DNA polymerases and cancer

Lange, Sabine S.; Takata, Kei-ichi; Wood, Richard D.

doi:10.1038/nrc2998

Cited by 615DNA Repair MechanismsGenetic factors in colorectal cancerCancer-related Molecular Pathways

DNA polymerases and cancer

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Lange, Sabine S., Takata, Kei-ichi, Wood, Richard D.·2011·Nature Reviews Cancer

DOI 10.1038/nrc2998PMC PMC3739438

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Abstract

There are 15 different DNA polymerases encoded in mammalian genomes, which are specialized for replication, repair or the tolerance of DNA damage. New evidence is emerging for lesion-specific and tissue-specific functions of DNA polymerases. Many point mutations that occur in cancer cells arise from the error-generating activities of DNA polymerases. However, the ability of some of these enzymes to bypass DNA damage may actually defend against chromosome instability in cells, and at least one DNA polymerase, Pol ζ, is a suppressor of spontaneous tumorigenesis. Because DNA polymerases can help cancer cells tolerate DNA damage, some of these enzymes might be viable targets for therapeutic strategies.

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Polη is the prototypic TLS polymerase and the only TLS polymerase known whose defects cause a human syndrome, the variant form of XP.
“DNA polymerase ␩ (Pol␩, encoded by the POLH gene) is the prototypic TLS polymerase and the only TLS polymerase known which defects lead to a human syndrome [20], the variant form of XP (XP-V) [11].”
From Gap-filling and bypass at the replication fork are both active mechanisms for tolerance of low-dose ultraviolet-induced DNA damage in the human genome (2014) · cites this paper as [20]

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Translesion Synthesis by Human DNA Polymerase η across Thymine Glycol Lesions
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DNA Repair Synthesis Facilitates RAD52-Mediated Second-End Capture during DSB Repair
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DNA polymerase kappa, implicated in spontaneous and DNA damage-induced mutagenesis, is overexpressed in lung cancer.
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Evidence that in Xeroderma Pigmentosum Variant Cells, which Lack DNA Polymerase η, DNA Polymerase ι Causes the Very High Frequency and Unique Spectrum of UV-Induced Mutations
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Phenotype-Based Identification of Mouse Chromosome Instability Mutants
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Human DNA Polymerase η Is Required for Common Fragile Site Stability during Unperturbed DNA Replication
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UV-B Radiation Induces Epithelial Tumors in Mice Lacking DNA Polymerase η and Mesenchymal Tumors in Mice Deficient for DNA Polymerase ι
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POLN, a Nuclear PolA Family DNA Polymerase Homologous to the DNA Cross-link Sensitivity Protein Mus308
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DNA Polymerase ζ Regulates Cisplatin Cytotoxicity, Mutagenicity, and The Rate of Development of Cisplatin Resistance
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Quantitative measurement of translesion replication in human cells: Evidence for bypass of abasic sites by a replicative DNA polymerase
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Expression of DNA polymerase β cancer-associated variants in mouse cells results in cellular transformation
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Human DNA polymerase iota protects cells against oxidative stress
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Participation of mouse DNA polymerase ι in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer
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DNA Polymerase POLN Participates in Cross-Link Repair and Homologous Recombination
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Human DNA polymerase possesses 5'-dRP lyase activity and functions in single-nucleotide base excision repair in vitro
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Identification of a novel REV1‐interacting motif necessary for DNA polymerase κ function
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The Roles of REV3 and RAD57 in Double-Strand-Break-Repair-Induced Mutagenesis of Saccharomyces cerevisiae
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Polymerase η mRNA Expression Predicts Survival of Non–Small Cell Lung Cancer Patients Treated with Platinum-Based Chemotherapy
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REV3 and REV1 Play Major Roles in Recombination-independent Repair of DNA Interstrand Cross-links Mediated by Monoubiquitinated Proliferating Cell Nuclear Antigen (PCNA)
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Association of terminal deoxynucleotidyl transferase with Ku
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Role of DNA polymerases η, ι and ζ in UV resistance and UV-induced mutagenesis in a human cell line
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Increased Susceptibility to UV-Induced Skin Carcinogenesis in Polymerase η–deficient Mice
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Immunodetection of DNA Repair Endonuclease ERCC1-XPF in Human Tissue
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Replication through an abasic DNA lesion: structural basis for adenine selectivity
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Analysis of specialized DNA polymerases expression in human gliomas: association with prognostic significance
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High fidelity and lesion bypass capability of human DNA polymerase δ
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hREV3 is essential for error-prone translesion synthesis past UV or benzo[a]pyrene diol epoxide-induced DNA lesions in human fibroblasts
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Involvement of Mouse Rev3 in Tolerance of Endogenous and Exogenous DNA Damage
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Translesion Synthesis past Acrolein-derived DNA Adduct, γ-Hydroxypropanodeoxyguanosine, by Yeast and Human DNA Polymerase η
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Double-strand breaks induce homologous recombinational repair of interstrand cross-links via cooperation of MSH2, ERCC1-XPF, REV3, and the Fanconi anemia pathway
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Xeroderma Pigmentosum-Variant Patients from America, Europe, and Asia
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The Mitochondrial DNA Polymerase in Health and Disease
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The BRCT domain of mammalian Rev1 is involved in regulating DNA translesion synthesis
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Expression of human and mouse genes encoding polκ: testis‐specific developmental regulation and AhR‐dependent inducible transcription
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Cloning and characterization of the common fragile site FRA6F harboring a replicative senescence gene and frequently deleted in human tumors
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Lack of DNA Polymerase θ (POLQ) Radiosensitizes Bone Marrow Stromal CellsIn Vitroand Increases Reticulocyte Micronuclei after Total-Body Irradiation
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ATR Homolog Mec1 Controls Association of DNA Polymerase ζ-Rev1 Complex with Regions near a Double-Strand Break
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The catalytic activity of REV1 is employed during immunoglobulin gene diversification in DT40
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DNA REPAIR AND MUTAGENESIS, 2ND EDITION
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Structure of the Human Rev1–DNA–dNTP Ternary Complex
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Error-free replicative bypass of thymine glycol by the combined action of DNA polymerases κ and ζ in human cells
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Replication Bypass of the Acrolein-Mediated Deoxyguanine DNA-Peptide Cross-Links by DNA Polymerases of the DinB Family
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Multiple regions of chromosome 4 demonstrating allelic losses in breast carcinomas.
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A cancer-associated DNA polymerase δ variant modeled in yeast causes a catastrophic increase in genomic instability
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Polζ ablation in B cells impairs the germinal center reaction, class switch recombination, DNA break repair, and genome stability
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Haploinsufficiency in DNA Polymerase β Increases Cancer Risk with Age and Alters Mortality Rate
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REV1 restrains DNA polymerase ζ to ensure frame fidelity during translesion synthesis of UV photoproducts in vivo
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Decreased frequency and highly aberrant spectrum of ultraviolet-induced mutations in the hprt gene of mouse fibroblasts expressing antisense RNA to DNA polymerase zeta.
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Localization of the Deoxyribose Phosphate Lyase Active Site in Human DNA Polymerase ι by Controlled Proteolysis
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Loss of DNA Polymerase ζ Enhances Spontaneous Tumorigenesis
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Polk mutant mice have a spontaneous mutator phenotype
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Inhibitors of DNA polymerase β: Activity and mechanism
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Mammalian polymerase ζ is essential for post-replication repair of UV-induced DNA lesions
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Limited terminal transferase in human DNA polymerase μ defines the required balance between accuracy and efficiency in NHEJ
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Novel Enzymatic Function of DNA Polymerase ν in Translesion DNA Synthesis Past Major Groove DNA−Peptide and DNA−DNA Cross-Links
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Sequence context-dependent replication of DNA templates containing UV-induced lesions by human DNA polymerase ι
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Cells deficient in the base excision repair protein, DNA polymerase beta, are hypersensitive to oxaliplatin chemotherapy
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A real-time fluorescence method for enzymatic characterization of specialized human DNA polymerases
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A human DNA polymerase η complex containing Rad18, Rad6 and Rev1; proteomic analysis and targeting of the complex to the chromatin‐bound fraction of cells undergoing replication fork arrest
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Down-regulation of DNA polymerases κ, η, ι, and ζ in human lung, stomach, and colorectal cancers
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Mutational Specificity of γ-Radiation-Induced Guanine−Thymine and Thymine−Guanine Intrastrand Cross-Links in Mammalian Cells and Translesion Synthesis Past the Guanine−Thymine Lesion by Human DNA Polymerase η
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A Novel Inhibitor of DNA Polymerase β Enhances the Ability of Temozolomide to Impair the Growth of Colon Cancer Cells
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Translesion synthesis of 7,8-dihydro-8-oxo-2′-deoxyguanosine by DNA polymerase eta in vivo
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“, lesions induced by ionizing radiation, including 8-oxo”
Background
The Translesion Polymerase Rev3L in the Tolerance of Alkylating Anticancer Drugs
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A Critical Role for REV1 in Regulating the Induction of C:G Transitions and A:T Mutations during Ig Gene Hypermutation
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DNA polymerase β is critical for mouse meiotic synapsis
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DNA polymerases ν and θ are required for efficient immunoglobulin V gene diversification in chicken
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Evidence for the Involvement of Human DNA Polymerase N in the Repair of DNA Interstrand Cross-Links
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Overexpression of DNA polymerase results in an increased rate of frameshift mutations during base excision repair
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Separate Roles of Structured and Unstructured Regions of Y-Family DNA Polymerases
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Upregulation of Error-Prone DNA Polymerases Beta and Kappa Slows Down Fork Progression Without Activating the Replication Checkpoint
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A unique error signature for human DNA polymerase ν
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Reevaluation of the role of DNA polymerase θ in somatic hypermutation of immunoglobulin genes
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[9]McCulloch SD Kunkel TA The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res 2008 PMC3639319 18166979
[113]Daigaku Y Davies AA Ulrich HD Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 2010 465 951 955 20453836 PMC2888004
[180]Lemée F POLQ up-regulation is associated with poor survival in breast cancer, perturbs DNA replication and promotes genetic instability Proc Natl Acad Sci (USA) 2010 107 13390 13395 20624954 PMC2922118

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Authors: Lange, S. S., Takata, K.-I., & Wood, R. D.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
Corresponding author: Wood, Richard D.
ORCID: Lange, Sabine S.
Takata, Kei-ichi
Wood, Richard D.
Venue: Nature Reviews Cancer
Publisher: Springer Science and Business Media LLC
Published: 2011-01-24
Volume: 11
Issue: 2
Pages: 96-110
ISSN: 1474-175X (ISSN-L)
1474-1768
DOI: 10.1038/nrc2998
PMC: PMC3739438
OpenAlex: W2078485114
Cited by: 615
References: 201
Citations by year: 2026: 16 · 2025: 20 · 2024: 49 · 2023: 49 · 2022: 26 · 2021: 27 · 2020: 30 · 2019: 35 · 2018: 34 · 2017: 58 · 2016: 55 · 2015: 48 · 2014: 49 · 2013: 45 · 2012: 54
FWCI: 4.91
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature reviews. Cancer (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
University of Texas MD Anderson Cancer Center
National Cancer Institute (CA132840, R01CA132840, P01CA097175, CA09717, P30CA016672)
National Institute of Environmental Health Sciences (P30ES007784)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Keywords: DNA polymerase, cancer, translesion synthesis, DNA damage tolerance, DNA replication, DNA repair, spontaneous tumor development, chromosomal instability, point mutations, therapeutic target
MeSH terms: Cell Transformation, Neoplastic, DNA-Directed DNA Polymerase, DNA Repair, Humans, Neoplasms, Gene Expression Regulation, Neoplastic, Molecular Targeted Therapy

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