Postreplication gaps at UV lesions are signals for checkpoint activation
Open accessAbstract
Exposure of eukaryotic cells to UV light induces a checkpoint response that delays cell-cycle progression after cells enter S phase. It has been hypothesized that this checkpoint response provides time for repair by signaling the presence of structures generated when the replication fork encounters UV-induced DNA damage. To gain insight into the nature of the signaling structures, we used time-lapse microscopy to determine the effects of deficiencies in translesion DNA polymerases on the checkpoint response of the fission yeast Schizosaccharomyces pombe . We found that disruption of the genes encoding translesion DNA polymerases Polκ and Polη significantly prolonged the checkpoint response, indicating that the substrates of these enzymes are signals for checkpoint activation. Surprisingly, we found no evidence that the translesion polymerases Rev1 and Polζ repair structures that are recognized by the checkpoint despite their role in maintaining viability after UV irradiation. Quantitative flow cytometry revealed that cells lacking translesion polymerases replicate UV-damaged DNA at the same rate at WT cells, indicating that the enhanced checkpoint response of cells lacking Polκ and Polη is not the result of stalled replication forks. These observations support a model in which postreplication DNA gaps with unrepaired UV lesions in the template strand act both as substrates for translesion polymerases and as signals for checkpoint activation.
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If ssDNA gaps are left unfilled, checkpoint signals are activated and lead to G2-phase cell cycle arrest.
“If the ssDNA gaps are left unfilled, checkpoint signals are activated leading to a G2-phase cell cycle arrest [17][18][19].”
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 [17]
Translesion DNA polymerase activities seem to counteract the generation of the UV-induced checkpoint signal.
“Interestingly, translesion DNA polymerase activities (TLS) seem to counteract the generation of the UV-induced checkpoint signal [61,69].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [69]
Cites
Genome maintenance mechanisms for preventing cancer
Hoeijmakers, J. H. J. (2001) · Nature · doi:10.1038/35077232 · Cited by 3,939 · see citing works
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
Ultraviolet radiation-mediated damage to cellular DNA
Cadet, J., Sage, E., & Douki, T. (2005) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/j.mrfmmm.2004.09.012 · Cited by 932 · see citing works
Efficient Bypass of a Thymine-Thymine Dimer by Yeast DNA Polymerase, Polη
Johnson, R. E., Prakash, S., & Prakash, L. (1999) · Science · doi:10.1126/science.283.5404.1001 · Cited by 736 · see citing works
Interfaces Between the Detection, Signaling, and Repair of DNA Damage
Rouse, J. W., & Jackson, S. P. (2002) · Science · doi:10.1126/science.1074740 · Cited by 688 · see citing works
Eukaryotic Translesion Polymerases and Their Roles and Regulation in DNA Damage Tolerance
Waters, L. S., Minesinger, B. K., Wiltrout, M. E., D'Souza, S., Woodruff, R. V., & Walker, G. C. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00034-08 · Cited by 591 · 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
Lindsay, H. D., Griffiths, D. J. F., Edwards, R. J., Christensen, P. U., Murray, J. M., Osman, F., Walworth, N. C., & Carr, A. M. (1998) · Genes & Development · doi:10.1101/gad.12.3.382 · Cited by 385 · see citing works
Ellison, V., & Stillman, B. (2003) · PLoS Biology · doi:10.1371/journal.pbio.0000033 · Cited by 363 · see citing works
Douki, T., & Cadet, J. (2001) · Biochemistry · doi:10.1021/bi0022543 · Cited by 337 · see citing works
Bermudez, V. P., Lindsey-Boltz, L. A., Cesare, A. J., Maniwa, Y., Griffith, J. D., Hurwitz, J., & Sancar, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437927100 · Cited by 324 · see citing works
Prakash, L. (1981) · Molecular and General Genetics MGG · doi:10.1007/bf00352525 · Cited by 291 · see citing works
Blastyák, A., Pintér, L., Unk, I., Prakash, L., Prakash, S., & Haracska, L. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.07.030 · Cited by 285 · see citing works
Suffering in silence: the tolerance of DNA damage
Friedberg, E. C. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1781 · Cited by 271 · see citing works
Polesky, A. H., Steitz, T. A., Grindley, N. D. F., & Joyce, C. M. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)77342-0 · Cited by 259 · see citing works
Yeast Rad17/Mec3/Ddc1: A sliding clamp for the DNA damage checkpoint
Majka, J., & Burgers, P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437148100 · Cited by 255 · 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
Griffiths, D. J. F., Barbet, N., McCready, S. J., Lehmann, A. R., & Carr, A. M. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00269.x · Cited by 204 · see citing works
Fission Yeast Eso1p Is Required for Establishing Sister Chromatid Cohesion during S Phase
Tanaka, K., Yonekawa, T., Kawasaki, Y., Kai, M., Furuya, K., Iwasaki, M., Murakami, H., Yanagida, M., & Okayama, H. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.10.3459-3469.2000 · Cited by 182 · see citing works
Gibbs, P., McDonald, J. P., Woodgate, R., & Lawrence, C. W. (2004) · Genetics · doi:10.1534/genetics.104.034611 · Cited by 180 · see citing works
Torres‐Ramos, C. A., Prakash, S., & Prakash, L. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.7.2419-2426.2002 · Cited by 170 · see citing works
A Sliding Clamp Model for the Rad1 Family of Cell Cycle Checkpoint Proteins
Thelen, M. P., Venclovas, Č., & Fidelis, K. A. (1999) · Cell · doi:10.1016/s0092-8674(00)80587-5 · Cited by 150 · see citing works
Regulation of replication timing in fission yeast
Kim, S.-M., & Huberman, J. A. (2001) · The EMBO Journal · doi:10.1093/emboj/20.21.6115 · Cited by 136 · see citing works
Requirement of DNA Polymerase η for Error-Free Bypass of UV-Induced CC and TC Photoproducts
Yu, S.-L., Johnson, R. E., Prakash, S., & Prakash, L. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.1.185-188.2001 · Cited by 133 · 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
NOBEL LECTURE: Yeast and Cancer
Hartwell, L. H. (2002) · Bioscience Reports · doi:10.1023/a:1020918107706 · Cited by 116 · see citing works
Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint
Giannattasio, M., Lazzaro, F., Longhese, M. P., Plevani, P., & Muzi‐Falconi, M. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600051 · Cited by 113 · see citing works
Neecke, H., Lucchini, G., & Pia Longhese, M. (1999) · The EMBO Journal · doi:10.1093/emboj/18.16.4485 · Cited by 94 · see citing works
Gangavarapu, V., Prakash, S., & Prakash, L. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01331-07 · Cited by 92 · 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
Rhind, N., & Russell, P. R. (1998) · Genetics · doi:10.1093/genetics/149.4.1729 · Cited by 67 · see citing works
Efficient labeling of fission yeast Schizosaccharomyces pombe with thymidine and BUdR
Hodson, J. A. (2003) · Nucleic Acids Research · doi:10.1093/nar/gng134 · Cited by 66 · see citing works
Shedding Light on the DNA Damage Checkpoint
Callegari, A. J., & Kelly, T. J. (2007) · Cell Cycle · doi:10.4161/cc.6.6.3984 · Cited by 60 · see citing works
Self-citationMcCready, S. J., Carr, A. M., & Lehmann, A. R. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb00959.x · Cited by 57 · see citing works
UV irradiation induces a postreplication DNA damage checkpoint
Callegari, A. J., & Kelly, T. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607343103 · Cited by 51 · see citing works
Self-citationAcidic Residues Critical for the Activity and Biological Function of Yeast DNA Polymerase η
Kondratick, C. M., Washington, M. T., Prakash, S., & Prakash, L. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.6.2018-2025.2001 · Cited by 46 · see citing works
Eukaryotic mutagenesis and translesion replication dependent on DNA polymerase ζ and Rev I protein
Lawrence, C. W., & Maher, V. M. (2001) · Biochemical Society Transactions · doi:10.1042/bst0290187 · Cited by 38 · see citing works
Sempowski, G. D., Rhein, M. E., Scearce, R. M., & Haynes, B. F. (2002) · European Journal of Immunology · doi:10.1002/1521-4141(200211)32:11 · Cited by 38 · see citing works
Insights into the cellular role of enigmatic DNA polymerase ι
Vidal, A. E., & Woodgate, R. (2009) · DNA repair · doi:10.1016/j.dnarep.2008.12.007 · Cited by 17 · see citing works
Bypass Replication in Vitro of UV-Induced Photoproducts Blocking Leading or Lagging Strand Synthesis
Nikolaishvili‐Feinberg, N., & Cordeiro‐Stone, M. (2001) · Biochemistry · doi:10.1021/bi011474t · Cited by 16 · see citing works
Lombaerts, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.14.2868 · Cited by 10 · see citing works
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Effect of Nanoparticles on the Cell Life Cycle
Mahmoudi, M., Azadmanesh, K., Shokrgozar, M. A., Journeay, W. S., & Laurent, S. (2011) · Chemical Reviews · doi:10.1021/cr1003166 · Cited by 352 · see citing works
Repriming of DNA synthesis at stalled replication forks by human PrimPol
Mouron, S. A., Rodríguez‐Acebes, S., Martínez-Jiménez, M. I., García-Gómez, S., Chocrón, S., Blanco, L., & Méndez, J. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2719 · Cited by 322 · see citing works
ATR: a master conductor of cellular responses to DNA replication stress
Flynn, R. L., & Zou, L. (2011) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.09.005 · Cited by 290 · see citing works
DNA Fiber Analysis: Mind the Gap!
Quinet, A., Carvajal-Maldonado, D., Lemacon, D. S., & Vindigni, A. (2017) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2017.03.019 · Cited by 240 · see citing works
Lesion Bypass and the Reactivation of Stalled Replication Forks
Marians, K. J. (2018) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-062917-011921 · Cited by 163 · see citing works
The Intra-S Checkpoint Responses to DNA Damage
Iyer, D., & Rhind, N. (2017) · Genes · doi:10.3390/genes8020074 · Cited by 113 · 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
Timing and spacing of ubiquitin‐dependent DNA damage bypass
Ulrich, H. D. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.028 · Cited by 73 · see citing works
Quinet, 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
Betous, R., Pillaire, M., Pierini, L., van der Laan, S., Recolin, B., Ohl-Séguy, E., Guo, C., Niimi, N., Grúz, P., Nohmi, T., et al. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.148 · Cited by 68 · see citing works
Boyer, A.-S., Grgurević, S., Cazaux, C., & Hoffmann, J. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.09.022 · Cited by 65 · see citing works
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Skoneczna, A., Kaniak, A., & Skoneczny, M. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv028 · Cited by 57 · see citing works
Rudd, S. G., Glover, L., Jóźwiakowski, S. K., Horn, D., & Doherty, A. J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.034 · Cited by 55 · see citing works
Hedglin, M., & Benkovic, S. J. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00046 · Cited by 50 · see citing works
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García‐Rodríguez, N., Morawska, M., Wong, R. P. C., Daigaku, Y., & Ulrich, H. D. (2018) · The EMBO Journal · doi:10.15252/embj.201798369 · Cited by 50 · see citing works
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Han, J., Liu, T., Huen, M. S. Y., Hu, L. T., Chen, Z., & Huang, J. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201311007 · Cited by 44 · see citing works
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Novarina, D., Amara, F., Lazzaro, F., Plevani, P., & Muzi-Falconi, M. (2011) · DNA Repair · doi:10.1016/j.dnarep.2011.04.030 · Cited by 43 · see citing works
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Kahli, M., Osmundson, J., Yeung, R., & Smith, D. J. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1242 · Cited by 40 · see citing works
Mognato, M., Burdak‐Rothkamm, S., & Rothkamm, K. (2020) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2020.108346 · Cited by 40 · see citing works
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Inturi, S., Tewari‐Singh, N., Agarwal, C., White, C. W., & Agarwal, R. (2014) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2014.04.002 · Cited by 38 · see citing works
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Hedglin, M., & Benkovic, S. J. (2017) · Biochemistry · doi:10.1021/acs.biochem.6b01213 · Cited by 25 · see citing works
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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
Romero, Z. J., Armstrong, T. J., Henrikus, S. S., Chen, S. H., Glass, D. J., Ferrazzoli, A. E., Wood, E. A., Chitteni‐Pattu, S., van Oijen, A. M., Lovett, S. T., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz960 · Cited by 19 · see citing works
Tapia-Alveal, C., & O’Connell, M. J. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-03-0272 · Cited by 19 · see citing works
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Wigan, M., Pinder, A., Giles, N., Pavey, S., Burgess, A., Wong, S., Sturm, R. A., & Gabrielli, B. (2012) · Journal of Investigative Dermatology · doi:10.1038/jid.2012.41 · Cited by 17 · see citing works
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Warmerdam, D. O., Brinkman, E. K., Marteijn, J. A. F., Medema, R. H., Kanaar, R., & Smits, V. A. J. (2013) · Journal of Cell Science · doi:10.1242/jcs.118265 · Cited by 11 · see citing works
Uchiyama, M., Terunuma, J., & Hanaoka, F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0130000 · Cited by 11 · see citing works
Coordination of DNA damage tolerance mechanisms with cell cycle progression in fission yeast
Callegari, A. J., & Kelly, T. J. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1121353 · Cited by 7 · see citing works
Self-citationLimited Repair of Critical DNA Damage in Cells Exposed to Low Dose Radiation
Gaziev, A. I., & Shaikhaev, G. (2012) · InTech eBooks · doi:10.5772/33611 · Cited by 5 · see citing works
Roadworks of DNA Damage Bypass during and after Replication
Daigaku, Y. (2012) · Genes and Environment · doi:10.3123/jemsge.34.77 · Cited by 4 · see citing works
Cellular Responses to DNA Damage
Klapacz, J., & Gollapudi, B. B. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.95611-3 · Cited by 2 · see citing works
Mastro, T. L., Tripathi, V. P., & Forsburg, S. L. (2020) · Journal of Cell Science · doi:10.1242/jcs.238709 · 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
Kochenova, O. V. (2016) · DigitalCommons@UNMC
Gasser, S. M., & Shimada, K. (2018) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.732910825.793553438
Ripandelli, R. A. A., Wood, E. A., Robinson, A., van Oijen, A. M., & Cox, M. M. (2026) · PLoS Genetics · doi:10.1371/journal.pgen.1012110
- Authors
- Callegari, A. J., Clark, E., Pneuman, A., & Kelly, T. J.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-04-19
- Volume
- 107
- Issue
- 18
- Pages
- 8219-8224
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2889594
- OpenAlex
- W1996421216
- Cited by
- 54
- References
- 41
- Citations by year
- 2026: 1 · 2023: 2 · 2022: 1 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 5 · 2016: 2 · 2015: 5 · 2014: 6 · 2013: 9 · 2012: 5
- FWCI
- 2.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM050806)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- UV-induced DNA damage, DNA damage checkpoint, translesion DNA polymerases, Rev1, replication fork stalling, S-phase checkpoint, Schizosaccharomyces pombe, DNA repair, checkpoint signaling
- MeSH terms
- Y-Family DNA Polymerases, Cell Cycle, DNA Damage, DNA-Directed DNA Polymerase, DNA Replication, DNA, Fungal, Pyrimidines, Schizosaccharomyces, Ultraviolet Rays
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