Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis
Abstract
The expression of the Escherichia coli DNA polymerases pol V (UmuD'2C complex) and pol IV (DinB) increases in response to DNA damage. The induction of pol V is accompanied by a substantial increase in mutations targeted at DNA template lesions in a process called SOS-induced error-prone repair. Here we show that the common DNA template lesions, TT (6-4) photoproducts, TT cis-syn photodimers and abasic sites, are efficiently bypassed within 30 seconds by pol V in the presence of activated RecA protein (RecA*), single-stranded binding protein (SSB) and pol III's processivity beta,gamma-complex. There is no detectable bypass by either pol IV or pol III on this time scale. A mutagenic 'signature' for pol V is its incorporation of guanine opposite the 3'-thymine of a TT (6-4) photoproduct, in agreement with mutational spectra. In contrast, pol III and pol IV incorporate adenine almost exclusively. When copying undamaged DNA, pol V exhibits low fidelity with error rates of around 10(-3) to 10(-4), with pol IV being 5- to 10-fold more accurate. The effects of RecA protein on pol V, and beta,gamma-complex on pol IV, cause a 15,000- and 3,000-fold increase in DNA synthesis efficiency, respectively. However, both polymerases exhibit low processivity, adding 6 to 8 nucleotides before dissociating. Lesion bypass by pol V does not require beta,gamma-complex in the presence of non-hydrolysable ATPgammaS, indicating that an intact RecA filament may be required for translesion synthesis.
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These multiplet mutations are likely the consequence of error-prone bypass polymerization during translesion synthesis and are consistent with processivity of bypass polymerases persisting for several nucleotides after the bypass-requiring blocking lesion.
“These multiplet mutations are likely the consequence of error-prone bypass polymerization during translesion synthesis and are consistent with the processivity of bypass polymerases persisting for several nucleotides after the bypass-requiring blocking lesion (39 -41).”
From Why Cockayne syndrome patients do not get cancer despite their DNA repair deficiency (2016) · cites this paper as [41]
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A model for SOS-lesion-targeted mutations in Escherichia coli
Pham, P., Bertram, J. G., O’Donnell, M. E., Woodgate, R., & Goodman, M. F. (2001) · Nature · doi:10.1038/35053116 · Cited by 127 · see citing works
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Functional Uncoupling of Twin Polymerases
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Self-citationMeddows, T. R., Savory, A. P., Grove, J. I., Moore, T., & Lloyd, R. G. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04677.x · Cited by 119 · see citing works
DNA Damage Control by Novel DNA Polymerases: Translesion Replication and Mutagenesis
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Purification and Characterization of polκ, a DNA Polymerase Encoded by the Human DINB1 Gene
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Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase
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Self-citationMultiple Functions of DNA Polymerases
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Self-citationLessons from 50 years of SOS DNA-damage-induced mutagenesis
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The nonmutagenic repair of broken replication forks via recombination
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Inefficient Bypass of an Abasic Site by DNA Polymerase η
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The diverse spectrum of sliding clamp interacting proteins
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Human DNA polymerase kappa synthesizes DNA with extraordinarily low fidelity
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The “A” rule revisited: polymerases as determinants of mutational specificity
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Adaptive Mutation in Escherichia coliPreprint
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Coping with replication ‘train wrecks’ in Escherichia coli using Pol V, Pol II and RecA proteins
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Self-citationLow Fidelity DNA Synthesis by a Y Family DNA Polymerase Due to Misalignment in the Active Site
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Self-citationSloppier copier DNA polymerases involved in genome repair
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Self-citationSources of spontaneous mutagenesis in bacteria
Schroeder, J. W., Yeesin, P., Simmons, L. A., & Wang, J. D. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1394262 · Cited by 101 · see citing works
DNA Polymerase V and RecA Protein, a Minimal Mutasome
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Self-citationTaylor, J. (2002) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(02)00252-x · Cited by 102 · see citing works
Self-citationBiological Properties of Single Chemical−DNA Adducts: A Twenty Year Perspective
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- Authors
- Tang, M., Pham, P., Shen, X., Taylor, J.-S., O'Donnell, M., Woodgate, R., & Goodman, M. F.
- Affiliations
- University of Southern California (US)
- Washington University in St. Louis (US)
- National Institutes of Health (US)
- Corresponding author
- Goodman, Myron F.
- Venue
- Nature
- Published
- 2000-04
- Volume
- 404
- Issue
- 6781
- Pages
- 1014-1018
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1510371408
- Cited by
- 443
- References
- 30
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 6 · 2023: 5 · 2022: 7 · 2021: 5 · 2020: 9 · 2019: 6 · 2018: 12 · 2017: 14 · 2016: 10 · 2015: 10 · 2014: 19 · 2013: 13 · 2012: 21
- FWCI
- 16.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
- Keywords
- DNA polymerase IV, DNA polymerase V, DinB, SOS response, error-prone DNA repair, translesion synthesis, 6-4 photoproducts, abasic sites, RecA filament, polymerase fidelity, mutational signatures, DNA damage response
- MeSH terms
- DNA Damage, DNA-Directed DNA Polymerase, DNA, Bacterial, Escherichia coli, Rec A Recombinases, SOS Response, Genetics, Templates, Genetic, Mutagenesis, DNA Polymerase beta, Escherichia coli Proteins
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