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polι, a remarkably error-prone human DNA polymerase
Open accessAbstract
The Saccharomyces cerevisiae RAD30 gene encodes DNA polymerase η. Humans possess two Rad30 homologs. One ( RAD30A/POLH ) has previously been characterized and shown to be defective in humans with the Xeroderma pigmentosum variant phenotype. Here, we report experiments demonstrating that the second human homolog ( RAD30B ), also encodes a novel DNA polymerase that we designate polι. polι, is a distributive enzyme that is highly error-prone when replicating undamaged DNA. At template G or C, the average error frequency was ∼1 × 10 −2 . Our studies revealed, however, a striking asymmetry in misincorporation frequency at template A and T. For example, template A was replicated with the greatest accuracy, with misincorporation of G, A, or C occurring with a frequency of ∼1 × 10 −4 to 2 × 10 −4 . In dramatic contrast, most errors occurred at template T, where the misincorporation of G was, in fact, favored ∼3:1 over the correct nucleotide, A, and misincorporation of T occurred at a frequency of ∼6.7 × 10 −1 . These findings demonstrate that polι is one of the most error-prone eukaryotic polymerases reported to date and exhibits an unusual misincorporation spectrum in vitro.
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“The most striking violation of Watson-Crick base pairing rules is exhibited by Pol , which inserts dGTP opposite template T even more efficiently than it inserts A opposite T (12-14), i.e. its error rate for this mispair approaches 1 (Fig. 1).”
From DNA Replication Fidelity (2004) · cites this paper as [12]
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“…of one or two mismatched nucleotides by a low processivity, error-prone polymerase (mispair inserter), such as the recently identified pol ι (Rad30B) (Tissier et al., 2000), pol κ (Ohashi et al., 2000), pol λ (Aoufouchi et al., 2000; Garcia-Diaz et al., 2000), or, perhaps, pol μ…”
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Self-citationInteraction with PCNA Is Essential for Yeast DNA Polymerase η Function
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“Co-infection in Sf9 insect cells and pull-downs of poli and polh Recombinant virus expressing poli tagged with GST at its N-terminus was made as previously described (Tissier et al., 2000b).”
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Sutton, M. D., & Walker, G. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111036998 · Cited by 184
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“The in vitro data obtained by others has shown that pol is a highly error-prone DNA polymerase (16).”
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Highly Frequent Frameshift DNA Synthesis by Human DNA Polymerase μ
Zhang, Y., Wu, X., Yuan, F., Xie, Z., & Wang, Z. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.23.7995-8006.2001 · Cited by 83
Spatz, A., Giglia‐Mari, G., Benhamou, S., & Sarasin, A. R. (2001) · PubMed · Cited by 82
Boudsocq, F. (2002) · DNA Repair · doi:10.1016/s1568-7864(02)00019-8 · Cited by 79
Translesion Synthesis: Insights into the Selection and Switching of DNA Polymerases
Zhao, L., & Washington, M. T. (2017) · Genes · doi:10.3390/genes8010024 · Cited by 82
Localisation of human Y-family DNA polymerase κ: relationship to PCNA foci
Ogi, T., Kannouche, P. L., & Lehmann, A. R. (2004) · Journal of Cell Science · doi:10.1242/jcs.01603 · Cited by 79
“Polι is a paralog of polη (Tissier et al., 2000), but despite extensive studies on its activities in vitro, its function in vivo remains unknown.”
BackgroundPlosky, B. S., Frank, E. G., Berry, D. A., Vennall, G. P., McDonald, J. P., & Woodgate, R. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn058 · Cited by 79
Self-citationLi, Z., Xiao, W., McCormick, J. J., & Maher, V. M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062047799 · Cited by 77
Choi, J., & Guengerich, F. P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600112200 · Cited by 74
A neomorphic cancer cell-specific role of MAGE-A4 in trans-lesion synthesis
Gao, Y., Mutter‐Rottmayer, E., Greenwalt, A., Goldfarb, D., Yan, F., Yang, Y., Martinez‐Chacin, R. C., Pearce, K. H., Tateishi, S., Major, M. B., et al. (2016) · Nature Communications · doi:10.1038/ncomms12105 · Cited by 74
Lesion Bypass of N2-Ethylguanine by Human DNA Polymerase ι
Pence, M. G., Blans, P., Zink, C. N., Hollis, T., Fishbein, J. C., & Perrino, F. W. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807296200 · Cited by 73
Sabbioneda, S., Gourdin, A. M., Green, C., Zotter, A., Giglia‐Mari, G., Houtsmuller, A. B., Vermeulen, W., & Lehmann, A. R. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-07-0724 · Cited by 77
“Pol is a paralogue of pol (Tissier et al., 2000), but its precise function remains to be established.”
BackgroundFrank, E. G. (2002) · Nucleic Acids Research · doi:10.1093/nar/gkf643 · Cited by 72
Self-citationWhat role for AID: mutator, or assembler of the immunoglobulin mutasome?
Reynaud, C., Aoufouchi, S., Faili, A., & Weill, J. (2003) · Nature Immunology · doi:10.1038/ni0703-631 · Cited by 72
Translesion DNA Polymerases and Cancer
Makridakis, N. M., & Reichardt, J. K. V. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00174 · Cited by 70
Johnson, R. E., Prakash, L., & Prakash, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503859102 · Cited by 71
Structural basis of error‐prone replication and stalling at a thymine base by human DNA polymerase ι
Kirouac, K. N., & Ling, H. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.122 · Cited by 71
“DNA replication by polι on template pyrimidines displays extremely high error rates, while incorporation opposite template purines is more accurate (Kunkel et al., 2003; Tissier et al., 2001; Tissier et al., 2000; Zhang et al., 2000).”
BackgroundResultInfluentialDNA polymerases and somatic hypermutation of immunoglobulin genes
Seki, M., Gearhart, P. J., & Wood, R. D. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400582 · Cited by 71
Longerich, S., Tanaka, A., Bozek, G., Nicolae, D. L., & Storb, U. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20051604 · Cited by 69
“Both have the highest error rates when copying T, leading to transitions from A (T) (41, 42).”
BackgroundExpression of error-prone polymerases in BL2 cells activated for Ig somatic hypermutation
Poltoratsky, V. P., Woo, C. J., Tippin, B. L., Martín, A., Goodman, M. F., & Scharff, M. D. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141222198 · Cited by 69
DNA polymerase iota and related Rad30–like enzymes
McDonald, J. P., Tissier, A., Frank, E. G., Iwai, S., Hanaoka, F., & Woodgate, R. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2000.0748 · Cited by 68
Self-citation
Metadata
- Authors
- Tissier, A., McDonald, J. P., Frank, E. G., & Woodgate, R.
- Affiliations
- National Institutes of Health (US)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2000-07-01
- Volume
- 14
- Issue
- 13
- Pages
- 1642-1650
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC316739
- OpenAlex
- W1908705633
- Cited by
- 315
- References
- 68
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 2 · 2023: 4 · 2022: 2 · 2021: 7 · 2020: 5 · 2019: 7 · 2018: 5 · 2017: 11 · 2016: 9 · 2015: 10 · 2014: 9 · 2013: 11 · 2012: 11
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- 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
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- DNA polymerase eta, error-prone DNA replication, xeroderma pigmentosum variant, Saccharomyces cerevisiae
- MeSH terms
- Base Sequence, DNA-Directed DNA Polymerase, Humans, Isoenzymes, Mutation, DNA Primers
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