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

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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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Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery
Datta, S. R., Dudek, H., Tao, X., Masters, S., Fu, H., Gotoh, Y., & Greenberg, M. E. (1997) · Cell · doi:10.1016/s0092-8674(00)80405-5 · Cited by 5,689
DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139
Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., & Bonner, W. M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.10.5858 · Cited by 5,438
Phosphorylation meets ubiquitination: the control of NF-κB activity
Karin, M., & Ben-Neriah, Y. (2000) · Annual Review of Immunology · doi:10.1146/annurev.immunol.18.1.621 · Cited by 4,766
DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation
Bakkenist, C. J., & Kastan, M. B. (2003) · Nature · doi:10.1038/nature01368 · Cited by 3,466
Structure, Recognition, and Processing of Cisplatin−DNA Adducts
Jamieson, E. R., & Lippard, S. J. (1999) · Chemical Reviews · doi:10.1021/cr980421n · Cited by 2,953
NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation.
Wang, C.-Y., Mayo, M., Korneluk, R., Goeddel, D., & Baldwin, A. (1998) · Science · doi:10.1126/science.281.5383.1680 · Cited by 2,950
Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes
Zou, L., & Elledge, S. J. (2003) · Science · doi:10.1126/science.1083430 · Cited by 2,693
Serine Phosphorylation of Death Agonist BAD in Response to Survival Factor Results in Binding to 14-3-3 Not BCL-XL
Zha, J., Harada, H., Yang, E., Jockel, J., & Korsmeyer, S. J. (1996) · Cell · doi:10.1016/s0092-8674(00)81382-3 · Cited by 2,578
Biochemical Pathways of Caspase Activation During Apoptosis
Budihardjo, I. I., Oliver, H., Lutter, M. L., Luo, X., & Wang, X. (1999) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.15.1.269 · Cited by 2,577
Regulation of Cell Death Protease Caspase-9 by Phosphorylation
Cardone, M. H., Roy, N., Stennicke, H. R., Salvesen, G. S., Franke, T. F., Stanbridge, E., Frisch, S., & Reed, J. C. (1998) · Science · doi:10.1126/science.282.5392.1318 · Cited by 2,481

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Peto, 1984, IARC Sci. Publ., 627
Roos, 2007, Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O(6)-methylguanine, Oncogene, 26, 186, 10.1038/sj.onc.1209785 · DOI

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Ming, X., Bo, Z., Miao, Y., Chen, H., Bao, C., Sun, L., Xi, R., Zhong, Q., Zhao, P., Jung, Y., et al. (2022) · The FASEB Journal · doi:10.1096/fj.202101360rr · Cited by 14
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Kamakura, N., Yamamoto, J., Brooks, P. J., Iwai, S., & Kuraoka, I. (2012) · Chemical Research in Toxicology · doi:10.1021/tx300351p · Cited by 14

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
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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