we speculate that the increased DNA damage tolerance capacity in pre-treated samples would lead to less checkpoint activation (due to less ssDNA that could activate ATR), meaning that pol eta is key to maintain the homeostasis of the cell cycle progression (right number of e…”
Hedglin, M., & Benkovic, S. J. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00046 · Cited by 50 · see citing works
Kinase-independent function of checkpoint kinase 1 (Chk1) in the replication of damaged DNA
Speroni, J., Federico, M. B., Mansilla, S. F., Soria, G., & Gottifredi, V. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1116345109 · Cited by 51 · see citing works
Diverse roles of RAD18 and Y-family DNA polymerases in tumorigenesis
Yang, Y., Gao, Y., Zlatanou, A., Tateishi, S., Yurchenko, V., Rogozin, I. B., & Vaziri, C. (2018) · Cell Cycle · doi:10.1080/15384101.2018.1456296 · Cited by 51 · see citing works
SPRTN protease and checkpoint kinase 1 cross-activation loop safeguards DNA replication
Halder, S., Torrecilla, I., Burkhalter, M. D., Popović, M., Fielden, J., Vaz, B., Oehler, J., Pilger, D., Lessel, D., Wiseman, K., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11095-y · Cited by 44 · see citing works
Tsanov, N., Kermi, C., Coulombe, P., van der Laan, S., Hodroj, D., & Maiorano, D. (2014) · Nucleic Acids Research · doi:10.1093/nar/gkt1400 · Cited by 48 · see citing works
Opletalova, K., Bourillon, A., Yang, W., Pouvelle, C., Armier, J., Despras, E., Martin, L., Mateus, C., Robert, C., Kannouche, P. L., et al. (2013) · Human Mutation · doi:10.1002/humu.22462 · Cited by 47 · see citing works
Self-citationKrijger, P. H. L., van den Berk, P. C. M., Wit, N., Langerak, P., Jansen, J. G., Reynaud, C., de Wind, N., & Jacobs, H. (2011) · DNA repair · doi:10.1016/j.dnarep.2011.08.005 · Cited by 45 · see citing works
Ray, A., Blevins, C., Wani, G., & Wani, A. A. (2016) · PLOS ONE · doi:10.1371/journal.pone.0159344 · Cited by 44 · see citing works
Filling gaps in translesion DNA synthesis in human cells
Quinet, A., Lerner, L. K., Martins, D. J., & Menck, C. F. M. (2018) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2018.02.004 · Cited by 41 · see citing works
Maiorano, D., Etri, J. E., Franchet, C., & Hoffmann, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22083924 · Cited by 41 · see citing works
p53 activates G1 checkpoint following DNA damage by doxorubicin during transient mitotic arrest
Hyun, S., & Jang, Y. (2014) · Oncotarget · doi:10.18632/oncotarget.3103 · Cited by 37 · see citing works
Despras, E., Delrieu, N., Garandeau, C., Ahmed‐Seghir, S., & Kannouche, P. L. (2012) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21741 · Cited by 35 · see citing works
Self-citationAuclair, Y., Rouget, R., Belisle, J. M., Costantino, S., & Drobetsky, E. A. (2010) · DNA Repair · doi:10.1016/j.dnarep.2010.03.013 · Cited by 34 · see citing works
Villafañez, F., García, I. A., Carbajosa, S., Pansa, M. F., Mansilla, S., Llorens, M. C., Angiolini, V., Guantay, L., Jacobs, H., Madauss, K. P., et al. (2019) · Oncogene · doi:10.1038/s41388-019-0724-7 · Cited by 30 · see citing works
PrimPol-deficient cells exhibit a pronounced G2 checkpoint response following UV damage
Bailey, L. J., Bianchi, J., Hégarat, N., Hochegger, H., & Doherty, A. J. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1128597 · Cited by 30 · see citing works
Jansen, J. G., Temviriyanukul, P., Wit, N., Delbos, F., Reynaud, C., Jacobs, H., & de Wind, N. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku779 · Cited by 30 · see citing works
GENETIC VARIATION AND DNA REPLICATION TIMING, OR WHY IS THERE LATE REPLICATING DNA?
Herrick, J. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01407.x · Cited by 29 · see citing works
Elvers, I., Hagenkort, A., Johansson, F., Djureinovic, T., Lagerqvist, A., Schultz, N., Stoimenov, I., Erixon, K., & Helleday, T. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks646 · Cited by 27 · see citing works
Spatiotemporal regulation of PCNA ubiquitination in damage tolerance pathways
Masuda, Y., & Masutani, C. (2019) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2019.1687420 · Cited by 26 · see citing works
Bélanger, F., Angers, J.-P., Fortier, É., Hammond-Martel, I., Costantino, S., Drobetsky, E., & Wurtele, H. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.685883 · Cited by 24 · see citing works
Bournique, E., Dall’Osto, M., Hoffmann, J., & Bergoglio, V. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.08.002 · Cited by 23 · see citing works
Sokòl, A. M., Cruet-Hennequart, S., Pasero, P., & Carty, M. P. (2013) · Scientific Reports · doi:10.1038/srep03277 · Cited by 23 · see citing works
Bénureau, Y., Pouvelle, C., Dupaigne, P., Baconnais, S., Tavares, E. M., Mazón, G., Despras, E., Cam, É. L., & Kannouche, P. L. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac746 · Cited by 22 · see citing works
Self-citationRenaud, E., & Rosselli, F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053693 · Cited by 20 · see citing works
Polymerase η suppresses telomere defects induced by DNA damaging agents
Pope-Varsalona, H., Liu, F., Guzik, L. J., & Opresko, P. L. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1030 · Cited by 20 · see citing works
Li, X., Ren, J., Chen, P., Chen, Y., Wu, M. C., Wu, Y., Chen, K., & Li, J. (2018) · Acta Pharmacologica Sinica · doi:10.1038/aps.2017.187 · Cited by 19 · see citing works
Immunofluorescence microscopy-based detection of ssDNA foci by BrdU in mammalian cells
Kilgas, S., Kiltie, A. E., & Ramadan, K. (2021) · STAR Protocols · doi:10.1016/j.xpro.2021.100978 · Cited by 17 · see citing works
de Andrade-Lima, L. C., Andrade, L. N. D. S., & Menck, C. F. M. (2014) · Journal of Cell Science · doi:10.1242/jcs.161596 · Cited by 15 · see citing works
Menck, C. F. M., Galhardo, R. S., & Quinet, A. (2023) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2023.111840 · Cited by 14 · see citing works
Papel das proteínas XPD e DNA polimerase eta nas respostas de células humanas a danos no genoma
Lerner, L. K. (2014) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.5.2014.tde-20102014-103732 · Cited by 13 · see citing works
Efeitos da luz UVA em células de pacientes com Xeroderma Pigmentosum Variante
Moreno, N. C. (2018) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.41.2018.tde-22012018-162542 · Cited by 13 · see citing works
Federico, M. B., Siri, S. O., Calzetta, N. L., Paviolo, N. S., de la Vega, M. B., Martino, J., Campana, M. C., Wiesmüller, L., & Gottifredi, V. (2020) · Oncogene · doi:10.1038/s41388-020-1265-9 · Cited by 12 · see citing works
Transcriptional repression upon S phase entry protects genome integrity in pluripotent cells
Gökbuget, D., Lenshoek, K., Boileau, R. M., Bayerl, J., Huang, H. H., Wiita, A. P., Laird, D. J., & Blelloch, R. H. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01092-7 · Cited by 10 · see citing works
Dall’Osto, M., Pierini, L., Valery, N., Hoffmann, J., & Pillaire, M. (2021) · Molecular and Cellular Biology · doi:10.1128/mcb.00090-21 · Cited by 9 · see citing works
Stow, E. C., Simmons, J. R., An, R., Schoborg, T. A., Davenport, N. M., & Labrador, M. (2019) · Gene · doi:10.1016/j.gene.2022.146208 · Cited by 9 · see citing works
Ahmed‐Seghir, S., Pouvelle, C., Despras, E., Cordonnier, A. M., Sarasin, A. R., & Kannouche, P. L. (2015) · DNA repair · doi:10.1016/j.dnarep.2015.02.017 · Cited by 9 · see citing works
Self-citationMoreno, N. C., Garcia, C. C. M., Rocha, C. R. R., Munford, V., & Menck, C. F. M. (2018) · Photochemistry and Photobiology · doi:10.1111/php.13041 · Cited by 9 · see citing works
Mutations in the insulator protein Suppressor of Hairy wing induce genome instability
Hsu, S.-J., Stow, E. C., Simmons, J. R., Wallace, H. A., Lopez, A. A., Stroud, S., & Labrador, M. (2020) · Chromosoma · doi:10.1007/s00412-020-00743-8 · Cited by 7 · see citing works
Caffeine Abolishes the Ultraviolet-Induced REV3 Translesion Replication Pathway in Mouse Cells
Takezawa, J., Aiba, N., Kajiwara, K., & Yamada, K. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12128513 · Cited by 7 · see citing works
Bénureau, Y., Tavares, E. M., Muhammad, A., Baconnais, S., Cam, É. L., & Pauline, D. (2020) · Biology Methods and Protocols · doi:10.1093/biomethods/bpaa012 · Cited by 7 · see citing works
Human TLS DNA polymerase: saviors or threats under replication stress?
Rajpurohit, Y. S., Lal, M., Sharma, D. K., & Soni, I. (2025) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-025-05291-2 · Cited by 6 · see citing works
Yamashita, T., Okura, M., Ishii‐Osai, Y., & Hida, T. (2016) · The Journal of Dermatology · doi:10.1111/1346-8138.13333 · Cited by 3 · see citing works
Bénureau, Y., Pouvelle, C., Tavares, E. M., Pauline, D., Despras, E., Cam, É. L., & Kannouche, P. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.12.336107 · Cited by 2 · see citing works
Self-citationREV7 associates with ATRIP and inhibits ATR kinase activity
Biller, M., Kabir, S., Nipper, S., Allen, S., Kayali, Y., Kuncik, S., Sasanuma, H., Zhou, P., Vaziri, C., & Tomida, J. (2026) · Nucleic Acids Research · doi:10.1093/nar/gkaf1527 · Cited by 1 · see citing works
Gan, W., Wang, L., Bhoopalan, V., Xi, Y., Bhalla, D. K., Wang, D., & Xu, X. (2013) · Open Journal of Genetics · doi:10.4236/ojgen.2013.34032 · Cited by 1 · see citing works
CTF18 interacts with replication protein A in response to replication stress
Kaneko, Y., Daitoku, H., Komeno, C., & Fukamizu, A. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.5262 · Cited by 1 · see citing works
Xeroderma Pigmentosum and the DNA Damage Response to Ultraviolet Light
Cleaver, J. E. (2016) · Springer eBooks · doi:10.1007/978-1-59745-458-2_24 · Cited by 1 · see citing works
Coupling of translesion synthesis with the replisome stabilized at stalled replication forks by ATRPreprint
Yoon, J.-H., Karthi, S., Johnson, R. E., Prakash, L., & Prakash, S. (2026) · Genes & Development · doi:10.1101/gad.353474.125 · Cited by 1 · see citing works
Lima, L. C. D. A. (2014) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2014.tde-28112014-100235
Vessoni, A. T. (2015) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2015.tde-06102015-200543
Studies on Molecular Basis for FOXO1-DNA Damage Responses
悠太, 金. (2016) · Terrestrial Environment Research Center (University of Tsukuba)
Okuda, M., Fujii, M., Kawasumi, R., & Hirota, K. (2025) · DNA repair · doi:10.1016/j.dnarep.2025.103919
Norris, J. L., Rogers, L. O., Young, G., Pytko, K. G., Dannenberg, R. L., Perreault, S., Kaushik, V., Antony, E., & Hedglin, M. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf1478
Tsanov, N. (2012) · theses.fr (ABES) · doi:10.70675/2122f712z2f95z45caz8f82za68872f01e3c
Role of CTF18 and SAMHD1 in human DNA replication and genome integrity maintenance
Silva, M. J. (2014) · theses.fr (ABES) · doi:10.70675/988b3c5fzb231z4dbfz989cz8f4343b71a76
Caractérisation fonctionnelle de la tolérance aux endommagements de l’ADN des embryons précoces
Furno, E. L. (2019) · theses.fr (ABES) · doi:10.70675/cf32bcd5z3031z4693z8b1bz62fe76673ccc
Régulation des étapes précoces de la recombinaison homologue humaine par BRCA2 et RAD52
Muhammad, A. (2021) · theses.fr (ABES) · doi:10.70675/2a4e3f69zfa80z4fbcz832fzafaf38393628
Simmons, J. R., Kemp, J. D. J., & Labrador, M. (2026) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkag185 · Cited by 1 · see citing works
Sakurai, Y., Yokoi, M., Sugimoto, T., Ohkumo, T., 森田, 大., Tsukamoto, T., Oda, T., Gi, M., Kakehashi, A., Yamashita, T., et al. (2026) · DNA repair · doi:10.1016/j.dnarep.2026.103974
- Authors
- Despras, E., Daboussi, F., Hyrien, O., Marheineke, K., & Kannouche, P. L.
- Affiliations
- Université Paris-Sud (FR)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Kannouche, Patricia L.
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-02-01
- Volume
- 19
- Issue
- 9
- Pages
- 1690-1701
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- OpenAlex
- W2150058269
- Cited by
- 80
- References
- 54
- Citations by year
- 2026: 4 · 2025: 3 · 2023: 3 · 2022: 1 · 2021: 5 · 2020: 5 · 2019: 6 · 2018: 5 · 2017: 4 · 2016: 8 · 2015: 5 · 2014: 11 · 2013: 6 · 2012: 7
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Molecular Genetics (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Keywords
- xeroderma pigmentosum variant, DNA polymerase eta, translesion synthesis, UV photoproducts, ATR-Chk1 pathway, replication fork stalling, S-phase checkpoint, S phase delay, UCN-01, UV-C irradiation, single-stranded DNA, DNA combing
- MeSH terms
- Checkpoint Kinase 1, Y-Family DNA Polymerases, Cell Line, DNA, DNA Damage, DNA-Directed DNA Polymerase, DNA Replication, Flow Cytometry, Humans, Protein Kinases, Transfection, Ultraviolet Rays, Xeroderma Pigmentosum, Blotting, Western, Signal Transduction, Protein Serine-Threonine Kinases, Cell Cycle Proteins, RNA, Small Interfering, Ataxia Telangiectasia Mutated Proteins
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