The DNA Damage Response: Making It Safe to Play with Knives

Ciccia, Alberto; Elledge, Stephen J.

doi:10.1016/j.molcel.2010.09.019

Cited by 4,368DNA Repair MechanismsCancer-related Molecular PathwaysPARP inhibition in cancer therapy

The DNA Damage Response: Making It Safe to Play with Knives

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Ciccia, Alberto, Elledge, Stephen J.·2010·Molecular Cell

DOI 10.1016/j.molcel.2010.09.019PMC PMC2988877

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Abstract

Damage to our genetic material is an ongoing threat to both our ability to faithfully transmit genetic information to our offspring as well as our own survival. To respond to these threats, eukaryotes have evolved the DNA damage response (DDR). The DDR is a complex signal transduction pathway that has the ability to sense DNA damage and transduce this information to the cell to influence cellular responses to DNA damage. Cells possess an arsenal of enzymatic tools capable of remodeling and repairing DNA; however, their activities must be tightly regulated in a temporal, spatial, and DNA lesion-appropriate fashion to optimize repair and prevent unnecessary and potentially deleterious alterations in the structure of DNA during normal cellular processes. This review will focus on how the DDR controls DNA repair and the phenotypic consequences of defects in these critical regulatory functions in mammals.

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Poly-ADP-ribose chains act as a scaffold for repair proteins, ensuring effective recruitment of SSBR and DSBR machinery.
“Poly-ADP-ribose chains act as a scaffold for repair proteins, ensuring effective recruitment of single-strand break repair (SSBR) and double-strand break repair (DSBR) machinery.”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
PARP1 and PARP2 are the main enzymes with a function in damage signaling.
“PARP1 and PARP2 are the main enzymes with a function in damage signaling.”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
PAR chains are rapidly disassembled by PARG, allowing the whole event to repeat.
“Poly-ADP-ribose (PAR) chains are rapidly disassembled by poly (ADP-ribose) glycohydrolase (PARG), allowing the whole event to repeat [55,66].”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
PARPs work as signaling molecules in single-strand break repair.
“In contrast, poly [ADP-ribose] polymerases (PARPs) work as signaling molecules in single-strand break repair.”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
PARPs catalyze a conserved posttranslational modification transferring ADP-ribose residues from NAD+ onto amino acid moieties of various proteins, including histones and PARP itself, forming poly-ADP-ribose chains.
“PARPs catalyze an evolutionary conserved posttranslational modification in which ADP-ribose residues from nicotinamide adenine dinucleotide (NAD+) molecules are transferred onto amino acid moieties of various proteins, including histone proteins and PARP itself, leading to polymeric ADP-ribose chains formation.”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]

PARP1 is responsible for the majority of ADP-ribosylation events in the cell.
“In fact, PARP1 is responsible for the majority of ADP-ribosylation events in cell.”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
PARP binding is only temporary due to emerging electrostatic interactions.
“PARP binding is only temporary due to emerging electrostatic interactions.”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
MRE11, a component of the MRN complex, possesses endo- and exonucleolytic activity that enables single-stranded DNA formation.
“Double-strand break repair protein (MRE11), one of the components of MRN possess endo and exonucleolytic activity that enables single strand DNA (ssDNA) formation [55,118].”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
ssDNA is coated with RPA protein, which contributes to the stability of DNA fragments and forms a platform for RAD51.
“ssDNA is then coated with RPA protein that comprise to the stability of DNA fragments and form a platform for DNA repair protein RAD51 (RAD51) protein [55].”
From Focus on UV-Induced DNA Damage and Repair—Disease Relevance and Protective Strategies (2020) · cites this paper as [55]
Checkpoints actively stimulate repair processes and, in higher eukaryotes, trigger apoptosis when damage cannot be successfully dealt with.
“The checkpoints also actively stimulate the repair processes [1–9] and, in higher eukaryotes, trigger the apoptotic response, if damage cannot be dealt with successfully [10–12].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [9]
DDR pathways that safeguard genomic integrity may show reduced activity in stem cells with age.
“These observations suggest that DDR pathways, evolved to safeguard genomic integrity and maximize survival of the organism13,44–46, may show reduced activity in stem cells with age.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [44]
ATR is critical for UV DNA damage signaling and is linked with NER.
“ATR (ATM and Rad3-related) is critical to UV DNA damage signaling (Ciccia and Elledge, 2010) and is intimately linked with NER”
From RETRACTED: PKA-Mediated Phosphorylation of ATR Promotes Recruitment of XPA to UV-Induced DNA Damage (2014) · cites this paper as Ciccia and Elledge, 2010
Oxidative stress is estimated to cause roughly 10,000 DNA alterations per cell each day, accounting for a major share of endogenous DNA damage.
“It is estimated that oxidative stress may induce approximately 10,000 DNA alterations per cell per day, representing a major portion of endogenous DNA damage [17–20].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [19]
Oxidative stress can produce many forms of DNA damage or replication stress, including base and sugar damage, AP sites, single-strand breaks, double-strand breaks, tandem base modifications, interstrand crosslinks, protein-DNA crosslinks, mismatched pairs with damaged bases, stalled replication forks, and oxidatively generated clustered lesions.
“Oxidative stress can induce a variety of different types of DNA damage or replication stress, such as base (purine and pyrimidine) damage, sugar moiety damage, Apurinic/apyrimidinic (AP) sites, DNA single-strand breaks (SSBs), DNA double-strand breaks (DSBs), tandem base modifications (e.g., DNA intrastrand crosslink), DNA interstrand crosslinks, protein–DNA crosslinks, mismatched pairs with dam”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [19]
Cells use multiple DNA repair and DNA damage response pathways to preserve genomic integrity after oxidative DNA damage.
“In response to oxidative DNA damage, various DNA repair and DNA damage response (DDR) pathways are employed by cells to maintain genomic integrity [12, 18, 19, 31]”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [19]
DNA damage response pathways are conserved surveillance mechanisms that coordinate DNA repair, cell cycle progression, transcription, apoptosis, and senescence.
“To maintain genome stability, the DDR pathways are conserved surveillance mechanisms coordinating DNA repair, cell cycle progression, transcription, apoptosis, and senescence [19, 39–41].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [19]

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Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia
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Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4–ligase IV during chromosomal translocation formation
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Regulation of DNA Repair through DeSUMOylation and SUMOylation of Replication Protein A Complex
Dou, H., Huang, C., Singh, M. M., Carpenter, P. B., & Yeh, E. T. H. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.07.021 · Cited by 212 · see citing works
FANCM and FAAP24 Function in ATR-Mediated Checkpoint Signaling Independently of the Fanconi Anemia Core Complex
Collis, S. J., Ciccia, A., Deans, A. J., Hořejšı́, Z., Martin, J. S., Maslen, S., Skehel, M. J., Elledge, S. J., West, S. C., & Boulton, S. J. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.10.014 · Cited by 210 · see citing works
Self-citation
A genetic screen identifies the Triple T complex required for DNA damage signaling and ATM and ATR stability
Hurov, K. E., Cotta-Ramusino, C., & Elledge, S. J. (2010) · Genes & Development · doi:10.1101/gad.1934210 · Cited by 210 · see citing works
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MHF1-MHF2, a Histone-Fold-Containing Protein Complex, Participates in the Fanconi Anemia Pathway via FANCM
Singh, T. R., Saro, D., Ali, A. M., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.036 · Cited by 201 · see citing works
DNA Polymerases as Potential Therapeutic Targets for Cancers Deficient in the DNA Mismatch Repair Proteins MSH2 or MLH1
Martin, S. A., McCabe, N., Mullarkey, M. J., Cummins, R., Burgess, D. J., Nakabeppu, Y., Oka, S., Kay, E. W., Lord, C. J., & Ashworth, A. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.046 · Cited by 201 · see citing works
Defective embryonic neurogenesis in Ku-deficient but not DNA-dependent protein kinase catalytic subunit-deficient mice
Gu, Y., Sekiguchi, J., Gao, Y., Dikkes, P., Frank, K. M., Ferguson, D. O., Hasty, P., Chun, J. J. M., & Alt, F. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.6.2668 · Cited by 198 · see citing works
Ku is a 5′-dRP/AP lyase that excises nucleotide damage near broken ends
Roberts, S. A., Strande, N. T., Burkhalter, M. D., Strom, C. N., Havener, J. M., Hasty, P., & Ramsden, D. A. (2010) · Nature · doi:10.1038/nature08926 · Cited by 196 · see citing works
Cell cycle–dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24
Kim, J. M., Kee, Y., Gurtan, A. M., & D’Andrea, A. D. (2008) · Blood · doi:10.1182/blood-2007-09-113092 · Cited by 189 · see citing works
Role of Double-Stranded DNA Translocase Activity of Human HLTF in Replication of Damaged DNA
Blastyák, A., Hajdú, I., Unk, I., & Haracska, L. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00863-09 · Cited by 187 · see citing works
Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexesPreprint
Takai, H., Xie, Y., de Lange, T., & Pavletich, N. P. (2010) · Genes & Development · doi:10.1101/gad.1956410 · Cited by 186 · see citing works
Recent Advances in Cancer Therapy Targeting Proteins Involved in DNA Double-Strand Break Repair
Bolderson, E., Richard, D. J., Zhou, B. S., & Khanna, K. K. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0096 · Cited by 185 · see citing works
Phosphorylation of Exo1 modulates homologous recombination repair of DNA double-strand breaks
Bolderson, E., Tomimatsu, N., Richard, D. J., Boucher, D., Kumar, R., Pandita, T. K., Burma, S., & Khanna, K. K. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1164 · Cited by 184 · see citing works
RIDDLE immunodeficiency syndrome is linked to defects in 53BP1-mediated DNA damage signaling
Stewart, G. S., Stanković, T., Byrd, P. J., Wechsler, T., Miller, E. S., Huissoon, A., Drayson, M. T., West, S. C., Elledge, S. J., & Taylor, A. M. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708408104 · Cited by 183 · see citing works
Self-citation
RecQ helicases: guardian angels of the DNA replication fork
Bachrati, C. Z., & Hickson, I. D. (2008) · Chromosoma · doi:10.1007/s00412-007-0142-4 · Cited by 180 · see citing works
Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance
Unk, I., Hajdú, I., Blastyák, A., & Haracska, L. (2010) · DNA repair · doi:10.1016/j.dnarep.2009.12.013 · Cited by 178 · see citing works
The DNA Damage Response Arouses the Immune System
Gasser, S., & Raulet, D. H. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4603 · Cited by 178 · see citing works
DNA damage and decisions: CtIP coordinates DNA repair and cell cycle checkpoints
You, Z., & Bailis, J. M. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.04.002 · Cited by 176 · see citing works
Drosophila MUS312 and the Vertebrate Ortholog BTBD12 Interact with DNA Structure-Specific Endonucleases in DNA Repair and Recombination
Andersen, S. L., Bergstralh, D. T., Kohl, K. P., LaRocque, J. R., Moore, C. B., & Sekelsky, J. J. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.06.019 · Cited by 175 · see citing works
NBA1, a new player in the Brca1 A complex, is required for DNA damage resistance and checkpoint control
Wang, B., Hurov, K., Hofmann, K., & Elledge, S. J. (2009) · Genes & Development · doi:10.1101/gad.1770309 · Cited by 172 · see citing works
Self-citation
Identification of a novel, widespread, and functionally important PCNA-binding motif
Gilljam, K. M., Feyzi, E., Aas, P. A., de Sousa, M. M. L., Müller, R., Vågbø, C. B., Catterall, T., Liabakk, N., Slupphaug, G., Drabløs, F., et al. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200903138 · Cited by 169 · see citing works
DNA Repair Defects in Stem Cell Function and Aging
Park, Y., & Gerson, S. L. (2004) · Annual Review of Medicine · doi:10.1146/annurev.med.56.082103.104546 · Cited by 166 · see citing works
MERIT40 facilitates BRCA1 localization and DNA damage repairPreprint
Feng, L., Huang, J., & Chen, J. (2009) · Genes & Development · doi:10.1101/gad.1770609 · Cited by 163 · see citing works
Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage
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
Regulation of Translesion Synthesis DNA Polymerase η by Monoubiquitination
Bienko, M., Green, C., Sabbioneda, S., Crosetto, N., Matić, I., Hibbert, R. G., Begovic, T., Niimi, A., Mann, M., Lehmann, A. R., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2009.12.039 · Cited by 160 · see citing works
A PP4 phosphatase complex dephosphorylates RPA2 to facilitate DNA repair via homologous recombination
Lee, D.-H., Pan, Y., Kanner, S., Sung, P., Borowiec, J. A., & Chowdhury, D. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1769 · Cited by 157 · see citing works
MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks
Wu, L., Luo, K., Lou, Z., & Chen, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802885105 · Cited by 156 · see citing works
ATR activation and replication fork restart are defective in FANCM‐deficient cells
Schwab, R. A., Blackford, A. N., & Niedźwiedź, W. (2010) · The EMBO Journal · doi:10.1038/emboj.2009.385 · Cited by 155 · see citing works
MERIT40 controls BRCA1–Rap80 complex integrity and recruitment to DNA double-strand breaksPreprint
Shao, G., Patterson-Fortin, J., Messick, T. E., Feng, D., Shanbhag, N. M., Wang, Y., & Greenberg, R. A. (2009) · Genes & Development · doi:10.1101/gad.1739609 · Cited by 154 · see citing works
A novel human AP endonuclease with conserved zinc‐finger‐like motifs involved in DNA strand break responses
Kanno, S., Kuzuoka, H., Sasao, S., Hong, Z., Lan, L., Nakajima, S., & Yasui, A. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601663 · Cited by 153 · see citing works
14-3-3 proteins, FHA domains and BRCT domains in the DNA damage response
Mohammad, D. H., & Yaffe, M. B. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.04.004 · Cited by 152 · see citing works
Replication checkpoint kinase Cds1 regulates Mus81 to preserve genome integrity during replication stressPreprint
Kai, M., Boddy, M. N., Russell, P. R., & Wang, T. S. ‐. (2005) · Genes & Development · doi:10.1101/gad.1304305 · Cited by 145 · see citing works
53BP1: function and mechanisms of focal recruitment
FitzGerald, J. E., Grenon, M., & Lowndes, N. F. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370897 · Cited by 141 · see citing works
The annealing helicase HARP protects stalled replication forksPreprint
Yuan, J., Ghosal, G., & Chen, J. (2009) · Genes & Development · doi:10.1101/gad.1836409 · Cited by 141 · see citing works
Dephosphorylation of the C-terminal Tyrosyl Residue of the DNA Damage-related Histone H2A.X Is Mediated by the Protein Phosphatase Eyes Absent
Krishnan, N., Jeong, D. G., Jung, S., Ryu, S. E., Xiao, A., Allis, C. D., Kim, S. J., & Tonks, N. K. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.c900032200 · Cited by 140 · see citing works
RAG-dependent primary immunodeficiencies
Sobacchi, C., Marrella, V., Rucci, F., Vezzoni, P., & VILLA, A. M. (2006) · Human Mutation · doi:10.1002/humu.20408 · Cited by 136 · see citing works
Essential role of Tip60-dependent recruitment of ribonucleotide reductase at DNA damage sites in DNA repair during G1 phasePreprint
Niida, H., Katsuno, Y., Sengoku, M., Shimada, M., Yukawa, M., Ikura, M., Ikura, T., Kohno, K., Shima, H., Suzuki, H., et al. (2010) · Genes & Development · doi:10.1101/gad.1863810 · Cited by 136 · see citing works
The FANCM/FAAP24 Complex Is Required for the DNA Interstrand Crosslink-Induced Checkpoint Response
Huang, M., ‍Kim, J. M., Shiotani, B., Yang, K., Zou, L., & D’Andrea, A. D. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.07.005 · Cited by 134 · see citing works
The annealing helicase HARP is recruited to DNA repair sites via an interaction with RPAPreprint
Yusufzai, T. M., Kong, X., Yokomori, K., & Kadonaga, J. T. (2009) · Genes & Development · doi:10.1101/gad.1831509 · Cited by 134 · see citing works
A RECQ5–RNA polymerase II association identified by targeted proteomic analysis of human chromatin
Aygün, O., Svejstrup, J. Q., & Liu, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804424105 · Cited by 133 · see citing works
Human ELG1 Regulates the Level of Ubiquitinated Proliferating Cell Nuclear Antigen (PCNA) through Its Interactions with PCNA and USP1
Lee, K., Yang, K., Cohn, M. A., Sikdar, N., D’Andrea, A. D., & Myung, K. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.092544 · Cited by 133 · see citing works
The neurological phenotype of ataxia-telangiectasia: Solving a persistent puzzle
Biton, S., Barzilai, A., & Shiloh, Y. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.03.006 · Cited by 133 · see citing works
Mre11–Rad50–Nbs1‐dependent processing of DNA breaks generates oligonucleotides that stimulate ATM activity
Jazayeri, A. R., Balestrini, A., Garner, E., Haber, J. E., & Costanzo, V. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.128 · Cited by 131 · see citing works
The ubiquitin landscape at DNA double-strand breaks
Messick, T. E., & Greenberg, R. A. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200908074 · Cited by 130 · see citing works

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Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
Oxidative stress and autophagy: The clash between damage and metabolic needs
Filomeni, G., De Zio, D., & Cecconi, F. (2015) · Cell Death & Differentiation · doi:10.1038/cdd.2014.150 · Cited by 2,195 · see citing works
ROS and the DNA damage response in cancer
Srinivas, U. S., Tan, B. W. Q., Vellayappan, B. A., & Jeyasekharan, A. D. (2019) · Redox Biology · doi:10.1016/j.redox.2018.101084 · Cited by 2,144 · see citing works
“This response includes DNA damage recognition, activation of checkpoints, cell cycle arrest, and eventually final outcomes of repair, apoptosis and immune clearance [4,5].”
Background
Mechanisms of DNA damage, repair, and mutagenesis
Chatterjee, N., & Walker, G. C. (2017) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22087 · Cited by 2,039 · 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
cGAS surveillance of micronuclei links genome instability to innate immunity
Mackenzie, K. J., Carroll, P., Martin, C.-A., Murina, O., Fluteau, A., Simpson, D. J., Olova, N., Sutcliffe, H., Rainger, J. K., Leitch, A., et al. (2017) · Nature · doi:10.1038/nature23449 · Cited by 1,752 · see citing works
The ATM protein kinase: regulating the cellular response to genotoxic stress, and more
Shiloh, Y., & Ziv, Y. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3546 · Cited by 1,649 · 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
CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes
Liang, P., Xu, Y., Zhang, X., Ding, C., Huang, R., Zhang, Z., Lv, J., Xie, X., Chen, Y., Li, Y., et al. (2015) · Protein & Cell · doi:10.1007/s13238-015-0153-5 · Cited by 1,135 · see citing works
Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications
Polo, S. E., & Jackson, S. P. (2011) · Genes & Development · doi:10.1101/gad.2021311 · Cited by 1,092 · see citing works
p38MAPK is a novel DNA damage response‐independent regulator of the senescence‐associated secretory phenotype
Freund, A., Patil, C. K., & Campisi, J. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.69 · Cited by 1,039 · see citing works
The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4.
Kang, C., Xu, Q., Martin, T. D., Li, M. Z., Demaria, M., Aron, L., Lu, T., Yankner, B. A., Campisi, J., & Elledge, S. J. (2015) · Science · doi:10.1126/science.aaa5612 · Cited by 982 · see citing works
Self-citation
Oxidative Stress in Human Pathology and Aging: Molecular Mechanisms and Perspectives
Hajam, Y. A., Rani, R., Ganie, S. Y., Sheikh, T. A., Javaid, D., Qadri, S. S., Pramodh, S., Alsulimani, A., Alkhanani, M. F., Harakeh, S., et al. (2022) · Cells · doi:10.3390/cells11030552 · Cited by 915 · see citing works
Stem cell aging: mechanisms, regulators and therapeutic opportunities
Oh, J., Lee, Y. D., & Wagers, A. J. (2014) · Nature Medicine · doi:10.1038/nm.3651 · Cited by 796 · see citing works
Catastrophic nuclear envelope collapse in cancer cell micronuclei
Hatch, E. M., Fischer, A. H., Deerinck, T. J., & Hetzer, M. W. (2013) · Cell · doi:10.1016/j.cell.2013.06.007 · Cited by 741 · see citing works
Small-molecule–induced DNA damage identifies alternative DNA structures in human genes
Rodriguez, R., Miller, K. M., Forment, J. V., Bradshaw, C. R., Nikan, M., Britton, S., Oelschlaegel, T., Xhemalce, B., Balasubramanian, S., & Jackson, S. P. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.780 · Cited by 741 · see citing works
Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells
Flach, J., Bakker, S. T., Mohrin, M., Conroy, P. C., Pietras, E. M., Reynaud, D., Alvarez, S., Diolaiti, M. E., Ugarte, F., Forsberg, E. C., et al. (2014) · Nature · doi:10.1038/nature13619 · Cited by 650 · see citing works
More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance
Lukas, J., Lukas, C., & Bartek, J. (2011) · Nature Cell Biology · doi:10.1038/ncb2344 · Cited by 645 · see citing works
The effects of deregulated DNA damage signalling on cancer chemotherapy response and resistance
Bouwman, P., & Jonkers, J. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3342 · Cited by 615 · see citing works
Chromatin Remodeling at DNA Double-Strand Breaks
Price, B. D., & D’Andrea, A. D. (2013) · Cell · doi:10.1016/j.cell.2013.02.011 · Cited by 588 · see citing works
Targeted genome editing in human repopulating haematopoietic stem cells
Genovese, P., Schiroli, G., Escobar, G., Di Tomaso, T., Firrito, C., Calabria, A., Moi, D., Mazzieri, R., Bonini, C., Holmes, M. C., et al. (2014) · Nature · doi:10.1038/nature13420 · Cited by 555 · see citing works
ARID1A Deficiency Impairs the DNA Damage Checkpoint and Sensitizes Cells to PARP Inhibitors
Shen, J., Peng, Y., Wei, L., Zhang, W., Yang, L., Lan, L., Kapoor, P., Ju, Z., Mo, Q., Shih, I.-M., et al. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-14-0849 · Cited by 522 · see citing works
The cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes
Blazek, D., Kohoutek, J., Bartholomeeusen, K., Johansen, E., Hulinkova, P., Luo, Z., Cimermancic, P., Ule, J., & Peterlin, B. M. (2011) · Genes & Development · doi:10.1101/gad.16962311 · Cited by 522 · see citing works
Heterochromatin: Guardian of the Genome
Janssen, A., Colmenares, S. U., & Karpen, G. H. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062653 · Cited by 500 · see citing works
RPA-coated single-stranded DNA as a platform for post-translational modifications in the DNA damage response
Maréchal, A., & Zou, L. (2015) · Cell Research · doi:10.1038/cr.2014.147 · Cited by 465 · see citing works
Causes of genome instability
Aguilera, A., & García-Muse, T. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133232 · Cited by 476 · see citing works
The p53 network: cellular and systemic DNA damage responses in aging and Cancer
Reinhardt, H. C., & Schumacher, B. (2012) · Trends in Genetics · doi:10.1016/j.tig.2011.12.002 · Cited by 458 · see citing works
CHK2 kinase in the DNA damage response and beyond
Zannini, L., Delia, D., & Buscemi, G. (2014) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mju045 · Cited by 455 · see citing works
A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response
Adamson, B., Smogorzewska, A., Sigoillot, F. D., King, R. W., & Elledge, S. J. (2012) · Nature Cell Biology · doi:10.1038/ncb2426 · Cited by 433 · see citing works
Self-citation
SIRT4 Has Tumor-Suppressive Activity and Regulates the Cellular Metabolic Response to DNA Damage by Inhibiting Mitochondrial Glutamine Metabolism
Jeong, S. M., Xiao, C., Finley, L. W. S., Lahusen, T., Souza, A. L., Pierce, K., Li, Y.-H., Wang, X., Laurent, G., German, N. J., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.02.024 · Cited by 445 · see citing works
DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin
Ayrapetov, M. K., Gursoy-Yuzugullu, O., Xu, C., Xu, Y., & Price, B. D. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1403565111 · Cited by 391 · see citing works
DNA damage responses and p53 in the aging process
Ou, H.-L., & Schumacher, B. (2018) · Blood · doi:10.1182/blood-2017-07-746396 · Cited by 377 · see citing works
SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling
Toiber, D., Erdel, F., Bouazoune, K., Silberman, D. M., Zhong, L., Mulligan, P., Sebastian, C., Cosentino, C., Martinez-Pastor, B., Giacosa, S., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.06.018 · Cited by 381 · see citing works
DNA Damage in Stem Cells
Vitale, I., Manic, G., De Maria, R., Kroemer, G., & Galluzzi, L. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.04.006 · Cited by 361 · see citing works
The Role of SIRT1 on DNA Damage Response and Epigenetic Alterations in Cancer
Alves-Fernandes, D. K., & Jasiulionis, M. G. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133153 · Cited by 385 · see citing works
Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography
Thompson, L. H. (2012) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2012.06.002 · Cited by 357 · see citing works
Functional transcription promoters at DNA double-strand breaks mediate RNA-driven phase separation of damage-response factors
Pessina, F., Giavazzi, F., Yin, Y., Gioia, U., Vitelli, V., Galbiati, A., Barozzi, S., Garre, M., Oldani, A., Flaus, A., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0392-4 · Cited by 360 · see citing works
Prime, Repair, Restore: The Active Role of Chromatin in the DNA Damage Response
Soria, G., Polo, S. E., & Almouzni, G. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.06.002 · Cited by 342 · see citing works
Precise Gene Editing Preserves Hematopoietic Stem Cell Function following Transient p53-Mediated DNA Damage Response
Schiroli, G., Conti, A., Ferrari, S., della Volpe, L., Jacob, A., Albano, L., Beretta, S., Calabria, A., Vavassori, V., Gasparini, P., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.02.019 · Cited by 342 · see citing works
Mechanisms that Regulate Stem Cell Aging and Life Span
Signer, R. A. J., & Morrison, S. J. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.01.001 · Cited by 320 · see citing works
Distinct but Concerted Roles of ATR, DNA-PK, and Chk1 in Countering Replication Stress during S Phase
Buisson, R., Boisvert, J. L., Benes, C. H., & Zou, L. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.029 · Cited by 316 · see citing works
RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair
Galanty, Y., Belotserkovskaya, R., Coates, J., & Jackson, S. P. (2012) · Genes & Development · doi:10.1101/gad.188284.112 · Cited by 314 · see citing works
DNA damage induces reactive oxygen species generation through the H2AX-Nox1/Rac1 pathway
Kang, M. A., So, E.-Y., Simons, A. L., Spitz, D. R., & Ouchi, T. (2012) · Cell Death & Disease · doi:10.1038/cddis.2011.134 · Cited by 311 · see citing works
Nuclear Acetyl-CoA Production by ACLY Promotes Homologous Recombination
Sivanand, S., Rhoades, S., Jiang, Q., Lee, J. V., Benci, J., Zhang, J., Yuan, S., Viney, I., Zhao, S., Carrer, A., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.06.008 · Cited by 295 · 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
DNA Damage Response: Three Levels of DNA Repair Regulation
Sirbu, B. M., & Cortez, D. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012724 · Cited by 272 · see citing works
Nuclear initiated NF-κB signaling: nemo and ATM take center stage
Miyamoto, S. (2011) · Cell Research · doi:10.1038/cr.2010.179 · Cited by 253 · see citing works
The core spliceosome as target and effector of non-canonical ATM signalling
Tresini, M., Warmerdam, D. O., Kolovos, P., Snijder, L., Vrouwe, M. G., Demmers, J. A. A., van IJcken, W. F. J., Grosveld, F. G., Medema, R. H., Hoeijmakers, J. H. J., et al. (2015) · Nature · doi:10.1038/nature14512 · Cited by 252 · see citing works
Do DNA Double-Strand Breaks Drive Aging?
White, R. R., & Vijg, J. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.08.004 · Cited by 232 · see citing works
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Authors: Ciccia, A., & Elledge, S. J.
Affiliations: Brigham and Women's Hospital (US)
Corresponding author: Elledge, Stephen J.
ORCID: Ciccia, Alberto
Elledge, Stephen J.
Venue: Molecular Cell
Publisher: Elsevier BV
Published: 2010-10
Volume: 40
Issue: 2
Pages: 179-204
ISSN: 1097-2765 (ISSN-L)
DOI: 10.1016/j.molcel.2010.09.019
PMC: PMC2988877
OpenAlex: W2077436902
Cited by: 4,368
References: 246
Citations by year: 2026: 198 · 2025: 240 · 2024: 246 · 2023: 301 · 2022: 292 · 2021: 335 · 2020: 343 · 2019: 308 · 2018: 292 · 2017: 303 · 2016: 329 · 2015: 289 · 2014: 288 · 2013: 269 · 2012: 201
FWCI: 16.84
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1056 d)
Locations: Molecular Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Howard Hughes Medical Institute
National Institute of General Medical Sciences (R37GM044664)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
Keywords: DNA damage response, DNA repair, signal transduction, DNA damage recognition, DNA repair regulation, mammalian cells, genetic stability, genome stability
MeSH terms: Animals, DNA, DNA Damage, DNA Repair, Models, Genetic, Recombination, Genetic, Signal Transduction, DNA Breaks, Double-Stranded, Eukaryota

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The DNA Damage Response: Making It Safe to Play with Knives

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