Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint
Open accessAbstract
The ATR-dependent DNA damage response pathway can respond to a diverse group of lesions as well as inhibitors of DNA replication. Using the Xenopus egg extract system, we show that lesions induced by UV irradiation and cis-platinum cause the functional uncoupling of MCM helicase and DNA polymerase activities, an event previously shown for aphidicolin. Inhibition of uncoupling during elongation with inhibitors of MCM7 or Cdc45, a putative helicase cofactor, results in abrogation of Chk1 phosphorylation, indicating that uncoupling is necessary for activation of the checkpoint. However, uncoupling is not sufficient for checkpoint activation, and DNA synthesis by Polα is also required. Finally, using plasmids of varying size, we demonstrate that all of the unwound DNA generated at a stalled replication fork can contribute to the level of Chk1 phosphorylation, suggesting that uncoupling amplifies checkpoint signaling at each individual replication fork. Taken together, these observations indicate that functional uncoupling of MCM helicase and DNA polymerase activities occurs in response to multiple forms of DNA damage and that there is a general mechanism for generation of the checkpoint-activating signal following DNA damage.
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Long single-stranded DNA can be generated by uncoupling MCM helicase and DNA polymerase during replication stress, by CtIP-mediated double-strand break end resection, by Exo1-mediated processing of nucleotide excision repair intermediates after UV, and by APE2-mediated single-strand break end resection in oxidative stress.
“A long stretch of ssDNA can be generated through the functional uncoupling of minichromosome maintenance (MCM) helicase and DNA polymerase in DNA replication stress, the DSB end resection by DNA exonuclease such as CtIP in DSB response, the Exo1-mediated processing of NER intermediates after UV radiation, and the SSB end resection by AP endonuclease 2 (APE2) in oxidative stress [86, 97–99]”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [97]
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Cites
The DNA damage response: putting checkpoints in perspective
Zhou, B.-B. S., & Elledge, S. J. (2000) · Nature · doi:10.1038/35044005 · Cited by 3,213 · 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
Liu, Q., Guntuku, S., Cui, X.-S., Matsuoka, S., Cortez, D., Tamai, K., Luo, G., Carattini-Rivera, S., DeMayo, F., Bradley, A., et al. (2000) · Genes & Development · doi:10.1101/gad.14.12.1448 · Cited by 1,625 · see citing works
ATR-Mediated Checkpoint Pathways Regulate Phosphorylation and Activation of Human Chk1
Zhao, H., & Piwnica-Worms, H. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.13.4129-4139.2001 · Cited by 1,091 · see citing works
Principles of Tumor Suppression
Sherr, C. J. (2004) · Cell · doi:10.1016/s0092-8674(03)01075-4 · Cited by 1,028 · see citing works
Geminin, an inhibitor of DNA replication, is degraded during mitosis.
Mcgarry, T., & Kirschner, M. (1998) · Cell · doi:10.1016/s0092-8674(00)81209-x · Cited by 988 · see citing works
ATR and ATRIP: Partners in Checkpoint Signaling
Cortez, D., Guntuku, S., Qin, J., & Elledge, S. J. (2001) · Science · doi:10.1126/science.1065521 · Cited by 985 · see citing works
Fork Reversal and ssDNA Accumulation at Stalled Replication Forks Owing to Checkpoint Defects
Sogo, J. M., Lopes, M., & Foiani, M. (2002) · Science · doi:10.1126/science.1074023 · Cited by 824 · see citing works
S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex
Katou, Y., Kanoh, Y., Bando, M., Noguchi, H., Tanaka, H., Ashikari, T., Sugimoto, K., & Shirahige, K. (2003) · Nature · doi:10.1038/nature01900 · Cited by 649 · see citing works
Cliby, W. A., Roberts, C. J., Cimprich, K. A., Stringer, C. M., Lamb, J. R., Schreiber, S. L., & Friend, S. H. (1998) · The EMBO Journal · doi:10.1093/emboj/17.1.159 · Cited by 534 · see citing works
Self-citationRegulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatinPreprint
Zou, L., Cortez, D., & Elledge, S. J. (2002) · Genes & Development · doi:10.1101/gad.950302 · Cited by 498 · see citing works
Walter, J. C., & Newport, J. (2000) · Molecules and Cells · doi:10.1016/s1097-2765(00)80241-5 · Cited by 472 · see citing works
Self-citationA unified view of the DNA-damage checkpoint
Melo, J. A., & Toczyski, D. P. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00312-5 · Cited by 457 · see citing works
Replication protein A-mediated recruitment and activation of Rad17 complexes
Zou, L., Liu, D., & Elledge, S. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2336100100 · Cited by 431 · see citing works
Kumagai, A., & Dunphy, W. G. (2000) · Molecular Cell · doi:10.1016/s1097-2765(05)00092-4 · Cited by 430 · see citing works
Guo, Z., Kumagai, A., Wang, S. X., & Dunphy, W. G. (2000) · Genes & Development · doi:10.1101/gad.842500 · Cited by 417 · see citing works
A Central Role for DNA Replication Forks in Checkpoint Activation and Response
Tercero, J. A., Longhese, M. P., & Diffley, J. F. X. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00169-2 · Cited by 394 · see citing works
Two checkpoint complexes are independently recruited to sites of DNA damage in vivo
Melo, J. A., Cohen, J., & Toczyski, D. P. (2001) · Genes & Development · doi:10.1101/gad.903501 · Cited by 384 · see citing works
ATR and ATM regulate the timing of DNA replication origin firing
Shechter, D., Costanzo, V., & Gautier, J. (2004) · Nature Cell Biology · doi:10.1038/ncb1145 · Cited by 383 · see citing works
Pellicioli, A., Lucca, C., Liberi, G., Marini, F., Lopes, M., Plevani, P., Romano, A., Fiore, P. P. D., & Foiani, M. (1999) · The EMBO Journal · doi:10.1093/emboj/18.22.6561 · Cited by 369 · see citing works
Ellison, V., & Stillman, B. (2003) · PLoS Biology · doi:10.1371/journal.pbio.0000033 · Cited by 363 · see citing works
An ATR- and Cdc7-Dependent DNA Damage Checkpoint that Inhibits Initiation of DNA Replication
Costanzo, V., Shechter, D., Lupardus, P. J., Cimprich, K. A., Gottesman, M. E., & Gautier, J. (2003) · Molecular Cell · doi:10.1016/s1097-2765(02)00799-2 · Cited by 355 · see citing works
Self-citationRecognition of cisplatin adducts by cellular proteins
Kartalou, M., & Essigmann, J. M. (2001) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(01)00142-7 · Cited by 350 · see citing works
Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases
Cortez, D., Glick, G. G., & Elledge, S. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403410101 · Cited by 324 · see citing works
Regulated chromosomal DNA replication in the absence of a nucleus.
Walter, J. C., Sun, L., & Newport, J. (1998) · Molecules and Cells · doi:10.1016/s1097-2765(00)80052-0 · Cited by 300 · see citing works
Self-citationEdwards, M. C., Tutter, A. V., Cvetic, C., Gilbert, C. H., Prokhorova, T. A., & Walter, J. C. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204438200 · Cited by 269 · see citing works
Self-citationRecruitment of Mec1 and Ddc1 Checkpoint Proteins to Double-Strand Breaks Through Distinct Mechanisms
Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K., & Sugimoto, K. (2001) · Science · doi:10.1126/science.1063827 · Cited by 258 · see citing works
Tanaka, S., Hu, S., Wang, T. S., et al. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)34343-6 · Cited by 257 · see citing works
A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication
Pacek, M., & Walter, J. C. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600369 · Cited by 254 · see citing works
Self-citationORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phasePreprint
Shimada, K., Pasero, P., & Gasser, S. M. (2002) · Genes & Development · doi:10.1101/gad.239802 · Cited by 207 · see citing works
Activation of the DNA Replication Checkpoint Through RNA Synthesis by Primase
Michael, W. M., Ott, R., Fanning, E., & Newport, J. W. (2000) · Science · doi:10.1126/science.289.5487.2133 · Cited by 206 · see citing works
Ward, I. M., Minn, K. T., & Chen, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.c300554200 · Cited by 205 · see citing works
Lee, J., Kumagai, A., & Dunphy, W. G. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00045-5 · Cited by 199 · see citing works
Arias, E. E., & Walter, J. C. (2004) · Genes & Development · doi:10.1101/gad.1255805 · Cited by 196 · see citing works
Self-citationHekmat-Nejad, M., You, Z., Yee, M., Newport, J. W., & Cimprich, K. A. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00855-1 · Cited by 193 · see citing works
Self-citationSterner, J. M., Dew-Knight, S., Musahl, C., Kornbluth, S. A., & Horowitz, J. M. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.5.2748 · Cited by 188 · see citing works
Moore, P. D., Bose, K., Rabkin, S. D., & Strauss, B. S. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.1.110 · Cited by 170 · see citing works
A requirement for replication in activation of the ATR-dependent DNA damage checkpointPreprint
Lupardus, P. J., Byun, T. S., Yee, M., Hekmat-Nejad, M., & Cimprich, K. A. (2002) · Genes & Development · doi:10.1101/gad.1013502 · Cited by 163 · see citing works
Self-citationIs the MCM2–7 complex the eukaryotic DNA replication fork helicase?
Labib, K. P. M., & Diffley, J. F. X. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00158-1 · 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
Walter, J. C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m008107200 · Cited by 151 · see citing works
Self-citationMimura, S., Masuda, T., Matsui, T., et al. (2000) · Genes to Cells · doi:10.1046/j.1365-2443.2000.00340.x · Cited by 137 · see citing works
Hexameric ring structure of the full‐length archaeal MCM protein complex
Pape, T., Meka, H., Chen, S., et al. (2003) · EMBO Reports · doi:10.1038/sj.embor.7400010 · Cited by 122 · see citing works
You, Z., Kong, L., & Newport, J. W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204120200 · Cited by 114 · see citing works
Mechanism of DNA polymerase .alpha. inhibition by aphidicolin
Sheaff, R. J., Ilsley, D. D., & Kuchta, R. D. (1991) · Biochemistry · doi:10.1021/bi00099a014 · Cited by 103 · see citing works
Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling
Tsao, C., Geisen, C., & Abraham, R. T. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600463 · Cited by 101 · see citing works
Lucas, I., Chevrier-Miller, M., Sogo, J. M., et al. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3500 · Cited by 98 · see citing works
Longhese, M. P. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.18.3533 · Cited by 96 · see citing works
DNA replication is required for the checkpoint response to damaged DNA in Xenopus egg extracts
Stokes, M. P., Hatten, R. A. V., Lindsay, H. D., & Michael, W. M. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200204127 · Cited by 82 · see citing works
Scudiero, D. A., & Strauss, B. S. (1974) · Journal of Molecular Biology · doi:10.1016/0022-2836(74)90421-5 · Cited by 81 · see citing works
Masuda, T., Mimura, S., & Takisawa, H. (2003) · Genes to Cells · doi:10.1046/j.1365-2443.2003.00621.x · Cited by 78 · see citing works
Mutational Effect of Fission Yeast Polα on Cell Cycle Events
Bhaumik, D., & Wang, T. S. ‐. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.8.2107 · Cited by 49 · see citing works
DNA Unwinding Is an MCM Complex-dependent and ATP Hydrolysis-dependent Process
Shechter, D., Ying, C. Y., & Gautier, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407772200 · Cited by 48 · see citing works
Fragile Sites: Breaking up over a Slowdown
Cimprich, K. A. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00158-1 · Cited by 45 · see citing works
Self-citationHexameric ring structure of the full-length archaeal MCM protein complex
Pape, T., Meka, H., Chen, S., et al. (2003) · EMBO Reports · doi:10.1038/sj.embor.embor7400010 · Cited by 42 · see citing works
Tight association of DNA primase with a subspecies of mouse DNA polymerase alpha.
Yagura, T., Tanaka, S., Kozu, T., et al. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)32272-5 · Cited by 37 · see citing works
DNA replication of mitotic chromatin in Xenopus egg extracts
Prokhorova, T. A., Mowrer, K., Gilbert, C. H., & Walter, J. (2003) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2336104100 · Cited by 35 · see citing works
Self-citationVeaute, X., Giglia‐Mari, G., Lawrence, C. W., et al. (2000) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(99)00052-x · Cited by 20 · see citing works
Extensive regions of single-stranded DNA in aphidicolin-treated melanoma cells
Loenn, U., & Loenn, S. (1988) · Biochemistry · doi:10.1021/bi00402a010 · Cited by 18 · see citing works
Stewart, B. W., & Hristoforidis, C. (1987) · Cancer Letters · doi:10.1016/0304-3835(87)90128-5 · Cited by 5 · see citing works
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Ciccia, A., & Elledge, S. J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.019 · Cited by 4,368 · see citing works
Causes and consequences of replication stress
Zeman, M. K., & Cimprich, K. A. (2014) · Nature Cell Biology · doi:10.1038/ncb2897 · Cited by 2,079 · see citing works
Self-citationATR: 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
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Harper, J. W., & Elledge, S. J. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.11.015 · Cited by 1,705 · see citing works
DNA Damage Sensing by the ATM and ATR Kinases
Marechal, A., & Zou, L. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012716 · Cited by 1,514 · see citing works
DNA damage-induced cell death: From specific DNA lesions to the DNA damage response and apoptosis
Roos, W. P., & Kaina, B. (2013) · Cancer Letters · doi:10.1016/j.canlet.2012.01.007 · Cited by 879 · 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
ATR signalling: more than meeting at the fork
Nam, E. A., & Cortez, D. (2011) · Biochemical Journal · doi:10.1042/bj20102162 · Cited by 316 · see citing works
Translesion DNA Synthesis and Mutagenesis in Eukaryotes
Sale, J. E. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012708 · Cited by 282 · 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
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Liu, S., Shiotani, B., Lahiri, M., Maréchal, A., Tse, A., Leung, C. C. Y., Glover, J. N. M., Yang, X. H., & Zou, L. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.019 · Cited by 281 · see citing works
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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
Self-citationYan, S., Sorrell, M., & Berman, Z. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1666-4 · Cited by 247 · 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
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Mechanisms of replication fork protection: a safeguard for genome stability
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Roles of UVA radiation and DNA damage responses in melanoma pathogenesis
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Quivy, J.-P., Gérard, A., Cook, A. J. L., Roche, D., & Almouzni, G. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1470 · Cited by 148 · see citing works
ATR and H2AX cooperate in maintaining genome stability under replication stress
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DNA replication as a target of the DNA damage checkpoint
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Yajima, H., Lee, K.-J., Zhang, S., Kobayashi, J., & Chen, B. P. C. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.11.036 · Cited by 124 · see citing works
TopBP1 and DNA polymerase-α directly recruit the 9-1-1 complex to stalled DNA replication forks
Yan, S., & Michael, W. M. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200810185 · Cited by 107 · see citing works
APE2 is required for ATR-Chk1 checkpoint activation in response to oxidative stress
Willis, J., Patel, Y., Lentz, B. L., & Yan, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301445110 · Cited by 100 · see citing works
Chang, D. J., Lupardus, P. J., & Cimprich, K. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606799200 · Cited by 101 · see citing works
Self-citationErrico, A., Costanzo, V., & Hunt, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706347104 · Cited by 92 · see citing works
Navadgi-Patil, V. M., & Burgers, P. M. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.03.011 · Cited by 93 · 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
Self-citationSchoonen, P. M., Kok, Y. P., Wierenga, E., Bakker, B., Foijer, F., Spierings, D. C. J., & van Vugt, M. A. T. M. (2019) · Molecular Oncology · doi:10.1002/1878-0261.12573 · Cited by 81 · see citing works
Unwind and slow down: checkpoint activation by helicase and polymerase uncoupling: Figure 1.
Cortez, D. (2005) · Genes & Development · doi:10.1101/gad.1316905 · Cited by 84 · see citing works
Despras, E., Daboussi, F., Hyrien, O., Marheineke, K., & Kannouche, P. L. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq046 · Cited by 80 · see citing works
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Bélanger, F., Fortier, E., Dubé, M., Lemay, J.-F., Buisson, R., Masson, J.-Y., Elsherbiny, A., Costantino, S., Carmona, E., Mes-Masson, A.-M., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0618 · Cited by 58 · see citing works
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Hilton, B. A., Liu, J., Cartwright, B. M., Liu, Y., Breitman, M., Wang, Y., Jones, R., Tang, H., Rusinol, A., Musich, P. R., et al. (2017) · The FASEB Journal · doi:10.1096/fj.201700014r · Cited by 52 · see citing works
Parisotto, M., Grelet, E., El Bizri, R., Dai, Y., Terzic, J., Eckert, D., Gargowitsch, L., Bornert, J.-M., & Metzger, D. (2018) · Journal of Experimental Medicine · doi:10.1084/jem.20171207 · Cited by 43 · see citing works
Majera, D., Skrott, Z., Chroma, K., Merchut-Maya, J. M., Mistrik, M., & Bartek, J. (2020) · Cells · doi:10.3390/cells9020469 · Cited by 43 · see citing works
Cell cycle stage-specific roles of Rad18 in tolerance and repair of oxidative DNA damage
Yang, Y., Durando, M., Smith-Roe, S. L., Sproul, C., Greenwalt, A. M., Kaufmann, W., Oh, S., Hendrickson, E. A., & Vaziri, C. (2013) · Nucleic Acids Research · doi:10.1093/nar/gks1325 · Cited by 33 · see citing works
Removing all obstacles: A critical role for p53 in promoting tissue renewal
Schoppy, D. W., Ruzankina, Y., & Brown, E. J. (2010) · Cell Cycle · doi:10.4161/cc.9.7.11194 · Cited by 32 · see citing works
Importin β-dependent nuclear import of TopBP1 in ATR–Chk1 checkpoint in Xenopus egg extracts
Bai, L., Michael, W. M., & Yan, S. (2014) · Cellular Signalling · doi:10.1016/j.cellsig.2014.01.006 · Cited by 19 · see citing works
- Authors
- Byun, T. S., Pacek, M., Yee, M.-C., Walter, J. C., & Cimprich, K. A.
- Affiliations
- Stanford University (US)
- Harvard University (US)
- Corresponding author
- Cimprich, Karlene A.
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2005-04-15
- Volume
- 19
- Issue
- 9
- Pages
- 1040-1052
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC1091739
- OpenAlex
- W2029369774
- Cited by
- 767
- References
- 60
- Citations by year
- 2026: 21 · 2025: 25 · 2024: 25 · 2023: 30 · 2022: 21 · 2021: 48 · 2020: 35 · 2019: 35 · 2018: 38 · 2017: 51 · 2016: 41 · 2015: 41 · 2014: 35 · 2013: 57 · 2012: 34
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (GM062193, R01GM062267, GM-62267, R01GM062193)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (2T32 HD 07249, T32HD007249)
- 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 › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- MCM helicase, DNA polymerase, DNA replication checkpoint, Chk1 phosphorylation, MCM7, Cdc45, replication fork stalling, UV-induced DNA damage, cisplatin, Xenopus egg extracts
- MeSH terms
- Checkpoint Kinase 1, Animals, Cell-Free System, Chromatin, DNA Damage, DNA-Directed DNA Polymerase, DNA Replication, DNA Helicases, DNA, Single-Stranded, Phosphorylation, Plasmids, Protein Kinases, Xenopus, Aphidicolin, Protein Serine-Threonine Kinases, DNA Primers, Cell Cycle Proteins, Xenopus Proteins, Adaptor Proteins, Signal Transducing, Ataxia Telangiectasia Mutated Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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