Error-Prone Repair DNA Polymerases in Prokaryotes and Eukaryotes

Goodman, Myron F.

doi:10.1146/annurev.biochem.71.083101.124707

Cited by 727DNA Repair MechanismsDNA and Nucleic Acid ChemistryBacterial Genetics and Biotechnology

Error-Prone Repair DNA Polymerases in Prokaryotes and Eukaryotes

Goodman, Myron F.·2002·Annual Review of Biochemistry

DOI 10.1146/annurev.biochem.71.083101.124707

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Abstract

▪ Abstract DNA repair is crucial to the well-being of all organisms from unicellular life forms to humans. A rich tapestry of mechanistic studies on DNA repair has emerged thanks to the recent discovery of Y-family DNA polymerases. Many Y-family members carry out aberrant DNA synthesis—poor replication accuracy, the favored formation of non-Watson-Crick base pairs, efficient mismatch extension, and most importantly, an ability to replicate through DNA damage. This review is devoted primarily to a discussion of Y-family polymerase members that exhibit error-prone behavior. Roles for these remarkable enzymes occur in widely disparate DNA repair pathways, such as UV-induced mutagenesis, adaptive mutation, avoidance of skin cancer, and induction of somatic cell hypermutation of immunoglobulin genes. Individual polymerases engaged in multiple repair pathways pose challenging questions about their roles in targeting and trafficking. Macromolecular assemblies of replication-repair “factories” could enable a cell to handle the complex logistics governing the rapid migration and exchange of polymerases.

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“Translesion synthesis (TLS) polymerases copy past lesions in DNA that block the major replicative polymerases (7)(8)(9)(10)(11).”
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Escherichia coli DNA polymerase II is stimulated by DNA polymerase III holoenzyme auxiliary subunits
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Identification and Characterization of Human DNA Polymerase β2, a DNA Polymerase β-Related Enzyme
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Lesion Bypass by the Escherichia coli DNA Polymerase V Requires Assembly of a RecA Nucleoprotein Filament
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Visualization of two binding sites for the Escherichia coli UmuD′2C complex (DNA pol V) on RecA-ssDNA filaments
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Self-citation
Mutagenic and Nonmutagenic Bypass of DNA Lesions byDrosophila DNA Polymerases dpolη and dpolι
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Isolation and genetic characterisation of the Drosophila homologue of (SCE)REV3, encoding the catalytic subunit of DNA polymerase ζ
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Persistent bacterial infections and persister cells
Fisher, R. A., Gollan, B., & Helaine, S. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.42 · Cited by 1,243 · see citing works
DNA damage and repair
Friedberg, E. C. (2003) · Nature · doi:10.1038/nature01408 · Cited by 1,177 · see citing works
Proliferating cell nuclear antigen (PCNA): a dancer with many partners
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Mutations induced by ultraviolet light
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DNA Replication Fidelity
Kunkel, T. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.r400006200 · Cited by 754 · see citing works
Eukaryotic DNA Polymerases
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Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase
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Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation
Pham, P., Bransteitter, R., Petruska, J. A., & Goodman, M. F. (2003) · Nature · doi:10.1038/nature01760 · Cited by 657 · see citing works
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A semi-synthetic organism with an expanded genetic alphabet
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Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products
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Long-term survival during stationary phase: evolution and the GASP phenotype
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Stationary phase in gram-negative bacteria
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The Biochemistry of Somatic Hypermutation
Peled, J. U., Kuang, F. L., Iglesias-Ussel, M. D., Roa, S., Kalis, S. L., Goodman, M. F., & Scharff, M. D. (2008) · Annual Review of Immunology · doi:10.1146/annurev.immunol.26.021607.090236 · Cited by 460 · see citing works
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The SOS system: A complex and tightly regulated response to DNA damage
Masłowska, K. H., Makiela‐Dzbenska, K., & Fijałkowska, I. J. (2018) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22267 · Cited by 460 · see citing works
Adaptive mutability of colorectal cancers in response to targeted therapies
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The Bacterial RecA Protein and the Recombinational DNA Repair of Stalled Replication Forks
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DNA Polymerase γ, The Mitochondrial Replicase
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DnaE2 Polymerase Contributes to In Vivo Survival and the Emergence of Drug Resistance in Mycobacterium tuberculosis
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Why nature really chose phosphate
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Translesion synthesis: Y-family polymerases and the polymerase switch
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What a difference a decade makes: Insights into translesion DNA synthesis
Yang, W., & Woodgate, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704219104 · Cited by 377 · see citing works
Trading Places: How Do DNA Polymerases Switch during Translesion DNA Synthesis?
Friedberg, E. C., Lehmann, A. R., & Fuchs, R. P. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.03.032 · Cited by 376 · see citing works
Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis
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Nucleotide Excision Repair
Reardon, J. T., & Sancar, A. (2005) · Progress in Nucleic Acid Research and Molecular Biology · doi:10.1016/s0079-6603(04)79004-2 · Cited by 350 · see citing works
The Structural Mechanism of Translocation and Helicase Activity in T7 RNA Polymerase
Yin, Y. W., & Steitz, T. A. (2004) · Cell · doi:10.1016/s0092-8674(04)00120-5 · Cited by 337 · see citing works
Translesion DNA Polymerases
Goodman, M. F., & Woodgate, R. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a010363 · Cited by 317 · see citing works
Self-citation
Human DNA Polymerase η Promotes DNA Synthesis from Strand Invasion Intermediates of Homologous Recombination
McIlwraith, M. J., Vaisman, A., Liu, Y., Fanning, E., Woodgate, R., & West, S. C. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.10.001 · Cited by 304 · see citing works
Estimation of the Spontaneous Mutation Rate per Nucleotide Site in a Drosophila melanogaster Full-Sib Family
Keightley, P. D., Ness, R. W., Halligan, D. L., & Haddrill, P. R. (2013) · Genetics · doi:10.1534/genetics.113.158758 · Cited by 293 · see citing works
Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals
Shachar, S., Ziv, O., Avkin, S., Adar, S., Wittschieben, J., Reißner, T., Chaney, S., Friedberg, E. C., Wang, Z., Carell, T., et al. (2009) · The EMBO Journal · doi:10.1038/emboj.2008.281 · Cited by 284 · see citing works
Beyond A, C, G and T: augmenting nature’s alphabet
Henry, A. A., & Romesberg, F. E. (2003) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2003.10.011 · Cited by 272 · see citing works
Suffering in silence: the tolerance of DNA damage
Friedberg, E. C. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1781 · Cited by 271 · see citing works
Immunoglobulin Gene Diversification
Maizels, N. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.110544 · Cited by 264 · see citing works
Functions of DNA polymerases
Bebenek, K., & Kunkel, T. A. (2004) · Advances in Protein Chemistry · doi:10.1016/s0065-3233(04)69005-x · Cited by 258 · see citing works
A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates
Jarosz, D. F., Godoy, V. G., Delaney, J. C., Essigmann, J. M., & Walker, G. C. (2006) · Nature · doi:10.1038/nature04318 · Cited by 258 · see citing works
Interaction of hREV1 with three human Y‐family DNA polymerases
Ohashi, E., Murakumo, Y., Kanjo, N., Akagi, J., Masutani, C., Hanaoka, F., & Ohmori, H. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00747.x · Cited by 256 · see citing works
Structure of a Sliding Clamp on DNA
Georgescu, R. E., Kim, S.-S., Yurieva, O., Kuriyan, J., Kong, X., & O’Donnell, M. E. (2008) · Cell · doi:10.1016/j.cell.2007.11.045 · Cited by 239 · see citing works
Toxicity of Nucleoside Analogues Used to Treat AIDS and the Selectivity of the Mitochondrial DNA Polymerase
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The Hydantoin Lesions Formed from Oxidation of 7,8-Dihydro-8-oxoguanine Are Potent Sources of Replication Errors in Vivo
Henderson, P. T., Delaney, J. C., Muller, J. G., Neeley, W. L., Tannenbaum, S. R., Burrows, C. J., & Essigmann, J. M. (2003) · Biochemistry · doi:10.1021/bi0347252 · Cited by 216 · see citing works
DNA polymerase θ (POLQ), double-strand break repair, and cancer
Wood, R. D., & Doublié, S. (2016) · DNA repair · doi:10.1016/j.dnarep.2016.05.003 · Cited by 214 · see citing works
High‐efficiency bypass of DNA damage by human DNA polymerase Q
Seki, M., Masutani, C., Yang, L. W., Schuffert, A., Iwai, S., Bahar, İ., & Wood, R. D. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600424 · Cited by 209 · see citing works
Co-localization in replication foci and interaction of human Y-family members, DNA polymerase polη and REVl protein
Tissier, A., Kannouche, P. L., Reck, M.-P., Lehmann, A. R., Fuchs, R. P., & Cordonnier, A. M. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.06.015 · Cited by 207 · see citing works
Error‐prone DNA polymerase IV is controlled by the stress‐response sigma factor, RpoS, in Escherichia coli
Layton, J. C., & Foster, P. L. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03704.x · Cited by 206 · see citing works
Genetic Composition of the Bacillus subtilis SOS System
Au, N., Kuester-Schoeck, E., Mandava, V., Bothwell, L. E., Canny, S., Chachu, K. A., Colavito, S. A., Fuller, S. N., Groban, E. S., Hensley, L. A., et al. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.22.7655-7666.2005 · Cited by 206 · see citing works
SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness
Yeiser, B., Pepper, E. D., Goodman, M. F., & Finkel, S. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092269199 · Cited by 202 · see citing works
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Revisiting the Central Dogma in the 21st Century
Shapiro, J. A. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04990.x · Cited by 199 · see citing works
Challenges and complexities in estimating both the functional impact and the disease risk associated with the extensive genetic variation in human DNA repair genes
Mohrenweiser, H. W., Wilson, D. M., & Jones, I. M. (2003) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(03)00049-6 · Cited by 198 · see citing works
Stress responses and genetic variation in bacteria
Foster, P. L. (2004) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2004.07.017 · Cited by 196 · see citing works
Tracing the network connecting brca and fanconi anaemia proteins
Venkitaraman, A. R. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1321 · Cited by 196 · see citing works
Induction of somatic hypermutation in immunoglobulin genes is dependent on DNA polymerase iota
Faili, A., Aoufouchi, S., Flatter, E., Guéranger, Q., Reynaud, C., & Weill, J. (2002) · Nature · doi:10.1038/nature01117 · Cited by 196 · see citing works
A Sliding-Clamp Toolbelt Binds High- and Low-Fidelity DNA Polymerases Simultaneously
Indiani, C., McInerney, P., Georgescu, R. E., Goodman, M. F., & O’Donnell, M. E. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.08.011 · Cited by 194 · see citing works
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The replisome uses mRNA as a primer after colliding with RNA polymerase
Pomerantz, R. T., & O’Donnell, M. E. (2008) · Nature · doi:10.1038/nature07527 · Cited by 190 · see citing works
Localization of DNA polymerases η and ι to the replication machinery is tightly co‐ordinated in human cells
Kannouche, P. L., de Henestrosa, A. R. F., Coull, B. J., Vidal, A. E., Gray, C., Zicha, D., Woodgate, R., & Lehmann, A. R. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf618 · Cited by 190 · see citing works
Snapshots of Replication through an Abasic Lesion
Ling, H., Boudsocq, F., Woodgate, R., & Yang, W. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00101-7 · Cited by 186 · see citing works
Error-Prone DNA Polymerases: When Making a Mistake is the Only Way to Get Ahead
Rattray, A. J., & Strathern, J. N. (2003) · Annual Review of Genetics · doi:10.1146/annurev.genet.37.042203.132748 · Cited by 182 · see citing works
Overview of Tumor Cell Chemoresistance Mechanisms
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Single-molecule DNA repair in live bacteria
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Generic expansion of the substrate spectrum of a DNA polymerase by directed evolution
Ghadessy, F. J., Ramsay, N. A., Boudsocq, F., Loakes, D., Brown, A. P. C., Iwai, S., Vaisman, A., Woodgate, R., & Holliger, P. (2004) · Nature Biotechnology · doi:10.1038/nbt974 · Cited by 178 · see citing works
Rev1 is essential for DNA damage tolerance and non‐templated immunoglobulin gene mutation in a vertebrate cell line
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Chemistry and Biology of DNA Containing 1,N2-Deoxyguanosine Adducts of the α,β-Unsaturated Aldehydes Acrolein, Crotonaldehyde, and 4-Hydroxynonenal
Minko, I. G., Kozekov, I. D., Harris, T. M., Rizzo, C. J., Lloyd, R. S., & Stone, M. P. (2009) · Chemical Research in Toxicology · doi:10.1021/tx9000489 · Cited by 176 · see citing works
The critical mutagenic translesion DNA polymerase Rev1 is highly expressed during G 2 /M phase rather than S phase
Waters, L. S., & Walker, G. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510167103 · Cited by 171 · see citing works
Crystal Structure of the Catalytic α Subunit of E. coli Replicative DNA Polymerase III
Lamers, M. H., Georgescu, R. E., Lee, S.-G., O’Donnell, M. E., & Kuriyan, J. (2006) · Cell · doi:10.1016/j.cell.2006.07.028 · Cited by 167 · see citing works
High incidence of epithelial cancers in mice deficient for DNA polymerase δ proofreading
Goldsby, R. E., Hays, L. E., Chen, X., Olmsted, E. A., Slayton, W. B., Spangrude, G. J., & Preston, B. D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.232340999 · Cited by 166 · see citing works
Why High-error-rate Random Mutagenesis Libraries are Enriched in Functional and Improved Proteins
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DNA replication fidelity in Escherichia coli : a multi-DNA polymerase affair
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DNA Helicases Required for Homologous Recombination and Repair of Damaged Replication Forks
Wu, L., & Hickson, I. D. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090636 · Cited by 158 · see citing works
Structural Insights into the Origins of DNA Polymerase Fidelity
Beard, W. A., & Wilson, S. H. (2003) · Structure · doi:10.1016/s0969-2126(03)00051-0 · Cited by 157 · see citing works
Evolutionary significance of stress-induced mutagenesis in bacteria
Tenaillon, O., Denamur, É., & Matić, I. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2004.04.002 · Cited by 157 · see citing works
Checkpoint activation regulates mutagenic translesion synthesisPreprint
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An analogy between the evolution of drug resistance in bacterial communities and malignant tissues
Lambert, G., Estévez-Salmerón, L., Oh, S., Liao, D., Emerson, B. M., Tlsty, T. D., & Austin, R. H. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3039 · Cited by 155 · see citing works
Y-family DNA polymerases in Escherichia coli
Jarosz, D. F., Beuning, P. J., Cohen, S., & Walker, G. C. (2007) · Trends in Microbiology · doi:10.1016/j.tim.2006.12.004 · Cited by 152 · see citing works
Damage repair DNA polymerases Y
Yang, W. (2003) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(02)00003-9 · Cited by 152 · see citing works
Environmental Stress and Lesion-Bypass DNA Polymerases
Nohmi, T. (2006) · Annual Review of Microbiology · doi:10.1146/annurev.micro.60.080805.142238 · Cited by 150 · see citing works
In vitro mutation artifacts after formalin fixation and error prone translesion synthesis during PCR
Quach, N., Goodman, M. F., & Shibata, D. K. (2004) · BMC Clinical Pathology · doi:10.1186/1472-6890-4-1 · Cited by 149 · see citing works
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Transcriptional Mutagenesis Induced by Uracil and 8-Oxoguanine in Escherichia coli
Brégeon, D., Doddridge, Z. A., You, H. J., Weiss, B., & Doetsch, P. W. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00360-5 · Cited by 146 · see citing works
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Efficient and accurate bypass of N 2 -(1-carboxyethyl)-2′-deoxyguanosine by DinB DNA polymerase in vitro and in vivo
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Fidelity of Escherichia coli DNA Polymerase IV
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Self-citation
Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro
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Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site
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A new model for SOS-induced mutagenesis: how RecA protein activates DNA polymerase V
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Repair mechanisms for oxidative DNA damage
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Mass Spectrometry of Structurally Modified DNA
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Error-prone replication for better or worse
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Damage of DNA and proteins by major lipid peroxidation products in genome stability
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Role of DNA Polymerase η in the UV Mutation Spectrum in Human Cells
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Loss of DNA Polymerase ζ Causes Chromosomal Instability in Mammalian Cells
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Authors: Goodman, M. F.
Affiliations: University of Southern California (US)
Corresponding author: Goodman, Myron F.
ORCID: Goodman, Myron F.
Venue: Annual Review of Biochemistry
Publisher: Annual Reviews
Published: 2002-06
Volume: 71
Issue: 1
Pages: 17-50
ISSN: 0066-4154 (ISSN-L)
1545-4509
DOI: 10.1146/annurev.biochem.71.083101.124707
OpenAlex: W2142513910
Cited by: 727
References: 202
Citations by year: 2026: 4 · 2025: 5 · 2024: 6 · 2023: 9 · 2022: 8 · 2021: 6 · 2020: 14 · 2019: 13 · 2018: 17 · 2017: 18 · 2016: 14 · 2015: 17 · 2014: 30 · 2013: 36 · 2012: 36
FWCI: 5.40
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Biochemistry (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5p01ag017179-03, 5r01gm042554-13)
National Institute on Aging (AG17179)
National Institute of General Medical Sciences (GM 42554, GM 21422)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Y-family DNA polymerases, error-prone DNA replication, DNA repair, mismatch extension, UV mutagenesis, adaptive mutation, skin cancer prevention, immunoglobulin genes
MeSH terms: Animals, DNA Damage, DNA-Directed DNA Polymerase, DNA Repair, DNA Replication, Escherichia coli, Eukaryotic Cells, Humans, Models, Genetic, Mutation, Nuclear Proteins, SOS Response, Genetics, Protein Structure, Tertiary, Somatic Hypermutation, Immunoglobulin

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Error-Prone Repair DNA Polymerases in Prokaryotes and Eukaryotes

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