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Replication Protein A Directs Loading of the DNA Damage Checkpoint Clamp to 5′-DNA Junctions
Open accessAbstract
The heterotrimeric checkpoint clamp comprises the Saccharomyces cerevisiae Rad17, Mec3, and Ddc1 subunits (Rad17/3/1, the 9-1-1 complex in humans). This DNA damage response factor is loaded onto DNA by the Rad24-RFC (replication factor C-like complex with Rad24) clamp loader and ATP. Although Rad24-RFC alone does not bind to naked partial double-stranded DNA, coating of the single strand with single-stranded DNA-binding protein RPA (replication protein A) causes binding of Rad24-RFC via interactions with RPA. However, RPA-mediated binding is abrogated when the DNA is coated with RPA containing a rpa1-K45E (rfa1-t11) mutation. These properties allowed us to determine the role of RPA in clamp-loading specificity. The Rad17/3/1 clamp is loaded with comparable efficiency onto naked primer/template DNA with either a 3'-junction or a 5'-junction. Remarkably, when the DNA was coated with RPA, loading of Rad17/3/1 at 3'-junctions was completely inhibited, thereby providing specificity to loading at 5'-junctions. However, Rad17/3/1 loaded at 5'-junctions can slide across double-stranded DNA to nearby 3'-junctions and thereby affect the activity of proteins that act at 3'-termini. These studies show a unique specificity of the checkpoint loader for 5'-junctions of RPA-coated DNA. The implications of this specificity for checkpoint function are discussed.
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“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 [105]
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The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint
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Self-citationReplication protein A: directing traffic at the intersection of replication and repair
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“This interaction is completely abolished with the mutant rfa-t11 protein indicating that RPA17 also binds to the N-terminus of RPA1 (98).”
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“Unlike the wild-type RPA, the rfa1-t11 mutant is unable to interact with Ddc2 (yeast homolog of human ATRIP), and fails to recruit Ddc2 and Ddc1 (yeast homolog of human Rad9) to sites of DNA damage (Zou and Elledge, 2003; Zou et al., 2003; Lucca et al., 2004; Majka et al., 2006).”
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“The presence of RPA is critical for this reaction and imparts specificity in loading, creating a preference for a 5 rather than a 3 primer end (18, 36).”
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Self-citationReconstitution of RPA-covered single-stranded DNA-activated ATR-Chk1 signaling
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“Based on the experience we have gained from establishing an RPA-ssDNA-dependent system, we expect it should be possible to develop an in vitro system dependent on the 9-1-1 complex as well by careful titration of the multiple components of the reaction (ATR-ATRIP, TopBP1, Rad17-RFC/9-1-1 complex, RPA, Chk1, and DNA) a…”
BackgroundInfluentialSelf-citationLangerak, P., & Russell, P. R. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0070 · Cited by 150
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“On the other hand, Rad24-RFC loads 9-1-1 specifically onto 50-primer/template junctions (Majka et al., 2006a).”
InfluentialSelf-citationSingle- and double-stranded DNA: building a trigger of ATR-mediated DNA damage response: Figure 1.Preprint
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“Indeed, at HO-induced DSBs in yeast, the formation of long stretches of ssDNA is needed for robust phosphorylation of Rad53, an effector kinase of Mec1 (Vaze et al. 2002).”
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“It is proposed that the 9-1-1 complex, which loads specifically onto 50 junctions [174, 175], signals replication stress on the lagging strand, while pol e and the leading strand factors Dpb11 and Sld2 detect replication perturbations on the leading strand, with both pathways independently leading to Mec1 activation […”
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“Loaded 9-1-1 interacts with the BRCT domain protein TopBP1, which binds the phosphorylated C-terminal tail of Rad9 (Delacroix et al., 2007) and thereby activates the checkpoint kinase ATR (Lee et al., 2007), itself tethered in the vicinity of the damaged DNA via interaction of its constitutive partner ATRIP, with RPA…”
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Self-citationChoreography of recombination proteins during the DNA damage response
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“In addition, RPA also recruits the alternative DNA clamp loader RAD17-RFC, which loads the 9-1-1 complex (RAD9-HUS1-RAD1) onto DNA [102-105].”
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“This solution as well as five 1:5 dilutions were spotted on plates without drugs and incubated for 2 days.”
BackgroundMethodInfluentialTopBP1 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
Dealing with DNA damage: Relationships between checkpoint and repair pathways
Warmerdam, D. O., & Kanaar, R. (2009) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2009.12.001 · Cited by 122
Cellular Functions of Human RPA1
Haring, S. J., Mason, A. C., Binz, S. K., & Wold, M. S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800881200 · Cited by 112
Self-citationSurvey of the year 2006 commercial optical biosensor literature
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Self-citationContinued primer synthesis at stalled replication forks contributes to checkpoint activation
Van, C., Yan, S., Michael, W. M., Waga, S., & Cimprich, K. A. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200909105 · Cited by 105
“The ssDNA–dsDNA junction is critical for the recruitment of the Rad9–Hus1–Rad1 (9-1-1) complex, a heterotrimeric clamp with structural homology to proliferating cell nuclear antigen (PCNA), which is the processivity factor for replicative polymerases (Bermudez et al., 2003; Ellison and Stillman, 2003; Zou et al., 2003…”
BackgroundInfluentialCaldwell, C. C., & Spies, M. (2020) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2020.1813070 · Cited by 106
Role of Cyclin B1 Levels in DNA Damage and DNA Damage-Induced Senescence
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“The 9-1-1 clamp is recruited to stalled forks independently of PCNA (46) at 5 primer-template junctions in vitro (35, 36).”
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Navadgi-Patil, V. M., & Burgers, P. M. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.03.011 · Cited by 93
Self-citationNoncanonical Role of the 9-1-1 Clamp in the Error-Free DNA Damage Tolerance Pathway
Karras, G. I., Fumasoni, M., Sienski, G., Vanoli, F., Branzei, D., & Jentsch, S. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.11.016 · Cited by 94
“Whereas PCNA is loaded on the 30 ends of gapped DNA (e.g., at replication forks), 9-1-1 is recruited to the 50 ends (e.g., at damaged sites), where it serves as a sensor for checkpoint signaling (Ellison and Stillman, 2003; Majka et al., 2006; Sancar et al., 2004).”
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Yao, N. Y., & O’Donnell, M. (2012) · Subcellular Biochemistry · doi:10.1007/978-94-007-4572-8_14 · Cited by 90
Anticheckpoint pathways at telomeres in yeast
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“Increased binding of Rad24 in the mutants may be a direct consequence of stronger RPA association, as RPA itself promotes Rad24 loadin”
BackgroundPhysiological Tolerance to ssDNA Enables Strand Uncoupling during DNA Replication
Ercilla, A., Benada, J., Gadi, S. A., Zonderland, G., Baldi, G., Somyajit, K., Ochs, F., Costanzo, V., Lukas, J., & Toledo, L. I. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.067 · Cited by 75
“This distinction has been a topic of discussion because active forks have a priori the same molecular requirements for ATR activation as a stalled fork, namely ssDNA (at the lagging strand) and a 50 end junction to recruit TOPBP1 and the 9-1-1 complex (MacDougall et al., 2007; Majka et al., 2006).”
BackgroundRPA Inhibition Increases Replication Stress and Suppresses Tumor Growth
Glanzer, J. G., Liu, S., Wang, L., Mosel, A., Peng, A., & Oakley, G. G. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-0306 · Cited by 79
“HAMNO induces γ-H2AX staining in a cell-cycle specific manner DBD-F binds ATRIP, Rad9, Rad17 and Nbs1 thereby recruiting and stabilizing the proteins involved in ATR activation (11, 13, 15, 27, 28).”
Timing and spacing of ubiquitin‐dependent DNA damage bypass
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“is another gene involved in DNA replication whose overexpression leads to G2/M delay. The Rfa1p protein is a subunit of the heterotrimeric replication protein A (RPA), which is involved in DNA replication, repair, and the DNA damage checkpoint”
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“Unlike RFC, which specifically recognizes 3 dsDNAssDNA junctions, the RAD17 complex preferentially recruits 9-1-1 complexes to 5 dsDNA-ssDNA junctions, which are associated with resected DSBs and stressed replication forks (Ellison and Stillman, 2003; Majka et al., 2006a; Zou et al., 2003).”
BackgroundReview: The lord of the rings: Structure and mechanism of the sliding clamp loader
Kelch, B. A. (2016) · Biopolymers · doi:10.1002/bip.22827 · Cited by 68
The fork and the kinase: A DNA replication tale from a CHK1 perspective
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ATR kinase activation in G1 phase facilitates the repair of ionizing radiation-induced DNA damage
Gamper, A. M., Rofougaran, R., Watkins, S. C., Greenberger, J. S., Beumer, J. H., & Bakkenist, C. J. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt833 · Cited by 71
“The exact origin and structure of the RPA foci/ ssDNA we observed in G1 phase are presently unknown, but considering that the structure is not a result of HDR (or replication stall), the DNA might not have the 50-recessed junction, which is needed for loading of the 9-1-1 complex (31,32).”
Giannattasio, M., & Branzei, D. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2474-4 · Cited by 67
“Dpb11Cut5/TopBP1 (DNA Polymerase B subunit 11/Cell Untimely Turn 5/Topoisomerase II Binding Protein 1) [161, 162], Ddc1Rad9/RAD9 [163], Dna2 [164] and ETAA1 (Ewing Tumor Associated Antigen 1) [165, 166] have emerged as direct activators of the apical kinases Mec1, Rad3, and ATR through physical interactions (Fig.”
BackgroundInfluentialStructural Basis of Mec1-Ddc2-RPA Assembly and Activation on Single-Stranded DNA at Sites of Damage
Deshpande, I., Seeber, A., Shimada, K., Keusch, J. J., Gut, H., & Gasser, S. M. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.09.019 · Cited by 68
“Similarly, the long unstructured C-terminal tail of 9-1-1 subunit Ddc1 can activate Mec1 kinase in vitro (Majka et al., 2006a), as well as in vivo, when artificially targeted together with Ddc2 to an integrated array of binding sites (Bonilla et al., 2008).”
BackgroundRPA Mediates Recruitment of MRX to Forks and Double-Strand Breaks to Hold Sister Chromatids Together
Seeber, A., Hegnauer, A. M., Hustedt, N., Deshpande, I., Poli, J., Eglinger, J., Pasero, P., Gut, H., Shinohara, M., Hopfner, K., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.10.032 · Cited by 74
“…for checkpoint and repair proteins, including but not limited toMec1-Ddc2 and 9-1-1, the DNA damage clamp, both at stalled forks and at DNA double-strand breaks (DSBs) (Paciotti et al., 2000; Rouse and Jackson, 2002; Xu et al., 2008; Zou and Elledge, 2003; Kanoh et al., 2006; Majka et al., 2006).”
BackgroundLoading clamps for DNA replication and repair
Bloom, L. B. (2009) · DNA repair · doi:10.1016/j.dnarep.2008.12.014 · Cited by 68
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“Indeed, activation of Mec1 in vitro depends on the appropriate loading of the Rad17-Mec3Ddc1 complex by Rad24 onto DNA (Majka et al., 2006b).”
BackgroundMethodInfluentialMammalian polymerase ζ is essential for post-replication repair of UV-induced DNA lesions
Jansen, J. G., Tsaalbi‐Shtylik, A., Hendriks, G., Verspuy, J. W. A., Gali, H., Haracska, L., & de Wind, N. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.09.006 · Cited by 64
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“Previous studies using the simple primed ssDNA substrates showed that the 3′-oriented loading of PCNA depends on RPA, which directionally binds to the ssDNA template (29, 38).”
BackgroundPCNA Loaders and Unloaders—One Ring That Rules Them All
Arbel, M., Choudhary, K., Tfilin, O., & Kupiec, M. (2021) · Genes · doi:10.3390/genes12111812 · Cited by 62
“Just artificially recruiting Ddc1 (one of the sunburnt in the 9-1-1) together with Ddc2 (the Mec1 partner) is enough to elicit the DRR [54] in the absence of DNA damage.”
BackgroundInfluentialReplication Checkpoint: Tuning and Coordination of Replication Forks in S Phase
Hustedt, N., Gasser, S. M., & Shimada, K. (2013) · Genes · doi:10.3390/genes4030388 · Cited by 62
“These structures, together with RPA, are sufficient to activate the ATR checkpoint in a cell-free system [37,50].”
BackgroundGenetic instability in budding and fission yeast—sources and mechanisms
Skoneczna, A., Kaniak, A., & Skoneczny, M. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv028 · Cited by 59
“Then the authors compared the frequency of mutational changes within those sequences with their transcription levels and were able to demonstrate simultaneously for numerous loci that positive correlation between transcription and mutagenesis does exist.”
BackgroundInfluentialQuantitative sensing and signalling of single-stranded DNA during the DNA damage response
Bantele, S. C. S., Lisby, M., & Pfander, B. (2019) · Nature Communications · doi:10.1038/s41467-019-08889-5 · Cited by 55
Send in the Clamps: Control of DNA Translesion Synthesis in Eukaryotes
Jansen, J. G., Fousteri, M. I., & de Wind, N. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.11.005 · Cited by 55
Cdc13 Telomere Capping Decreases Mec1 Association but Does Not Affect Tel1 Association with DNA Ends
Hirano, Y., & Sugimoto, K. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-12-1074 · Cited by 51
“The PCNA-like checkpoint clamps have been shown to target partial duplex DNA (Majka and Burgers, 2003; Majka et al., 2006).”
BackgroundStudying the DNA damage response using in vitro model systems
Garner, E., & Costanzo, V. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.04.015 · Cited by 47
Puddu, F., Piergiovanni, G., Plevani, P., & Muzi-Falconi, M. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002022 · Cited by 48
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“junctions (26, 48, 57), the ATR activating protein TopBP1”
BackgroundDiscovery of a Potent Stapled Helix Peptide That Binds to the 70N Domain of Replication Protein A
Frank, A. O., Vangamudi, B., Feldkamp, M. D., de Souza-Fagundes, E. M., Luzwick, J. W., Cortez, D., Olejniczak, E. T., Waterson, A. G., Rossanese, O. W., Chazin, W., et al. (2014) · Journal of Medicinal Chemistry · doi:10.1021/jm401730y · Cited by 47
RHINO forms a stoichiometric complex with the 9-1-1 checkpoint clamp and mediates ATR-Chk1 signaling
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DDK Phosphorylates Checkpoint Clamp Component Rad9 and Promotes Its Release from Damaged Chromatin
Furuya, K., Miyabe, I., Tsutsui, Y., Paderi, F., Kakusho, N., Masai, H., Niki, H., & Carr, A. M. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.10.026 · Cited by 42
“One potential function for DDK phosphorylation is thus to allow the DNA repair machinery to fully access the damage site by displacing 9-1-1 that sits at 50-DNA junction (Majka et al., 2006).”
BackgroundMultistep loading of a DNA sliding clamp onto DNA by replication factor C
Schrecker, M., Castaneda, J. C., Devbhandari, S., Kumar, C., Remus, D., & Hite, R. K. (2022) · eLife · doi:10.7554/elife.78253 · Cited by 38
“, 2003), Rad24- RFC loads the 9- 11 clamp at 5’ ss/dsDNA junctions (Ellison and Stillman, 2003; Castaneda et al., 2022; Majka et al., 2006), and Elg1- RFC appears to unload PCNA from dsDNA (Kubota et al.”
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Domenico, E. G. D., Romano, E., Porto, P. D., & Ascenzioni, F. (2014) · BioMed Research International · doi:10.1155/2014/787404 · Cited by 39
Assembly of Slx4 signaling complexes behind DNA replication forks
Balint, A., Kim, T. P., Gallo, D., Cussiol, J. R. R., de Oliveira, F. M. B., Yimit, A., Ou, J., Nakato, R., Gurevich, A., Shirahige, K., et al. (2015) · The EMBO Journal · doi:10.15252/embj.201591190 · Cited by 41
“Phosphorylation of H2A by Mec1 is promoted by Ddc1, Dpb11, and Ddc2 (Majka et al , 2006b; Mordes et al , 2008; Navadgi-Patil & Burgers, 2008, 2009b; Puddu et al , 2011; Bandhu et al , 2014), but recruitment of Mec1 to lesions independent of Ddc1 and Dpb11 is sufficient for basal kinase activity and…”
InfluentialPeritore, M., Reußwig, K.-U., Bantele, S. C. S., Straub, T., & Pfander, B. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.02.005 · Cited by 44
Zheng, F., Georgescu, R. E., Yao, N. Y., Li, H., & O’Donnell, M. E. (2022) · eLife · doi:10.7554/elife.77469 · Cited by 33
“…3 ′ ss/ds DNA junctions to load the PCNA clamp for DNA polymerases and other proteins (Kelch et al., 2012b); while Rad24-RFC primarily targets a 5 ′ ss/ds DNA junction for loading the 9-1-1 clamp to stimulate the ATR kinase (Ellison and Stillman, 2003; Majka et al., 2006; Majka and Burgers, 2003).”
BackgroundInfluentialHARPing on about the DNA damage response during replication: Figure 1.Preprint
Driscoll, R., & Cimprich, K. A. (2009) · Genes & Development · doi:10.1101/gad.1860609 · Cited by 35
“In the presence of RPA, this is thought to occur on the 59-primer end (Ellison and Stillman 2003; Majka et al. 2006).”
BackgroundSeparable roles for Mec1/ATR in genome maintenance, DNA replication, and checkpoint signalingPreprint
Lanz, M. C., Oberly, S., Sanford, E. J., Sharma, S., Chabes, A., & Smolka, M. B. (2018) · Genes & Development · doi:10.1101/gad.308148.117 · Cited by 37
“Ddc1 is a component of the yeast 9-1-1 DNA clamp that is loaded at the 5′ end of dsDNA:ssDNA junctions (Majka et al. 2006).”
BackgroundResultInfluentialKelly, R. M., & Davey, S. K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0085859 · Cited by 36
Mechanisms of loading and release of the 9-1-1 checkpoint clamp
Castaneda, J. C., Schrecker, M., Remus, D., & Hite, R. K. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00741-7 · Cited by 32
“ATRMec1 activation occurs specifically on replication protein A (RPA)-coated single-stranded DNA (ssDNA) adjacent to 5’ single-stranded/double-stranded DNA (ss/dsDNA) junctions that serve as a loading site for the 9-1-1 checkpoint clamp, which mediates ATRMec1 activation (4-6).”
BackgroundUbiquitin and SUMO signalling in DNA repair
Thomson, T. M., & Guerra‐Rebollo, M. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380116 · Cited by 34
Day, M., Oliver, A. W., & Pearl, L. H. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac588 · Cited by 32
“…at sites of ssDNA is dependent on the RAD9–RAD1–HUS1 (9–1–1) heterotrimeric checkpoint clamp (11) preferentially loaded at a 5 -recessed margin (12,13) by a specialised form of the het-eropentameric AAA+ Replication Factor C (RFC) clamp loader in which the large RFC1 subunit, required for loading…”
Rescue of replication failure by Fanconi anaemia proteins
Constantinou, A. (2011) · Chromosoma · doi:10.1007/s00412-011-0349-2 · Cited by 40
“The 5′ junction between ssDNA and dsDNA is recognised by RAD17RFC, which loads the 9–1–1 checkpoint clamp necessary for efficient ATR activation (Ellison and Stillman 2003; Majka et al. 2006; Zou et al. 2003).”
BackgroundFunctions of Multiple Clamp and Clamp-Loader Complexes in Eukaryotic DNA Replication
Ohashi, E., & Tsurimoto, T. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-6955-0_7 · Cited by 34
Cell-cycle-specific activators of the Mec1/ATR checkpoint kinase
Navadgi, V. M., & Burgers, P. (2011) · Biochemical Society Transactions · doi:10.1042/bst0390600 · Cited by 38
Self-citationDNA Damage and Replication Stress Checkpoints
Yates, L. A., Zhang, X., & Burgers, P. (2025) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-072324-031915 · Cited by 38
Self-citationDhingra, N., Wei, L., & Zhao, X. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006006 · Cited by 33
“9-1-1 then promotes Mec1 activation via allosteric stimulation of its kinase activity (6, 7).”
BackgroundFumarase is involved in DNA double-strand break resection through a functional interaction with Sae2
Leshets, M., Ramamurthy, D., Lisby, M., Lehming, N., & Pines, O. (2017) · Current Genetics · doi:10.1007/s00294-017-0786-4 · Cited by 33
The helicase Pif1 functions in the template switching pathway of DNA damage bypass
García‐Rodríguez, N., Wong, R. P. C., & Ulrich, H. D. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky648 · Cited by 33
“Notably, this model is analogous to a scenario that might apply at the 5′-junction of the gap, the loading site of the 9–1-1 checkpoint clamp (43,44).”
MethodDNA is loaded through the 9-1-1 DNA checkpoint clamp in the opposite direction of the PCNA clamp
Zheng, F., Georgescu, R. E., Yao, N. Y., O’Donnell, M. E., & Li, H. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00742-6 · Cited by 31
Ddc2 Mediates Mec1 Activation through a Ddc1- or Dpb11-Independent Mechanism
Bandhu, A., Kang, J., Fukunaga, K., Goto, G. H., & Sugimoto, K. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004136 · Cited by 32
Alver, R. C., Zhang, T., Josephrajan, A., Fultz, B. L., Hendrix, C. J., Das‐Bradoo, S., & Bielinsky, A. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku479 · Cited by 32
Depletion of RAD17 sensitizes pancreatic cancer cells to gemcitabine
Fredebohm, J., Wolf, J. M., Hoheisel, J. D., & Boettcher, M. (2013) · Journal of Cell Science · doi:10.1242/jcs.124768 · Cited by 30
Lindsey‐Boltz, L. A., Reardon, J. T., Wold, M. S., & Sancar, A. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.407825 · Cited by 31
“Phosphorylation of RPA modulates RPA interactions with checkpoint and other proteins (8, 10, 55).”
BackgroundSelf-citationHuman Exonuclease 5 Is a Novel Sliding Exonuclease Required for Genome Stability
Sparks, J. L., Kumar, R., Singh, M. K., Wold, M. S., Pandita, T. K., & Burgers, P. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.422444 · Cited by 29
“Directionality enforcement by RPA has been demonstrated previously for enzymes and factors involved in nucleotide excision repair and in theDNAdamage checkpoint, re-emphasizing the importance in carrying out these type of in vitro studies with the cognate form of RPA (29, 30).”
BackgroundSelf-citationArranging eukaryotic nuclear DNA polymerases for replication
Kunkel, T. A., & Burgers, P. (2017) · BioEssays · doi:10.1002/bies.201700070 · Cited by 30
“Examples are the checkpoint clamp 9-1-1 and Dna2 nuclease, which show promiscuous directionality on naked ssDNA but unique directionality on RPA-coated DNA [30, 31].”
BackgroundSelf-citationMolecular Mechanisms of DNA Replication Checkpoint Activation
Recolin, B., van der Laan, S., Tsanov, N., & Maiorano, D. (2014) · Genes · doi:10.3390/genes5010147 · Cited by 34
“cerevisiae, see Table 1) [113].”
9-1-1: PCNA's specialized cousin
Eichinger, C. S., & Jentsch, S. (2011) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2011.08.002 · Cited by 30
Theis, J. F., Irene, C., Dershowitz, A., Brost, R. L., Tobin, M. L., di Sanzo, F. M., Wang, J.-Y., Boone, C. M., & Newlon, C. S. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001227 · Cited by 29
“. Binding of the Rad17p-Ddc1p-Mec3p clamp results in activation of Mec1p kinase activity. Ddc1p is phosphorylated by Mec1p”
BackgroundThe Rad4TopBP1 ATR-Activation Domain Functions in G1/S Phase in a Chromatin-Dependent Manner
Lin, S.-J., Wardlaw, C. P., Morishita, T., Miyabe, I., Chahwan, C., Caspari, T., Schmidt, U. G., Carr, A. M., & Garcia, V. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002801 · Cited by 26
Recolin, B., van der Laan, S., & Maiorano, D. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1241 · Cited by 29
“We propose that the essential role of RPA in checkpoint signaling is to stabilize DNA polymerase-a at stalled forks and promote synthesis of single-stranded/double-stranded DNA hybrids as well as recruitment of the 9-1-1 complex onto this substrate mediated by Rad17, as previously suggested (8,12,16,17).”
MethodYet another job for Dna2: Checkpoint activation
Wanrooij, P. H., & Burgers, P. (2015) · DNA repair · doi:10.1016/j.dnarep.2015.04.009 · Cited by 29
“Conversely, Dna2 prefers 5′-flap structures [18,72].”
Self-citationSong, W., Pascal, J. M., Ellenberger, T., & Tomkinson, A. E. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.05.002 · Cited by 27
Metadata
- Authors
- Majka, J., Binz, S. K., Wold, M. S., & Burgers, P. M. J.
- Affiliations
- Washington University in St. Louis (US)
- University of Iowa (US)
- Corresponding author
- Burgers, Peter M.J.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2006-09
- Volume
- 281
- Issue
- 38
- Pages
- 27855-27861
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2161481116
- Cited by
- 205
- References
- 43
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 10 · 2023: 3 · 2022: 10 · 2021: 10 · 2020: 6 · 2019: 5 · 2018: 7 · 2017: 9 · 2016: 8 · 2015: 12 · 2014: 16 · 2013: 13 · 2012: 9
- FWCI
- 5.97
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (GM44721, GM-32431, R01GM044721, R01GM032431)
- 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 › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- replication protein A, clamp loading, DNA damage response, single-stranded DNA binding protein, Saccharomyces cerevisiae
- MeSH terms
- Adenosine Triphosphatases, DNA Damage, DNA Helicases, DNA-Binding Proteins, Endonucleases, Nuclear Proteins, Substrate Specificity, Cell Cycle Proteins, Proliferating Cell Nuclear Antigen, Saccharomyces cerevisiae Proteins, DNA Repair Enzymes, Intracellular Signaling Peptides and Proteins, Replication Protein A, Replication Protein C
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