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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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“Furthermore, mammals have another homolog of the yeast Rad30 protein (designated Pol i, Tissier et al., 2000) as well as a homolog of the E. coli DinB protein (designated Pol k, Ohashi et al., 2000).”
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“As a template DNA in its sequence contains all four bases including undamaged T, which Pol i favorably mispairs with ‘wooble’ G (28), Pol i was unable to efficiently elongate the running-start primer and reach the lesion (Figure 1C, lanes 6–8).”
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Polymerase iota - an odd sibling among Y family polymerases
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“…accuracy in nucleotide incorporation and increased rates of base substitutions and frameshifts, ranging from 10−3 to 10−1 errors per base pair (49, 56); propensity to incorporate nucleotides using aberrant DNA primer ends; absence of proofreading 3′→5′ exonuclease activity; and moderate -to-low…”
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Self-citationFilling gaps in translesion DNA synthesis in human cells
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“The fidelity of Pol is much poorer than that of Pol , particu- larly for incorporating nucleotides opposite the template pyrimidines (Johnson et al. 2000b; Tissier et al. 2000).”
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polι-dependent lesion bypass in vitro
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Self-citationMutagenic and Nonmutagenic Bypass of DNA Lesions byDrosophila DNA Polymerases dpolη and dpolι
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“Again, the data demonstrated that h Poli formed the base pairs of dG:dT and dA:dT with similar efficiency (11,44).”
BackgroundInfluentialChemical synthesis and translesion replication of a cis-syn cyclobutane thymine-uracil dimer
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“Human DNA polymerase iota (pol ι), a Y-family polymerase encoded by the POLI (RAD30B) gene, was shown to have TLS activity in 2000 [130].”
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Self-citationInaccurate DNA Synthesis in Cell Extracts of Yeast Producing Active Human DNA Polymerase Iota
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Maul, R. W., MacCarthy, T., Frank, E. G., Donigan, K. A., McLenigan, M. P., Yang, W. W., Saribasak, H., Huston, D., Lange, S. S., Woodgate, R., et al. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20151227 · Cited by 26
“Pol ι would also appear to be an attractive candidate for somatic hypermutation because of its very high misincorporation rate (Tissier et al., 2000).”
BackgroundInfluentialSelf-citationAnalyses of ultraviolet‐induced focus formation of hREV1 protein
Murakumo, Y., Mizutani, S., Yamaguchi, M., Ichihara, M., & Takahashi, M. (2006) · Genes to Cells · doi:10.1111/j.1365-2443.2006.00938.x · Cited by 26
Sez4 gene encoding an elongation subunit of DNA polymerase ζ is required for normal embryogenesis
Kajiwara, K., Wang, J. O., Sakurai, T., Yamashita, S., Tanaka, M., Sato, M., Tagawa, M., Sugaya, E., Nakamura, K., Nakao, K., et al. (2001) · Genes to Cells · doi:10.1046/j.1365-2443.2001.00410.x · Cited by 26
“In contrast, more recent studies demonstrated that the pol i encoded by another human homologue of yeast RAD30 can effect the error-prone bypass of UVinduced lesions (Tissier et al. 2000a,b; Zhang et al. 2000), probably together with pol z (Johnson et al. 2000).”
ResultBournique, E., Dall’Osto, M., Hoffmann, J., & Bergoglio, V. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.08.002 · Cited by 26
A strategy for the expression of recombinant proteins traditionally hard to purify
Frank, E. G., McDonald, J. P., Karata, K., Huston, D., & Woodgate, R. (2012) · Analytical Biochemistry · doi:10.1016/j.ab.2012.07.016 · Cited by 24
Self-citationParlanti, E., Fortini, P., Macpherson, P., Laval, J., & Dogliotti, E. (2002) · Oncogene · doi:10.1038/sj.onc.1205561 · Cited by 25
McVoy, M. A., & Nixon, D. E. (2005) · Journal of Virology · doi:10.1128/jvi.79.17.11115-11127.2005 · Cited by 24
“, polymerases , , , , and ) can be eliminated from consideration on the basis of their insensitivity to aphidicolin (23, 34, 37, 59, 64), PMEG and aphidicolin sensitivity do not serve to discriminate between damage repair and concatemer synthesis as potential roles for host DNA polymerases.”
BackgroundQuaternary structural diversity in eukaryotic DNA polymerases: monomeric to multimeric form
Acharya, N., Khandagale, P., Thakur, S., Sahu, J. K., & Utkalaja, B. G. (2020) · Current Genetics · doi:10.1007/s00294-020-01071-1 · Cited by 25
Replication across Template T/U by Human DNA Polymerase-ι
Jain, R., Nair, D. T., Johnson, R. E., Prakash, L., Prakash, S., & Aggarwal, A. K. (2009) · Structure · doi:10.1016/j.str.2009.04.011 · Cited by 22
“Compared to the purine templates, Polι is highly inefficient at incorporating the correct nucleotide A opposite template T; moreover, it incorporates a G opposite template T with an ~ 10-fold better catalytic efficiency than an A (Haracska et al., 2001; Johnson et al., 2000; Tissier et al., 2000; Washington et al., 20…”
BackgroundInfluentialSelective Modulation of DNA Polymerase Activity by Fixed‐Conformation Nucleoside Analogues
Eoff, R. L., McGrath, C. E., Maddukuri, L., Salamanca-Pinzon, S. G., Márquez, V. E., Marnett, L. J., Guengerich, F. P., & Egli, M. (2010) · Angewandte Chemie International Edition · doi:10.1002/anie.201003168 · Cited by 22
Dash, R. C., Ozen, Z., Rizzo, A. A., Lim, S., Korzhnev, D. M., & Hadden, M. K. (2018) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.8b00535 · Cited by 25
Louat, T., Servant, L., Rols, M., Bieth, A., Teissié, J., Hoffmann, J., & Cazaux, C. (2001) · PubMed · Cited by 22
Biochemical reconstitution of UV-induced mutational processes
Sugiyama, T., & Chen, Y. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz335 · Cited by 21
Su, Z., Gao, A., Li, X., Zou, S., He, C. S., Wu, J., Ding, W., & Zhou, J. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.706337 · Cited by 21
“Pol i (product of the POLI gene) was identified as the second homolog of yeast Rad30 gene in human (9).”
BackgroundHypoxia-inducible factor-1 mediates the expression of DNA polymerase ι in human tumor cells
Ito, A., Koshikawa, N., Mochizuki, S., Omura, K., & Takenaga, K. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.10.048 · Cited by 21
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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