Biochemical Characterization of DNA Damage Checkpoint Complexes: Clamp Loader and Clamp Complexes with Specificity for 5′ Recessed DNA
Open accessAbstract
The cellular pathways involved in maintaining genome stability halt cell cycle progression in the presence of DNA damage or incomplete replication. Proteins required for this pathway include Rad17, Rad9, Hus1, Rad1, and Rfc-2, Rfc-3, Rfc-4, and Rfc-5. The heteropentamer replication factor C (RFC) loads during DNA replication the homotrimer proliferating cell nuclear antigen (PCNA) polymerase clamp onto DNA. Sequence similarities suggest the biochemical functions of an RSR (Rad17-Rfc2-Rfc3-Rfc4-Rfc5) complex and an RHR heterotrimer (Rad1-Hus1-Rad9) may be similar to that of RFC and PCNA, respectively. RSR purified from human cells loads RHR onto DNA in an ATP-, replication protein A-, and DNA structure-dependent manner. Interestingly, RSR and RFC differed in their ATPase activities and displayed distinct DNA substrate specificities. RSR preferred DNA substrates possessing 5' recessed ends whereas RFC preferred 3' recessed end DNA substrates. Characterization of the biochemical loading reaction executed by the checkpoint clamp loader RSR suggests new insights into the mechanisms underlying recognition of damage-induced DNA structures and signaling to cell cycle controls. The observation that RSR loads its clamp onto a 5' recessed end supports a potential role for RHR and RSR in diverse DNA metabolism, such as stalled DNA replication forks, recombination-linked DNA repair, and telomere maintenance, among other processes.
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The PCNA-like 9-1-1 complex (Rad9-Rad1-Hus1) is recruited preferentially to the 5'-primed single-stranded/double-stranded DNA junction by RPA and the Rad17-RFC clamp loader.
“The PCNA-like clamp 9-1-1 complex (Rad9-Rad1-Hus1) is recruited preferentially to the 5′-primed ssDNA/dsDNA junction by RPA and the clamp loader Rad17-RFC complex [102–105].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [102]
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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
Hartwell, L. H., & Kastan, M. B. (1994) · Science · doi:10.1126/science.7997877 · Cited by 2,523 · see citing works
Cell cycle checkpoint signaling through the ATM and ATR kinases
Abraham, R. T. (2001) · Genes & Development · doi:10.1101/gad.914401 · Cited by 1,966 · see citing works
Wold, M. S. (1997) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.66.1.61 · Cited by 1,445 · see citing works
Using Antibodies: A Laboratory Manual
Harlow, E., & Lane, D. A. (1998) · Cited by 996 · 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
Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA
Krishna, T. S. R., Kong, X., Gary, S. L., Burgers, P., & Kuriyan, J. (1994) · Cell · doi:10.1016/0092-8674(94)90014-0 · Cited by 902 · 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
THE DNA REPLICATION FORK IN EUKARYOTIC CELLS
Waga, S., & Stillman, B. (1998) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.67.1.721 · Cited by 814 · see citing works
Self-citationThe many substrates and functions of ATM.
Kastan, M. B., & Lim, D.-S. (2000) · Nature Reviews Molecular Cell Biology · doi:10.1038/35043058 · Cited by 779 · 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
Garvik, B. M., Carson, M., & Hartwell, L. H. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.11.6128 · Cited by 629 · see citing works
Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro
Waga, S., & Stillman, B. (1994) · Nature · doi:10.1038/369207a0 · Cited by 557 · 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
ATR Homolog Mec1 Promotes Fork Progression, Thus Averting Breaks in Replication Slow Zones
Rita, S., & Kleckner, N. E. (2002) · Science · doi:10.1126/science.1071398 · Cited by 429 · see citing works
Yeast Checkpoint Genes in DNA Damage Processing: Implications for Repair and Arrest
Lydall, D. A., & Weinert, T. A. (1995) · Science · doi:10.1126/science.270.5241.1488 · Cited by 416 · 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
Tsurimoto, T., & Stillman, B. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)52385-1 · Cited by 381 · see citing works
Self-citationBermudez, 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
Crystal Structure of the Processivity Clamp Loader Gamma (γ) Complex of E. coli DNA Polymerase III
Jeruzalmi, D., O’Donnell, M. E., & Kuriyan, J. (2001) · Cell · doi:10.1016/s0092-8674(01)00463-9 · Cited by 322 · see citing works
Identification of RFC(Ctf18p, Ctf8p, Dcc1p)
Mayer, M. L., Gygi, S. P., Aebersold, R. H., & Hieter, P. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00254-4 · Cited by 319 · see citing works
PCNA connects DNA replication to epigenetic inheritance in yeast
Zhang, Z., Shibahara, K., & Stillman, B. (2000) · Nature · doi:10.1038/35041601 · Cited by 318 · see citing works
Self-citationVenclovas, Č., & Thelen, M. P. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.13.2481 · Cited by 268 · see citing works
Tsurimoto, T., & Stillman, B. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.3.1023 · Cited by 260 · see citing works
Self-citationJeruzalmi, D., Yurieva, O., Zhao, Y., Young, M. A., Stewart, J., Hingorani, M., O’Donnell, M. E., & Kuriyan, J. (2001) · Cell · doi:10.1016/s0092-8674(01)00462-7 · Cited by 260 · see citing works
Recruitment 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
Sliding Clamps of DNA Polymerases
Kuriyan, J., & O’Donnell, M. E. (1993) · Journal of Molecular Biology · doi:10.1006/jmbi.1993.1644 · Cited by 258 · 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
DNA Damage and Checkpoint Pathways
Weinert, T. A. (1998) · Cell · doi:10.1016/s0092-8674(00)81597-4 · Cited by 253 · see citing works
Characterization of the Five Replication Factor C Genes of Saccharomyces cerevisiae
Cullmann, G., Fien, K., Kobayashi, R., & Stillman, B. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.9.4661 · Cited by 245 · see citing works
Self-citationCaspari, T., Dahlén, M., Kanter-Smoler, G., Lindsay, H. D., Hofmann, K., Papadimitriou, K., Sunnerhagen, P., & Carr, A. M. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.4.1254-1262.2000 · Cited by 231 · see citing works
The internal workings of a DNA polymerase clamp‐loading machine
Turner, J., Hingorani, M., Kelman, Z., & O’Donnell, M. E. (1999) · The EMBO Journal · doi:10.1093/emboj/18.3.771 · Cited by 215 · see citing works
Multiple competition reactions for RPA order the assembly of the DNA polymerase δ holoenzyme
Yuzhakov, A., Kelman, Z., Hurwitz, J., & O’Donnell, M. E. (1999) · The EMBO Journal · doi:10.1093/emboj/18.21.6189 · Cited by 212 · see citing works
Tsurimoto, T., & Stillman, B. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.2.609 · Cited by 210 · see citing works
Self-citationA novel Rad24 checkpoint protein complex closely related to replication factor C
Green, C., Erdjument‐Bromage, H., Tempst, P., & Lowndes, N. F. (2000) · Current Biology · doi:10.1016/s0960-9822(99)00263-8 · Cited by 208 · 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
Lee, J., Kumagai, A., & Dunphy, W. G. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00045-5 · Cited by 199 · see citing works
Volkmer, E., & Karnitz, L. M. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.2.567 · Cited by 198 · see citing works
Purification and characterization of human DNA damage checkpoint Rad complexes
Lindsey‐Boltz, L. A., Bermudez, V. P., Hurwitz, J., & Sancar, A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.201373498 · Cited by 198 · see citing works
Kelman, Z., Yuzhakov, A., Andjelkovic, J., & O’Donnell, M. E. (1998) · The EMBO Journal · doi:10.1093/emboj/17.8.2436 · Cited by 188 · see citing works
Lcd1p Recruits Mec1p to DNA Lesions In Vitro and In Vivo
Rouse, J. W., & Jackson, S. P. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00507-5 · Cited by 179 · see citing works
Glover, B. P., & McHenry, C. S. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.36.23476 · Cited by 167 · see citing works
Clamping down on clamps and clamp loaders
Mossi, R., & Hübscher, U. (1998) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1998.254209.x · Cited by 164 · see citing works
Elg1 forms an alternative RFC complex important for DNA replication and genome integrity
Bellaoui, M., Chang, M., Ou, J., Xu, H., Boone, C., & Brown, G. W. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg406 · Cited by 157 · 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
Longhese, M. P., Paciotti, V., Fraschini, R., Zaccarini, R., Plevani, P., & Lucchini, G. (1997) · The EMBO Journal · doi:10.1093/emboj/16.17.5216 · Cited by 149 · see citing works
Burtelow, M. A., Roos‐Mattjus, P., Rauen, M. P., Babendure, J. R., & Karnitz, L. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102946200 · Cited by 142 · see citing works
St.Onge, R. P., Udell, C. M., Casselman, R., & Davey, S. K. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.6.1985 · Cited by 141 · see citing works
Hingorani, M., & O’Donnell, M. E. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.38.24550 · Cited by 141 · see citing works
Paciotti, V., Lucchini, G., Plevani, P., & Longhese, M. P. (1998) · The EMBO Journal · doi:10.1093/emboj/17.14.4199 · Cited by 132 · see citing works
Role of a Complex Containing Rad17, Mec3, and Ddc1 in the Yeast DNA Damage Checkpoint Pathway
Kondo, T., Matsumoto, K., & Sugimoto, K. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.2.1136 · Cited by 126 · see citing works
Replication factor A is required in vivo for DNA replication, repair, and recombination.
Longhese, M. P., Plevani, P., & Lucchini, G. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.7884 · Cited by 125 · see citing works
Kim, H., & Brill, S. J. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.11.3725-3737.2001 · Cited by 121 · see citing works
ELG1 , a yeast gene required for genome stability, forms a complex related to replication factor C
Ben‐Aroya, S., Koren, A., Liefshitz, B., Steinlauf, R., & Kupiec, M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1633757100 · Cited by 118 · see citing works
ATP Utilization by Yeast Replication Factor C
Gomes, X. V., Schmidt, S. L. G., & Burgers, P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011743200 · Cited by 117 · 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
Kostrub, C. F., Knudsen, K. E., Subramani, S. E., & Enoch, T. (1998) · The EMBO Journal · doi:10.1093/emboj/17.7.2055 · Cited by 114 · see citing works
Podust, L. M., Podust, V. N., Sogo, J. M., et al. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.6.3072 · Cited by 100 · see citing works
Brush, G. S. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.19.3725 · Cited by 98 · see citing works
Sugimoto, K., Ando, S., Shimomura, T., & Matsumoto, K. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.10.5905 · Cited by 92 · see citing works
Oakley, G. G., Loberg, L. I., Yao, J., Risinger, M. A., Yunker, R. L., Zernik-Kobak, M., Khanna, K. K., Lavin, M. F., Carty, M. P., & Dixon, K. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.5.1199 · Cited by 91 · see citing works
Functional and Physical Interaction between Rad24 and Rfc5 in the Yeast Checkpoint Pathways
Shimomura, T., Ando, S., Matsumoto, K., & Sugimoto, K. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.9.5485 · Cited by 82 · see citing works
Tsurimoto, T., & Stillman, B. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.2.609-619.1989 · Cited by 82 · see citing works
Self-citationCyclin-Dependent Kinase Inhibitor p21 Modulates the DNA Primer-Template Recognition Complex
Waga, S., & Stillman, B. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.7.4177 · Cited by 78 · see citing works
Self-citationCai, J., Gibbs, E., Uhlmann, F., Phillips, B., Yao, N. Y., O’Donnell, M. E., & Hurwitz, J. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.30.18974 · Cited by 71 · see citing works
Hingorani, M., Bloom, L. B., Goodman, M. F., & O’Donnell, M. E. (1999) · The EMBO Journal · doi:10.1093/emboj/18.18.5131 · Cited by 68 · see citing works
Checkpoint Proteins Influence Telomeric Silencing and Length Maintenance in Budding Yeast
Longhese, M. P., Paciotti, V., Neecke, H., & Lucchini, G. (2000) · Genetics · doi:10.1093/genetics/155.4.1577 · Cited by 68 · see citing works
Detecting the ability of viral, bacterial and eukaryotic replication proteins to track along DNA.
Tinker, R. L., Kassavetis, G. A., & Geiduschek, E. P. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06867.x · Cited by 67 · see citing works
Ellison, V., & Stillman, B. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.10.5979 · Cited by 59 · see citing works
Self-citationReplication Factor A Is Required In Vivo for DNA Replication, Repair, and Recombination
Longhese, M. P., Plevani, P., & Lucchini, G. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.7884-7890.1994 · Cited by 59 · see citing works
Podust, V. N., Tiwari, N., Ott, R., & Fanning, E. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.21.12935 · Cited by 47 · see citing works
Fission Yeast Rad17 Associates with Chromatin in Response to Aberrant Genomic Structures
Kai, M., Tanaka, H., & Wang, T. S. ‐. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.10.3289-3301.2001 · Cited by 46 · see citing works
Fission Yeast Rad26 Is a Regulatory Subunit of the Rad3 Checkpoint Kinase
Wolkow, T. D., & Enoch, T. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.01-03-0104 · Cited by 43 · see citing works
HRad17 Colocalizes with NHP2L1 in the Nucleolus and Redistributes after UV Irradiation
Chang, M.-S., Sasaki, H., Campbell, M. S., Kraeft, S., Sutherland, R., Yang, C., Liu, Y., Auclair, D., Hao, L., Sonoda, H., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.51.36544 · Cited by 39 · see citing works
Pietroni, P., Young, M. C., Latham, G. J., et al. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4687 · Cited by 39 · see citing works
Yao, N. Y., Hurwitz, J., & O’Donnell, M. E. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.2.1421 · Cited by 39 · see citing works
Yao, N. Y., Leu, F. P., Anjelkovic, J., Turner, J., & O’Donnell, M. E. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.15.11440 · Cited by 37 · see citing works
Reems, J. A., Wood, S., & McHenry, C. S. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.10.5606 · Cited by 36 · see citing works
Assembly of Functional Replication Factor C Expressed Using Recombinant Baculoviruses
Podust, V. N., & Fanning, E. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.10.6303 · Cited by 32 · see citing works
Mechanism of Bacteriophage T4 DNA Holoenzyme Assembly: The 44/62 Protein Acts as a Molecular Motor
Berdis, A. J., & Benkovic, S. J. (1997) · Biochemistry · doi:10.1021/bi962139l · Cited by 24 · see citing works
Flagged first, then by citations
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Sorted by citations
The DNA Damage Response: Making It Safe to Play with Knives
Ciccia, A., & Elledge, S. J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.019 · Cited by 4,368 · 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
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
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
Initiating Cellular Stress Responses
Bakkenist, C. J., & Kastan, M. B. (2004) · Cell · doi:10.1016/j.cell.2004.06.023 · Cited by 544 · see citing works
Maréchal, A., & Zou, L. (2015) · Cell Research · doi:10.1038/cr.2014.147 · Cited by 465 · see citing works
Dial 9–1–1 for DNA damage: the Rad9–Hus1–Rad1 (9–1–1) clamp complex
Parrilla-Castellar, E. R., Arlander, S. J. H., & Karnitz, L. (2004) · DNA Repair · doi:10.1016/j.dnarep.2004.03.032 · Cited by 342 · 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
Replication Protein A phosphorylation and the cellular response to DNA damage
Binz, S. K., Sheehan, A. M., & Wold, M. S. (2004) · DNA Repair · doi:10.1016/j.dnarep.2004.03.028 · Cited by 299 · 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
ATR autophosphorylation as a molecular switch for checkpoint activation
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
Common mechanisms of PIKK regulation
Lovejoy, C. A., & Cortez, D. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.04.006 · Cited by 277 · 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
Yan, S., Sorrell, M., & Berman, Z. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1666-4 · Cited by 247 · see citing works
Replication Protein A Directs Loading of the DNA Damage Checkpoint Clamp to 5′-DNA Junctions
Majka, J., Binz, S. K., Wold, M. S., & Burgers, P. M. J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605176200 · Cited by 205 · see citing works
The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint
Majka, J., Niedziela-Majka, A., & Burgers, P. M. J. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.11.027 · Cited by 186 · see citing works
Bonilla, C. Y., Melo, J. A., & Toczyski, D. P. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.03.023 · Cited by 161 · see citing works
Eukaryotic DNA damage checkpoint activation in response to double-strand breaks
Finn, K., Lowndes, N. F., & Grenon, M. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0875-3 · Cited by 127 · see citing works
Toueille, M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh652 · Cited by 122 · see citing works
Yeast DNA replication protein Dpb11 activates the Mec1/ATR checkpoint kinase
Navadgi-Patil, V. M., & Burgers, P. M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807435200 · Cited by 121 · see citing works
Wu, X., Shell, S. M., & Zou, Y. (2005) · Oncogene · doi:10.1038/sj.onc.1208674 · Cited by 113 · 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
Requirement of the Mre11 complex and exonuclease 1 for activation of the Mec1 signaling pathway
Nakada, D., Hirano, Y., & Sugimoto, K. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.22.10016-10025.2004 · Cited by 113 · see citing works
Vrouwe, M. G., Pines, A., Overmeer, R. M., Hanada, K., & Mullenders, L. H. F. (2011) · Journal of Cell Science · doi:10.1242/jcs.075325 · Cited by 100 · see citing works
The human Rad9–Rad1–Hus1 checkpoint complex stimulates flap endonuclease 1
Wang, W., Brandt, P., Rossi, M. L., Lindsey-Boltz, L., Podust, V., Fanning, E., Sancar, A., & Bambara, R. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407686101 · Cited by 98 · 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
The RFC Clamp Loader: Structure and Function
Yao, N. Y., & O’Donnell, M. (2012) · Subcellular Biochemistry · doi:10.1007/978-94-007-4572-8_14 · Cited by 90 · 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
Friedrich-Heineken, E., Toueille, M., Tännler, B., Bürki, C., Ferrari, E., Hottiger, M. O., & Hübscher, U. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.09.018 · Cited by 76 · see citing works
SMIRNOVA, E., TOUEILLE, M., MARKKANEN, E., & HÜBSCHER, U. (2005) · Biochemical Journal · doi:10.1042/bj20050211 · Cited by 74 · see citing works
The human checkpoint sensor Rad9–Rad1–Hus1 interacts with and stimulates NEIL1 glycosylase
Guan, X., Bai, H., Shi, G., Theriot, C. A., Hazra, T. K., Mitra, S., & Lu, A.-L. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm075 · Cited by 74 · see citing works
Gembka, A., Toueille, M., Smirnova, E., Poltz, R., Ferrari, E., Villani, G., & Hubscher, U. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkl1139 · Cited by 74 · see citing works
Recruitment of DNA damage checkpoint proteins to damage in transcribed and nontranscribed sequences
Jiang, G., & Sancar, A. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.1.39-49.2006 · Cited by 70 · see citing works
Guan, X., Madabushi, A., Chang, D.-Y., Fitzgerald, M. E., Shi, G., Drohat, A. C., & Lu, A.-L. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm678 · Cited by 65 · see citing works
Postreplication gaps at UV lesions are signals for checkpoint activation
Callegari, A. J., Clark, E., Pneuman, A., & Kelly, T. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003449107 · Cited by 54 · 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
Mechanism of Stimulation of Human DNA Ligase I by the Rad9-Rad1-Hus1 Checkpoint Complex
Wang, W., Lindsey-Boltz, L. A., Sancar, A., & Bambara, R. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602289200 · Cited by 49 · see citing works
DNA binding by the Rad9A subunit of the Rad9-Rad1-Hus1 complex
Hwang, B.-J., Gonzales, R., Corzine, S., Stenson, E., Pidugu, L., & Lu, A.-L. (2022) · PLOS ONE · doi:10.1371/journal.pone.0272645 · Cited by 9 · see citing works
- Authors
- Ellison, V., & Stillman, B.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Corresponding author
- Stillman, Bruce
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2003-11-17
- Volume
- 1
- Issue
- 2
- Pages
- e33
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC261875
- OpenAlex
- W2101942126
- Cited by
- 363
- References
- 80
- Citations by year
- 2026: 7 · 2025: 5 · 2024: 11 · 2023: 6 · 2022: 13 · 2021: 9 · 2020: 15 · 2019: 6 · 2018: 10 · 2017: 12 · 2016: 14 · 2015: 12 · 2014: 21 · 2013: 22 · 2012: 11
- FWCI
- 8.52
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, other-oa)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Cancer Institute (CA13106, P01CA013106)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Keywords
- DNA damage checkpoint, clamp loader, replication factor C, proliferating cell nuclear antigen, DNA loading, ATPase activity, genome stability, cell cycle arrest, DNA damage recognition, stalled replication forks, telomere maintenance
- MeSH terms
- Adenosine Triphosphate, DNA, DNA Damage, DNA Replication, Escherichia coli, Exonucleases, Humans, Models, Biological, Molecular Sequence Data, Protein Binding, Recombination, Genetic, Saccharomyces cerevisiae, Schizosaccharomyces, Substrate Specificity, Telomere, Protein Structure, Secondary, Cell Cycle Proteins, Proliferating Cell Nuclear Antigen, Dimerization, Schizosaccharomyces pombe Proteins, Cell Line, Tumor, Immunoprecipitation, Replication Protein C
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