DNA damage-induced cell death: From specific DNA lesions to the DNA damage response and apoptosis

Roos, Wynand P.; Kaina, Bernd

doi:10.1016/j.canlet.2012.01.007

Cited by 881DNA Repair MechanismsCell death mechanisms and regulationCancer-related Molecular Pathways

DNA damage-induced cell death: From specific DNA lesions to the DNA damage response and apoptosis

Roos, Wynand P., Kaina, Bernd·2013·Cancer Letters

DOI 10.1016/j.canlet.2012.01.007

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Abstract

DNA damaging agents are potent inducers of cell death triggered by apoptosis. Since these agents induce a plethora of different DNA lesions, it is firstly important to identify the specific lesions responsible for initiating apoptosis before the apoptotic executing pathways can be elucidated. Here, we describe specific DNA lesions that have been identified as apoptosis triggers, their repair and the signaling provoked by them. We discuss methylating agents such as temozolomide, ionizing radiation and cisplatin, all of them are important in cancer therapy. We show that the potentially lethal events for the cell are O(6)-methylguanine adducts that are converted by mismatch repair into DNA double-strand breaks (DSBs), non-repaired N-methylpurines and abasic sites as well as bulky adducts that block DNA replication leading to DSBs that are also directly induced following ionizing radiation. Transcriptional inhibition may also contribute to apoptosis. Cells are equipped with sensors that detect DNA damage and relay the signal via kinases to executors, who on their turn evoke a process that inhibits cell cycle progression and provokes DNA repair or, if this fails, activate the receptor and/or mitochondrial apoptotic cascade. The main DNA damage recognition factors MRN and the PI3 kinases ATM, ATR and DNA-PK, which phosphorylate a multitude of proteins and thus induce the DNA damage response (DDR), will be discussed as well as the downstream players p53, NF-κB, Akt and survivin. We review data and models describing the signaling from DNA damage to the apoptosis executing machinery and discuss the complex interplay between cell survival and death.

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Phosphorylation of downstream proteins by ATR leads to cell cycle arrest, DNA repair activation, and apoptotic death after severe damage.
“Phosphorylation activates these downstream proteins resulting in arrest of cell cycle progression, activation of DNA repair and, in cases of severe damage, apoptotic cell death 22, 34, 35.”
From Xeroderma Pigmentosa Group A (XPA), Nucleotide Excision Repair and Regulation by ATR in Response to Ultraviolet Irradiation (2017) · cites this paper as [35]

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The γH2AX Assay for Genotoxic and Nongenotoxic Agents: Comparison of H2AX Phosphorylation with Cell Death Response
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Cold Atmospheric Plasma Induces Apoptosis and Oxidative Stress Pathway Regulation in T‐Lymphoblastoid Leukemia Cells
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Pharmacologic inhibition of ATR and ATM offers clinically important distinctions to enhancing platinum or radiation response in ovarian, endometrial, and cervical cancer cells
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Promoting Apoptosis, a Promising Way to Treat Breast Cancer With Natural Products: A Comprehensive Review
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Enhanced Histone Deacetylase Activity in Malignant Melanoma Provokes RAD51 and FANCD2-Triggered Drug Resistance
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Strategy to enhance the therapeutic effect of doxorubicin in human hepatocellular carcinoma by selenocystine, a synergistic agent that regulates the ROS-mediated signaling
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Chemical Design of Magnetic Nanomaterials for Imaging and Ferroptosis-Based Cancer Therapy
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Strategic formulation of apigenin-loaded PLGA nanoparticles for intracellular trafficking, DNA targeting and improved therapeutic effects in skin melanoma in vitro
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Integrin α6/Akt/Erk signaling is essential for human breast cancer resistance to radiotherapy
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Ovarian Follicle Depletion Induced by Chemotherapy and the Investigational Stages of Potential Fertility-Protective Treatments—A Review
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Cell toxicity mechanism and biomarker
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Mechanistic Modelling of Radiation Responses
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Double‐strand DNA break repair: molecular mechanisms and therapeutic targets
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Mismatch Repair Deficiency as a Predictive Biomarker for Immunotherapy Efficacy
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Polyphenols: Major regulators of key components of DNA damage response in cancer
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Epigenetic inactivation of tumour suppressor coding and non-coding genes in human cancer: an update
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Olaparib modulates DNA repair efficiency, sensitizes cervical cancer cells to cisplatin and exhibits anti-metastatic property
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APTO-253 Stabilizes G-quadruplex DNA, Inhibits MYC Expression, and Induces DNA Damage in Acute Myeloid Leukemia Cells
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Uniform Widespread Nuclear Phosphorylation of Histone H2AX Is an Indicator of Lethal DNA Replication Stress
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Authors: Roos, W. P., & Kaina, B.
Affiliations: Johannes Gutenberg University Mainz (DE)
Corresponding author: Kaina, Bernd
ORCID: Roos, Wynand P.
Kaina, Bernd
Venue: Cancer Letters
Publisher: Elsevier BV
Published: 2013-05
Volume: 332
Issue: 2
Pages: 237-248
ISSN: 0304-3835 (ISSN-L)
DOI: 10.1016/j.canlet.2012.01.007
OpenAlex: W2064488040
Cited by: 879
References: 187
Citations by year: 2026: 40 · 2025: 37 · 2024: 52 · 2023: 77 · 2022: 77 · 2021: 76 · 2020: 79 · 2019: 63 · 2018: 89 · 2017: 55 · 2016: 64 · 2015: 67 · 2014: 58 · 2013: 32 · 2012: 12
FWCI: 4.93
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Cancer Letters (publishedVersion)
PubMed (publishedVersion)
Funders: Universitätsmedizin der Johannes Gutenberg-Universität Mainz
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Keywords: DNA damage response, apoptosis, DNA lesions, DNA mismatch repair, DNA double-strand breaks, abasic sites, bulky DNA adducts, ionizing radiation, temozolomide, cisplatin, DNA repair, MRN complex, ATM, ATR, DNA-dependent protein kinase, p53, NF-κB, Akt, survivin, transcriptional inhibition, cell cycle arrest, cancer therapy
MeSH terms: Survivin, Animals, Antineoplastic Agents, Cell Cycle, DNA, DNA Damage, DNA Repair, Guanine, Humans, Neoplasms, Phosphorylation, Radiation, Ionizing, Signal Transduction, NF-kappa B, Cell Death, Apoptosis, DNA Adducts, Inhibitor of Apoptosis Proteins, Proto-Oncogene Proteins c-akt

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DNA damage-induced cell death: From specific DNA lesions to the DNA damage response and apoptosis

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